Coevolution occurs when two (or more) species influence each other’s evolution. In this session, we look at coevolution in several diverse systems. Dr. McFall-Ngai begins with an overview of different types of symbiosis, including the important interactions between hosts and their beneficial microbes. Dr. Estes studies the coevolution of sea otters, sea urchins and kelp. Using historic records, he has been able to show the impact of human over-hunting of otters on an entire ecosystem. In the last video, Dr. Baldwin describes the amazingly intertwined lives of the Nicotiana attenuata plant and the Manduca sexta moth. In a fascinating twist, defensive toxins produced by the plant to prevent predation by the M. sexta caterpillar, may in fact protect the caterpillar from predation by a spider.
00:00:08.00 My name is Margaret McFall-Ngai
00:00:09.14 and I'm a professor
00:00:11.14 and the Director of the Pacific Biosciences Research Center,
00:00:13.14 School of Ocean and Earth Science and Technology,
00:00:16.07 the University of Hawaii at Manoa.
00:00:18.12 I'd like to start my lecture here
00:00:19.28 with thanking the iBiology team
00:00:21.22 for this opportunity to speak to you today
00:00:24.24 about the field of symbiosis.
00:00:27.12 So, the field of symbiosis is about living together
00:00:29.22 -- it's host-microbial interactions
00:00:32.15 that I will be talking about specifically today.
00:00:34.27 And there's a bit of a revolution in biology.
00:00:38.23 Symbiosis and host-microbial interactions
00:00:41.09 are taking center stage in biology.
00:00:46.11 And I'm going to talk to you today about why this is happening now
00:00:49.04 and exactly why we're sort of in the center of a revolution.
00:00:52.09 So, I'm going to start by talking about
00:00:54.20 the words that we use to describe symbiosis.
00:00:57.11 So, this person right here is
00:00:59.29 Heinrich Anton de Bary
00:01:02.16 and this particular person
00:01:04.25 lived in the 19th century,
00:01:07.04 and at the end of the 19th century
00:01:08.15 he coined the term symbiosis.
00:01:11.21 And the definition that he gave to this term
00:01:13.24 was the living together of unlike organisms.
00:01:16.23 And this particular definition of symbiosis
00:01:21.00 has remained with the field
00:01:22.19 until the present day
00:01:24.20 -- it's a very, very, very general way,
00:01:27.18 but very useful way
00:01:29.24 to think about this particular phenomenon in biology.
00:01:34.00 So, that said,
00:01:37.07 symbiosis is a bit of a catch-all term
00:01:39.05 with no information
00:01:40.19 concerning the effect of fitness.
00:01:42.22 So, what I'm showing up here is
00:01:45.06 I'm showing a very classic symbiosis
00:01:46.21 that a lot of people know of
00:01:49.28 and a lot of people think about,
00:01:51.18 and this is the symbiosis between
00:01:53.09 a clownfish and an anemone,
00:01:55.08 and they live together, persistently,
00:01:57.19 for much of their lives,
00:01:59.07 and it's a classic symbiosis
00:02:01.27 that you can think about.
00:02:03.00 But like I said, the word itself
00:02:05.05 confers no... no...
00:02:09.22 it's a catch-all word with no information
00:02:11.22 concerning the effect on the fitness
00:02:13.19 of either partner.
00:02:14.28 And so first I want to describe
00:02:17.18 what fitness means.
00:02:18.20 So, fitness is an individual's reproductive success,
00:02:23.10 and that is the number of offspring
00:02:25.10 that an individual leaves to the next generation.
00:02:28.06 And so let's think about this idea
00:02:32.14 in terms of symbiosis.
00:02:33.23 So, when we talk about fitness,
00:02:35.23 when we're talking about symbiosis,
00:02:37.14 I think there are...
00:02:39.02 I'm going to consider that there are two partners
00:02:41.03 -- there's symbiont #1 and symbiont #2 --
00:02:42.17 and in a mutualism,
00:02:44.25 which is one of the types of symbiosis,
00:02:46.17 both partners will benefit,
00:02:49.12 and what that means is that both partners
00:02:51.07 will have more in the successive generations
00:02:57.02 from being a partner with the other.
00:02:58.11 And so in the case of the clownfish
00:03:00.17 and the anemone,
00:03:02.03 the clownfish gets a very safe place to live,
00:03:04.07 because the tentacles of the anemone
00:03:06.03 are harmful to other animals;
00:03:07.20 the fish, the clownfish,
00:03:10.28 has learned ways to avoid the danger
00:03:13.08 of living in the tentacles of this anemone;
00:03:15.23 and the anemone gains from having the fish there
00:03:20.25 because the fish releases ammonia
00:03:22.17 that is taken up by the anemone
00:03:24.16 and it's used in the energy production
00:03:28.01 of the anemone.
00:03:30.27 So, this is a true mutualism.
00:03:32.24 The next type of symbiosis I'm going to consider is commensalism.
00:03:36.13 In a commensalism,
00:03:38.14 one partner benefits and one partner is unharmed
00:03:41.19 -- there's no change in the fitness,
00:03:43.25 no change in the reproductive fitness.
00:03:46.29 So, what I'm showing here
00:03:48.25 is another example and this example, here,
00:03:51.05 is the shark/pilot fish example,
00:03:54.21 and in this particular case
00:03:58.15 what happens is is
00:04:01.25 the shark is a messy eater
00:04:03.21 and he eats fish and all sorts of various things
00:04:07.11 and food is released around him
00:04:10.20 and the pilot fish that are associating with the shark
00:04:14.24 take advantage of the fact that the shark is a messy eater.
00:04:18.22 In this case, the pilot fish
00:04:22.01 gained from living with the shark,
00:04:23.12 but it seems to have no effect on the shark.
00:04:26.02 And so in this case, it's very likely that
00:04:28.07 the pilot fish will leave more to the next generation
00:04:30.07 from living with the shark,
00:04:32.10 but the shark...
00:04:34.05 it won't affect the shark's fitness whatsoever.
00:04:36.05 The third example that I'm going to give
00:04:38.28 is the example of parasitism.
00:04:40.26 So, these are the three major types of symbiosis,
00:04:42.27 and in parasitism what happens is
00:04:46.15 one partner benefits and one partner is harmed.
00:04:48.22 So, I'm showing down here a tree,
00:04:51.10 and this particular tree trunk
00:04:53.28 has a large gall on it,
00:04:56.07 and the large gall is present
00:04:59.19 because there is a pathogen that is living,
00:05:05.00 a microbial pathogen is living inside this gall
00:05:06.04 and has created this large gall on this tree.
00:05:11.00 Now, the pathogen, that microorganism that's living in that gall,
00:05:14.06 benefits from living...
00:05:15.23 from parasitizing this tree.
00:05:17.29 The tree on the other hand
00:05:19.25 is harmed by this association,
00:05:21.10 so this is a classic parasitism.
00:05:23.24 So, one of the things I should mention is that
00:05:26.05 as the field has grown,
00:05:27.26 there's a little bit of misuse of these terms,
00:05:32.04 and this is one of the reasons
00:05:34.11 why I wanted to bring this up.
00:05:35.25 The term commensalism
00:05:38.22 is often used by the biomedical community,
00:05:40.13 in my mind and the mind of a lot of people who study symbiosis,
00:05:45.07 And what they'll say is that
00:05:48.29 the microbes in your gut,
00:05:50.14 which I'm going to talk about a little bit...
00:05:51.24 the microbes in your gut are commensal,
00:05:54.11 and what this means is that
00:05:56.19 they have no effect on the host
00:05:58.24 -- they're benefiting but have no effect on the host.
00:06:01.14 But now we know that
00:06:03.29 they have a tremendous effect on the host
00:06:05.22 and are very often very important for our health,
00:06:10.01 and beneficial.
00:06:11.14 There are some in there that are likely commensal,
00:06:12.25 there are some in there that are likely
00:06:15.01 budding pathogens,
00:06:16.17 there are some in there that are likely,
00:06:18.00 or many in there, that are likely mutualists,
00:06:19.25 but we really can't categorize them,
00:06:22.14 so the very best thing to do in the instance
00:06:25.04 where you really don't understand
00:06:27.07 what type of symbiosis it is
00:06:29.19 is to just call it a symbiosis
00:06:31.19 and to call the partners a symbiont.
00:06:34.11 So, let's consider for a second
00:06:37.13 host-microbe symbioses.
00:06:38.29 So, what we're talking about is we're talking about
00:06:41.11 viruses, bacteria, protists
00:06:43.13 -- or single-celled eukaryotic cells --
00:06:45.02 and fungi, living with animals and plants, basically.
00:06:48.18 So, the question is,
00:06:51.02 is this a rarity?
00:06:52.21 And I have to say that when I started my career
00:06:54.09 working in this field,
00:06:56.23 back in the early 1980s,
00:06:58.12 this was considered a very unusual feature of symbiosis...
00:07:02.20 symbiosis was considered an unusual feature
00:07:04.19 in the biological world.
00:07:06.16 And in fact, if you look at a textbook,
00:07:09.03 even today,
00:07:11.00 you will see that symbiosis is covered,
00:07:13.16 but it's covered in only a few pages
00:07:15.10 of a 1200-page textbook.
00:07:17.13 It was and is today still considered a rarity,
00:07:20.15 but I hope you convince you that
00:07:23.00 it's not a rarity at all.
00:07:24.26 But why was it considered a rarity?
00:07:26.26 Well, we would find it...
00:07:28.29 historically, we were looking at
00:07:31.01 unusual situations in things like
00:07:34.14 the hydrothermal vent symbioses in the deep sea.
00:07:38.10 Down at 2000 meters, you know,
00:07:39.21 you see these smokers down at 2000 meters,
00:07:42.01 and these particular smokers
00:07:44.11 would have associated with them
00:07:46.16 these very large tube worms,
00:07:49.00 and these large tube worms
00:07:51.01 had in association with them,
00:07:53.29 bacteria, and these bacteria
00:07:55.28 allowed these particular tube worms
00:07:57.27 to live on the chemical energy
00:08:00.12 that was provided.
00:08:02.02 So that was a true symbiosis
00:08:04.16 that's been studied by lots and lots of people.
00:08:10.01 Bioluminescence is another kind of symbiosis
00:08:14.13 and very many organisms who are bioluminescent,
00:08:17.16 not all, but many organisms that are bioluminescent,
00:08:20.05 are bioluminescent because they harbor
00:08:22.18 luminous bacteria in association with the organism.
00:08:27.04 So, in the case of this anglerfish,
00:08:28.12 up here in the angle
00:08:30.15 is a pure culture of a particular bacterial species,
00:08:33.26 and that allows the anglerfish
00:08:36.21 to use that light in its predation.
00:08:40.09 And then, lastly,
00:08:42.10 I'm going to give the example of coral reefs.
00:08:44.24 Coral reefs would not form
00:08:47.04 if they did not have a very...
00:08:49.17 a mutualistic symbiosis
00:08:51.04 with a unicellular organism called
00:08:55.06 And these zooxanthellae live inside of the cells of corals
00:08:58.03 and they provide them with the photosynthate.
00:09:00.29 So, these zooxanthellae
00:09:06.03 are capable of photosynthesis
00:09:08.00 and they translocate the photosynthate to the host.
00:09:10.26 And so the zooxanthellae get a place to live
00:09:14.02 and the host coral is given the photosynthate,
00:09:18.27 and so they both benefit.
00:09:20.07 So, in all the cases I'm showing on this slide,
00:09:22.13 these are mutualistic symbioses,
00:09:24.26 and they're ones that have been
00:09:28.05 studied for over 100 years...
00:09:31.18 actually, not this one,
00:09:33.00 this one they discovered in the late 1970s,
00:09:34.10 but the many, many symbioses
00:09:36.07 that are mutualistic like this,
00:09:38.05 and kind of unusual,
00:09:39.21 have been studied for decades.
00:09:41.12 But now we're finding out that
00:09:43.13 nearly all animals and plants
00:09:45.20 are likely to have beneficial symbioses.
00:09:47.28 So, this is a whole new area,
00:09:51.27 this is a whole new finding,
00:09:53.17 and this new information
00:09:56.23 is from the last two decades of work.
00:09:58.29 And so I'm just showing
00:10:01.25 a whole array of animals
00:10:04.00 that are now known to have
00:10:05.27 beneficial symbioses with microbes.
00:10:10.29 So, I want to just take one minute
00:10:13.10 to pay tribute to what I...
00:10:15.22 the person who I consider
00:10:17.23 the mother of the field of symbiosis,
00:10:19.22 and this is Lynn Margulis.
00:10:21.07 And Lynn Margulis lived 1938-2011,
00:10:23.27 and she was the person
00:10:26.12 who felt that symbiosis was a major driver
00:10:28.17 in the evolution of animals and plants,
00:10:30.19 and she was always way ahead of her time.
00:10:33.20 She became famous f
00:10:35.19 or the endosymbiotic theory
00:10:38.11 of the origin of the eukaryotic cell,
00:10:39.17 and that is to say that bacteria
00:10:41.05 became symbiotic with other bacteria
00:10:43.03 and made a more complex cell.
00:10:45.14 And she showed that at the end of the 1970s,
00:10:50.06 it was very, very controversial,
00:10:52.00 she was way ahead of her time and always was,
00:10:54.09 but she is actually the person
00:10:57.07 who had the vision to say
00:11:00.19 exactly what we're seeing today,
00:11:02.04 and that is that symbiosis
00:11:04.02 is a major thing in biology
00:11:05.16 and has likely been over evolutionary history.
00:11:10.01 So, like I said, nearly all animals and plants
00:11:13.01 are likely to have beneficial symbiosis
00:11:16.05 and this is new information
00:11:18.12 from the last two decades of work.
00:11:20.12 And so what I'm showing here
00:11:22.27 is I'm showing a person,
00:11:24.09 and this person in this artistic rendering
00:11:27.18 is completely covered by microbes.
00:11:30.09 And we are, from the minute we're born,
00:11:34.00 through our life,
00:11:36.25 we associate very intimately with the microbial world.
00:11:39.06 And so we know now that you have as many, if not more,
00:11:42.25 microbial cells than human cells in your body.
00:11:45.04 So, you have about 10^13 human cells
00:11:47.08 and somewhere between 10^13 and 10^14 bacteria
00:11:50.00 that live with you, persistently,
00:11:52.26 your whole life and confer health.
00:11:57.06 So, the question is,
00:11:58.15 why didn't we know about this?
00:12:00.16 Why wasn't this more obvious?
00:12:03.07 Well, it turns out that there was
00:12:05.19 a huge technical problem
00:12:07.06 that we've been able to overcome.
00:12:09.05 And so, the technical problem
00:12:11.02 was a difficulty in identifying
00:12:14.15 and classifying the microorganisms,
00:12:15.17 and why we couldn't do that
00:12:17.15 was because most of these organisms
00:12:19.19 were unculturable under laboratory conditions,
00:12:22.19 and so they're called viable but nonculturable.
00:12:26.00 In other words, they live,
00:12:27.22 but we just can't bring them into the lab
00:12:29.28 and study them the way that we
00:12:33.13 would want to.
00:12:34.18 So, it's about less than 1% of the bacteria
00:12:38.15 that live in association with animals are culturable,
00:12:40.22 so this was a huge technical problem.
00:12:43.12 And so... because
00:12:45.17 we just couldn't know who they were.
00:12:47.10 The other thing was that...
00:12:50.15 another technical problem was that
00:12:53.12 they are relatively featureless.
00:12:55.12 So, what I'm showing here
00:12:57.17 is I'm showing a set of
00:13:00.12 different types of shapes and so on and so forth
00:13:02.27 that you might see
00:13:04.19 in different kinds of bacteria.
00:13:06.00 And so you might compare and contrast that
00:13:10.15 with the morphologies that you see of
00:13:13.09 very, very many plants and animals.
00:13:15.28 I mean, you can really, very well,
00:13:19.12 tell the differences between plants and animals;
00:13:21.21 with microbes, it's not so easy.
00:13:23.25 So, they weren't culturable
00:13:26.08 and you couldn't... they didn't...
00:13:27.26 they were pretty well featureless,
00:13:29.11 so these were big problems.
00:13:31.12 So, even though they're featureless,
00:13:33.06 we began to visualize microorganisms
00:13:36.03 back with Anton van Leeuwenhoek.
00:13:38.06 So, this is Anton van Leeuwenhoek
00:13:40.11 with, you know, several hundred years ago,
00:13:42.08 but he was a guy who
00:13:44.23 developed the very first microscopes,
00:13:47.06 and so he was the first person
00:13:49.26 who allowed us to visualize microorganisms.
00:13:51.16 And what Anton van Leeuwenhoek did was
00:13:54.15 he took a swab
00:13:56.19 and swabbed the inside of his cheek
00:13:58.10 and then he applied that to his microscope,
00:14:01.16 and he was able to see, for the first time,
00:14:06.23 So, not only was he the first person to see microorganisms,
00:14:08.21 but he was the first person to see microorganisms
00:14:10.26 that associate with humans,
00:14:12.08 and those were the microorganisms
00:14:14.16 inside of his own mouth.
00:14:17.07 So, then we fast-forward
00:14:19.29 to the electron microscope,
00:14:21.27 and the electron microscope
00:14:23.21 was invented several hundred years later,
00:14:25.21 in the late 1960s,
00:14:27.28 and the invention of the electron microscope
00:14:31.02 allowed us to see much more detail in microorganisms.
00:14:34.17 And this was actually the microscope
00:14:37.10 that allowed Lynn Margolis,
00:14:39.22 who I spoke about earlier,
00:14:41.06 to visualize the complexity of the eukaryotic cell
00:14:44.04 and to resolve the fact that,
00:14:46.12 in fact, the eukaryotic cell
00:14:49.07 was the result of a symbiotic association
00:14:51.22 between microorganisms,
00:14:54.22 or among microorganisms.
00:14:57.02 So, then fast-forward a little bit more...
00:15:01.22 so, these two characters,
00:15:04.26 Carl Woese and Norm Pace.
00:15:06.27 So, Carl and Norm were doing molecular biology
00:15:10.05 of microorganisms
00:15:11.20 at the University of Illinois...
00:15:13.22 well, Carl was at the University of Illinois
00:15:15.15 and he working with Norm Pace,
00:15:17.08 and they introduced the use of gene sequences
00:15:20.01 to determine relationships in the biological world.
00:15:22.08 So, notice that this is 1977,
00:15:25.04 so it's around the same sort of time that people
00:15:27.25 are beginning to think about using the microscope,
00:15:29.20 the electron microscope,
00:15:31.11 as a mechanism by which to classify the biological world,
00:15:34.26 but this was a new instrument
00:15:36.22 that Carl Woese and Norm Pace
00:15:38.24 introduced to the community of biologists.
00:15:42.08 So, the instrument was the 16S ribosomal RNA gene.
00:15:46.02 It's a highly conserved marker gene,
00:15:48.19 and the reason why this gene could be used
00:15:50.17 was because it's conserved throughout evolutionary history
00:15:53.12 and so it gives you an idea of
00:15:56.24 changes that are very, very old,
00:15:58.12 and would allow you to
00:16:00.21 classify all of the biosphere by molecular methods.
00:16:04.22 And this is the phylogenetic tree
00:16:07.26 that came as a result of the analysis
00:16:10.14 of the biological world.
00:16:12.07 And so what you'll see is you'll see that
00:16:16.15 there are the bacteria...
00:16:17.25 there are three domains of life
00:16:19.09 -- the bacteria, the archaea, and the eukaryea --
00:16:21.26 and the eukaryea contain
00:16:25.12 the animals, plants, and fungi.
00:16:27.09 And so, look at... the animals, plants, and fungi
00:16:30.12 are just these three twigs
00:16:32.03 at the very top of the tree of eukaryea,
00:16:35.21 which is, you know, is showing us that
00:16:39.02 the vast diversity of the biological world
00:16:41.13 is invested in the archaea and the bacteria.
00:16:44.27 So this was a huge change in our world view.
00:16:49.03 So, how big was this change?
00:16:51.20 Well, let's go all the way back to Aristotle.
00:16:56.07 So, Aristotle was one of the first people
00:16:58.08 to classify the biological world,
00:16:59.28 and what Aristotle did was
00:17:01.25 he classified it based on what he could see.
00:17:04.01 So it's animals and plants, basically.
00:17:08.18 So then, you know, fast-forward, as I mentioned,
00:17:11.09 to Anton van Leeuwenhoek,
00:17:13.03 who saw animals, plants, and what he called animalcules.
00:17:16.15 And then, in the 1970s,
00:17:20.20 there was a worker named...
00:17:24.24 who used the electron microscope,
00:17:26.14 his name was Thomas Whittaker,
00:17:27.23 and he developed something called the five kingdom model,
00:17:30.07 and so the five kingdom model
00:17:32.15 had sort of the featureless bacteria and archaea,
00:17:34.22 down here at the base,
00:17:36.11 the protists above that,
00:17:38.07 and those are the eukaryotic cells,
00:17:40.07 and then up at the top he had
00:17:42.24 the fungi, animals, and plants.
00:17:47.20 So, Carl Woese and Pace,
00:17:50.07 looking at this in context with their sequencing,
00:17:54.10 what they had was these three domains.
00:17:57.23 And remember that all, all of this,
00:18:02.05 up here at the top,
00:18:03.24 all of this stuff up here at the top
00:18:05.13 is now invested in this group here.
00:18:09.23 So, it's a huge change
00:18:11.23 in the way we see the biological world.
00:18:13.17 So, what have we done?
00:18:15.12 We have moved from having visual analysis...
00:18:19.02 for a couple thousand years,
00:18:21.22 we looked at the biological world
00:18:23.20 and we classified it based on what we could see,
00:18:27.00 and now what Carl Woese and Norm Pace did
00:18:30.27 was they gave us molecular analysis.
00:18:34.26 And molecular analysis is the... are the genes,
00:18:37.15 and that allowed us to very correctly
00:18:40.12 organize the biological world
00:18:43.23 as it actually exists.
00:18:45.23 So, what we found, of course,
00:18:47.06 is that the biological world
00:18:50.09 is mainly microbial,
00:18:52.11 and the animals, plants, and fungi
00:18:54.02 are but a small patina
00:18:57.07 on the top of the microbial world.
00:18:59.21 So, what did this revolution mean for symbiosis?
00:19:04.21 So, what it meant was that we could identify microbes
00:19:10.09 and determine their relationships,
00:19:12.21 among them and between them,
00:19:14.06 even those that we not culturable.
00:19:15.15 We could extract the DNA from them and say,
00:19:18.04 what is the DNA telling us about who they are and what they are doing?
00:19:21.13 But at first, with Carl Woese in the very, very beginning,
00:19:25.14 sequencing was excruciatingly slow and expensive.
00:19:29.20 And then, around 2006,
00:19:32.10 something called next-generation sequencing
00:19:35.05 came onto the scene,
00:19:36.21 and this has been
00:19:38.22 the most important thing of the whole revolution.
00:19:42.21 And imagine... this was only 10 years ago.
00:19:45.19 So, what happened at this point
00:19:47.29 was that there was a technology-enabled transformation
00:19:51.24 in our ability to sequence quickly and cheaply.
00:19:55.01 So, what I'm showing in this graph
00:19:57.05 is I'm showing the cost of sequencing per megabase...
00:20:02.18 so, you see, in 2001,
00:20:04.14 it was up at about 6000 dollars a megabase,
00:20:07.23 and it followed Moore's Law
00:20:10.03 -- the doubling in computer power every two years --
00:20:15.09 it followed Moore's Law for...
00:20:17.05 until about 2006, down here...
00:20:19.16 until about 2006,
00:20:21.25 and then next-gen sequencing was invented.
00:20:25.25 And look at what happened.
00:20:28.01 It went down from...
00:20:30.01 the cost went down from 600 dollars a megabase
00:20:32.06 to 35 cents in less than 10 years,
00:20:35.19 and now it's down to 3.5 cents.
00:20:38.13 And so this was incredibly enabling
00:20:41.05 to the community of biologists.
00:20:43.05 In other words, lots and lots and lots of people
00:20:45.23 had the resources
00:20:47.17 to be able to characterize the microbial world,
00:20:49.25 and so people have gone all around the world
00:20:53.18 characterizing the microbial world.
00:20:56.10 So, a whole frontier opens...
00:20:58.05 a whole frontier.
00:21:00.10 We can learn, who are the microbial partners
00:21:02.25 of animals and plants?
00:21:04.28 What are they doing?
00:21:06.11 How are they doing it?
00:21:07.18 And what is there importance to health and disease?
00:21:10.18 And so when you're thinking about a symbiosis
00:21:12.28 you think that many...
00:21:15.07 most of them are established new each generation.
00:21:17.19 Not all kinds are,
00:21:19.17 some of them the symbionts are passed
00:21:21.17 in or on the egg,
00:21:22.25 but most of them are established anew each generation,
00:21:25.14 just after birth.
00:21:27.02 And so when a baby is born,
00:21:28.27 what happens is at soon as
00:21:32.01 it goes through the mother's birth canal
00:21:34.12 it begins to acquire its microorganisms.
00:21:36.17 Then there's a development,
00:21:38.08 a trajectory that's not unlike
00:21:41.10 what goes on in the maturation of a forest
00:21:43.22 -- there's a succession of organisms --
00:21:46.05 and in humans you get
00:21:49.09 a mature set of microorganisms
00:21:51.01 somewhere between the ages of two and four.
00:21:53.26 And then what happens is you become a stable association,
00:21:55.29 that changes some over life
00:21:59.22 with various changes and aging and so on,
00:22:02.22 but it's a fairly stable population.
00:22:06.19 So there's a trajectory
00:22:08.00 and we're learning a great deal
00:22:10.16 about how all of this works at this point,
00:22:14.04 but it's new data...
00:22:15.23 I mean, it's just the beginning of the field.
00:22:18.01 What have we learned so far?
00:22:19.28 What we have learned so far is that
00:22:23.01 for many, many, many animals, including humans,
00:22:25.26 the complexity is absolutely daunting.
00:22:28.22 And what do I mean by that?
00:22:30.17 So, let's take humans for example.
00:22:32.12 So, what I'm showing here is I'm showing
00:22:34.11 my favorite comedian, Woody Allen,
00:22:36.09 and I've been very generous with him
00:22:39.25 -- I'm making him 6 feet tall
00:22:42.05 or a little bit over --
00:22:44.03 and so... but his,
00:22:46.14 if you compare the ratio is his size to a microbe's size,
00:22:48.26 2 meters to 2 microns,
00:22:50.22 so he's a lot bigger than a microorganism.
00:22:53.24 However, if you look at the number of genes
00:22:57.21 that Woody Allen has
00:23:00.19 compared to the number of genes that the microbes
00:23:02.18 associated with his body have,
00:23:04.05 the ratio is about 1:1.
00:23:07.18 If you look at cell number,
00:23:09.11 it's thought to be somewhere between 1:1 and 1:10.
00:23:13.11 In other words, there are about 10 times as many
00:23:15.29 microbes associated with you,
00:23:17.12 and that number has just this last year
00:23:20.11 become a little bit controversial,
00:23:21.24 so it's somewhere between here and here,
00:23:24.00 but that is to say that there are
00:23:26.25 just as many microbes associated with you
00:23:28.12 as you have human cells.
00:23:30.01 Then, if you look at gene diversity,
00:23:32.25 because instead of just...
00:23:34.09 so, you know, all of your eukaryotic...
00:23:36.14 all the human cells are of a single genome,
00:23:39.04 but the microbial cells are of
00:23:42.01 thousands, or hundreds if not thousands, of genomes.
00:23:46.07 The difference in gene diversity is thought...
00:23:48.22 for every single human gene
00:23:50.09 there are 200 genes of microbes,
00:23:53.11 so the gene diversity of microorganisms
00:23:55.09 is very much greater.
00:23:57.18 So at this point Woody Allen
00:23:59.22 feels pretty insignificant.
00:24:01.28 What I'm showing here is I'm showing the power of animal model systems
00:24:04.06 for the study of complex characters,
00:24:06.01 and the example that I'm using
00:24:08.07 is developmental biology.
00:24:09.23 And in development biology,
00:24:11.18 what I'm showing here is I'm showing
00:24:13.11 a fertilized egg,
00:24:15.22 and that fertilized egg goes from 1 cell to 10^13 cells
00:24:18.23 and produces something like
00:24:21.02 the miracle of George Clooney, my favorite actor.
00:24:23.14 So, this has been, this has been...
00:24:28.13 this approach has been extremely successful
00:24:30.18 to understand developmental biology.
00:24:34.10 So, what we've been able to do
00:24:36.29 is to take model systems,
00:24:38.15 you know, experiments that evolution has done,
00:24:40.14 and ask how, in this simple model system,
00:24:43.14 a particular developmental phenomenon
00:24:47.11 has been solved.
00:24:49.09 And so what I'm showing is
00:24:51.16 I'm showing an array of model systems
00:24:53.12 and I'm showing ones in which
00:24:55.27 Nobel Prizes have been awarded,
00:24:57.16 and it turns out that 6 Nobel Prizes
00:24:59.28 in developmental biology
00:25:01.14 have been awarded since 1995 and 2007,
00:25:04.06 and all 6 of them went to
00:25:07.24 individuals working on models.
00:25:09.09 So models have been an extremely valuable way
00:25:12.28 to study very complex characters.
00:25:15.09 So, because symbiosis
00:25:17.23 is such a complex character,
00:25:19.18 we feel, those of us in the field
00:25:22.03 who study models,
00:25:23.27 feel that it's a really good way to try to understand symbiotic associations.
00:25:28.10 So, we are developing,
00:25:30.02 the field is developing some models for symbiosis,
00:25:32.17 we're exploiting nature's toolkit
00:25:34.18 and, as I said,
00:25:36.22 evolution has done some enlightening experiments.
00:25:39.17 So what I'm showing here is I'm showing
00:25:41.27 a variety of them,
00:25:43.06 and so there are
00:25:45.05 various nematode symbioses
00:25:47.01 and various other invertebrate symbioses,
00:25:51.19 and we even have, over at UC Berkeley,
00:25:54.19 Nicole King studying the choanoflagellate symbioses,
00:25:58.13 at the base...
00:26:00.05 thought to be the base of the animal kingdom.
00:26:02.26 And then up here some vertebrate models.
00:26:06.05 Now, the vertebrates,
00:26:07.24 all the vertebrates have complex associations,
00:26:09.29 they have large consortia associated with them,
00:26:13.10 and so these people studying over here
00:26:15.10 are really interested in studying germ-free animals,
00:26:18.17 and so I sort of look at them as
00:26:20.21 engineered models.
00:26:22.10 Over here, many of them are studying
00:26:24.19 natural models
00:26:26.16 and these, the invertebrates are
00:26:28.21 naturally very simple associations,
00:26:33.01 and so they lend themselves to looking at a natural situation
00:26:35.12 and how that...
00:26:37.12 how the bacterium and the host animal get together
00:26:40.22 and maintain a stable association.
00:26:43.22 So, I...
00:26:46.17 my lab works on this beautiful animal, here,
00:26:48.24 the bob tail squid.
00:26:51.14 This is not a giant's hand, this is my technician's hand.
00:26:54.08 A very small squid that's indigenous
00:26:56.21 to the Hawaiian archipelago,
00:26:58.25 and this is the symbiosis that I've been working on
00:27:02.10 and that I would like to tell you about
00:27:04.10 in my next lecture.
00:27:07.02 Thank you very much.
00:00:07.25 I'm Jared Leadbetter
00:00:09.08 and I'm at the California Institute of Technology.
00:00:12.07 And, for some 24 years now,
00:00:14.14 my research has sought to clarify the relationship
00:00:16.26 between termites and their hindgut microbes.
00:00:19.21 Now, of particular interest to me
00:00:22.22 is the metabolism of hydrogen
00:00:24.20 that is generated during this fermentation of wood,
00:00:27.11 but today I want to give you a broad overview
00:00:30.17 on microbial diversity
00:00:33.08 and on some of the essentials
00:00:35.22 of termite hindgut microbiology.
00:00:38.26 So, I want to talk about
00:00:41.07 biological diversity in general,
00:00:43.14 because many who are interested in biology
00:00:45.17 are missing, actually, some of the
00:00:48.21 full diversity that we see in the microbial world.
00:00:52.01 And, then I also want to comment about
00:00:54.15 how some of this diversity is surprisingly abundant
00:00:56.28 in certain areas of the world,
00:00:58.23 and that we must understand
00:01:01.11 what that diversity does and how it functions.
00:01:03.03 So, this will bring me to termites
00:01:05.17 and the symbiosis they form with their hindgut microbes,
00:01:08.14 and I want to introduce you to several major groups
00:01:11.10 of termite hindgut microbes,
00:01:13.17 the cellulose decomposing protozoa,
00:01:17.01 methane producing archaea,
00:01:18.27 and a group of abundant and unusual bacterial
00:01:21.27 called spirochetes.
00:01:24.12 I'm going to then touch on
00:01:26.26 how we can study different termites
00:01:29.06 and learn about different events that may have occurred
00:01:31.19 during this symbiosis in the past,
00:01:33.22 and then I'll give you some conclusions.
00:01:39.02 I wonder how many people who are watching this
00:01:41.11 have grown up thinking about three kingdoms.
00:01:45.10 Up until the 1960s,
00:01:47.01 I think most people grew up thinking
00:01:50.17 that there were animals, plants, and fungi,
00:01:52.24 and that maybe, depending on their education,
00:01:55.27 even up through current years,
00:01:59.22 most enthusiasts of biology
00:02:02.11 understood there to be between three and five kingdoms.
00:02:05.07 Maybe you had the bacteria as a fourth
00:02:08.29 and the protists as a fifth,
00:02:13.04 But, starting in the 1960s we had a revolution
00:02:16.25 in the study of the relationships between different organisms,
00:02:19.10 and started to realize that many things that we were seeing,
00:02:22.06 and also not seeing,
00:02:24.13 are very, very different from these three major groups.
00:02:27.12 So, for example, if you look at a key gene
00:02:30.10 that is present in all known organisms,
00:02:33.00 you can make comparisons between this gene
00:02:36.13 and from that infer
00:02:38.24 how those organisms are related to each other.
00:02:41.16 The thing I want to point out on this slide
00:02:44.13 is that you have the fungi
00:02:46.02 and the animals
00:02:48.02 and the plants,
00:02:50.16 and those are just three twigs on a branch
00:02:53.27 that has many other twigs.
00:02:58.10 If those three twigs and the length of those lines
00:03:01.11 denote evolutionary relationships,
00:03:04.27 then there are more than three kingdoms.
00:03:07.25 There are easily a half-dozen.
00:03:10.20 The other thing I want to point out here
00:03:13.04 is that if you think about "plant metabolism"
00:03:16.11 there are some organisms on this tree
00:03:19.14 which also carry out photosynthesis,
00:03:23.13 let's say the kelp or the red seaweed,
00:03:28.09 but those branches are actually
00:03:31.11 very different from the plants.
00:03:32.28 They are as distantly related to plants
00:03:35.08 as you and I are from plants,
00:03:37.15 and I think that's very important.
00:03:39.12 Also, when we talk about single-celled eukaryotes, like protozoa,
00:03:43.11 we realize, oh,
00:03:46.17 Paramecium and the protozoan Babesia
00:03:49.08 are actually two very different organisms,
00:03:51.21 again, as distantly related to each other
00:03:54.14 as we are from let's say the yeast
00:03:57.01 that you use to make beer and bread.
00:04:03.11 So, the number of kingdoms
00:04:08.16 or major divisions of life
00:04:11.01 already gets more complex than those three that we know.
00:04:15.13 The truth is actually much more complex than that,
00:04:17.22 because this is now just a snippet
00:04:20.27 of a branch of a much more complex tree.
00:04:23.19 You'll see that I have just blown up
00:04:26.14 this section of a much larger tree.
00:04:29.27 One of the things I want to point out on this slide
00:04:32.18 is that there are many, many branches on this,
00:04:34.22 easily 100
00:04:37.18 which are more distant from each other
00:04:40.22 than the distance between corn and animals,
00:04:44.12 and what that suggests, then,
00:04:46.13 is that we have a lot to learn about
00:04:51.24 the differences between these different groups.
00:04:53.28 So, for instance, everything
00:04:56.12 that is lying outside of this circle is a microbe,
00:05:00.02 the single-celled organisms
00:05:01.19 which are smaller than you can see with your naked eye.
00:05:04.11 So, for as much as we can appreciate biological diversity
00:05:06.19 that you can see,
00:05:08.17 the true diversity of life
00:05:10.22 is beyond the resolution of the human eye
00:05:12.12 and we have to use other methods to really
00:05:14.02 understand how it works.
00:05:16.14 The second thing I want to point out
00:05:18.23 is how different the way of living is
00:05:22.15 for corn, or a plant,
00:05:24.20 and ourselves,
00:05:27.05 or from a yeast that's used to make bread and beer.
00:05:29.28 If the length of those lines,
00:05:31.25 which is comparatively short,
00:05:33.28 and the differences of these organisms is so great,
00:05:38.06 imagine the possible differences
00:05:41.13 in the ways that these organisms live.
00:05:44.08 So, we are potentially really missing out,
00:05:46.28 not just on the diversity
00:05:49.17 in terms of how things are related,
00:05:51.16 but also missing out on the diversity
00:05:53.25 of what organisms are actually doing in the environment.
00:05:56.10 And so, if we're to understand the environment,
00:05:58.16 we really have to learn more about
00:06:00.22 what these other organisms are doing.
00:06:04.27 Let's come back to this tree.
00:06:07.06 Let's come back to this organism kelp.
00:06:09.23 I want to illustrate another point:
00:06:11.25 it's not just that there are many, many organisms out there
00:06:14.25 which are different from the organisms we're most familiar with,
00:06:17.04 but in some environments those organisms are present
00:06:21.15 and very, very abundant.
00:06:23.14 Take the kelp -
00:06:25.29 you can find kelp forests off the coast of California,
00:06:29.02 and those kelp are performing
00:06:31.21 what we might call "plant metabolism".
00:06:33.25 So, they are the primary producers in those environments,
00:06:36.06 but, keep in mind, they're not plants.
00:06:39.03 So, the story of these coastal ecosystems
00:06:43.03 is in a large part driven
00:06:45.12 by an organism that's very different from a plant,
00:06:47.20 and so if we want to understand those coastal ecosystems
00:06:50.10 part of the story is understanding
00:06:53.02 the biology of kelp
00:06:54.20 and understanding in what ways they are similar
00:06:57.03 and different to the terrestrial,
00:06:59.05 or land plants that we study.
00:07:03.24 Now, I want to shift from the oceans
00:07:06.02 to my own research, which is study on
00:07:08.25 termites and their hindgut microbes,
00:07:11.00 and I want to point out that the termite hindgut
00:07:14.02 is an environment.
00:07:16.02 It happens to be an environment that lives
00:07:18.17 in a small insect,
00:07:20.15 but we can compare and contrast that environment
00:07:22.16 with, for instance,
00:07:24.24 a very rich marine environment like the Sargasso Sea.
00:07:28.03 There are certain reasons why
00:07:30.16 you might want to study a small environment
00:07:31.14 like in a termite.
00:07:33.00 The Sargasso Sea is a wonderful and amazing place,
00:07:34.28 and very important to study, but it's a thousand kilometers across,
00:07:38.07 and there's only one of the them.
00:07:41.03 The termite hindgut is only about one cubic millimeter in volume,
00:07:46.01 and yet it contains hundreds and hundreds
00:07:48.13 of microbes that you find no where else in nature.
00:07:51.08 Just if you were to take the top millimeter
00:07:53.14 of the Sargasso Sea,
00:07:55.22 the volume of that across those thousands of kilometers
00:07:59.19 is 19 orders of magnitude greater
00:08:01.27 than the volume of that one termite.
00:08:03.21 So, we can actually bring a termite into the laboratory
00:08:05.28 and be able to study an entire environment.
00:08:09.25 The hindgut... it's tiny yet complex...
00:08:12.18 many hundreds of species
00:08:14.20 and some of those species are yet unstudied,
00:08:17.13 so it is still bewildering complex,
00:08:20.11 and it's well-bounded.
00:08:22.12 We know that the gut lining
00:08:23.00 and the outside of the termite
00:08:24.27 are where you might define the boundaries of that system.
00:08:27.26 The Sargasso Sea is wonderful,
00:08:29.25 but there's only one of them,
00:08:31.29 and its boundaries are a little bit user-defined.
00:08:34.03 We think that it's, you know,
00:08:35.23 the currents that are intersecting here and there
00:08:37.25 are what bound that region,
00:08:39.13 whereas in the insect it's very well-bounded.
00:08:42.00 And, of course, the termite is available
00:08:44.09 in large number of replicates,
00:08:46.04 so we can, in a laboratory,
00:08:48.22 have that one environment that's tiny and well-bounded
00:08:51.10 replicated in termite, after termite, after termite.
00:08:54.13 So, we can start to do some comparative studies
00:08:56.08 and perturbation studies
00:08:58.07 which are just not possible with a large environment
00:09:00.25 like the Sargasso Sea,
00:09:02.13 for which there's only one.
00:09:07.06 So, I study a very particular termite
00:09:09.14 that we find in ponderosa pine
00:09:11.18 that's fallen in the Angeles National Forest
00:09:14.02 of southern California,
00:09:15.19 and here is one of these ponderosa pines
00:09:18.10 and two of my former students,
00:09:20.25 who have peeled off some of the bark from this log,
00:09:22.28 which has been on the ground for probably five or ten years,
00:09:25.15 and if you look a little bit more closely
00:09:27.24 you can see that just on the underside of that bark
00:09:29.18 are a number of termites
00:09:31.19 of different, what we call, morphological castes.
00:09:34.02 These ones with the dark mandibles are actually soldiers.
00:09:36.29 Rather than eating wood,
00:09:38.21 they have big mandibles that they can use to attack,
00:09:41.01 for instance, another termite or an invading ant.
00:09:45.22 So, this is termite that we study, for the most part,
00:09:49.01 in my laboratory.
00:09:50.18 It's the Dampwood Termite, Zootermopsis nevadensis,
00:09:54.17 and it's about a centimeter in length.
00:09:56.09 It's one of the larger termites that you'll find on Earth.
00:09:58.27 Now, this is what we call a worker,
00:10:02.24 and from another specimen I've extracted the hindgut tract,
00:10:07.29 and that is shown here.
00:10:10.18 And, what you'll observe is that
00:10:13.17 there is a long tubular region,
00:10:15.18 which is somewhat analogous to our small intestine,
00:10:18.24 and then you have this hindgut paunch,
00:10:22.10 which is somewhat analogous
00:10:25.07 to our large intestine,
00:10:27.02 and it's in this paunch
00:10:29.22 that really you find a lot of things that excite microbiologists.
00:10:33.04 You find a density of microbes
00:10:35.08 you find nowhere else in nature,
00:10:37.12 and they represent all three domains of life.
00:10:40.04 Earlier on that slide,
00:10:42.06 I'd shown you that the tree of life,
00:10:44.16 where you actually have three major subgroups,
00:10:47.05 and those are the archaea,
00:10:49.00 the bacteria,
00:10:50.19 and the eukaryotes.
00:10:52.09 You find single-celled relatives of all three of those groups,
00:10:56.06 comprising hundreds of species,
00:10:58.07 in this hindgut paunch.
00:11:00.19 So, before I tell you about termite gut microbes,
00:11:03.04 I want to tell you a little bit more about termites.
00:11:05.17 There are about 3000 species of termites on Earth.
00:11:10.24 Termites are related to cockroaches
00:11:13.24 and to the mantids, like the praying mantis,
00:11:15.19 and they're actually, although insects,
00:11:18.05 quite distantly related to ants, wasps, and bees,
00:11:22.02 which are also social.
00:11:24.06 So, this is an example of where
00:11:27.06 society, or sociality in insects,
00:11:29.12 has arisen in two different groups of insects
00:11:31.08 which are very different from each other.
00:11:33.19 So, termites, and those 3,000 species of them,
00:11:37.07 can be subgrouped into several different families,
00:11:41.11 and their closest relative in the insect world
00:11:45.04 is what we call the Wood Roach,
00:11:47.04 which is a non-social but wood-feeing insect
00:11:49.22 that you find in the Carolinas
00:11:52.19 and the Pacific Northwest
00:11:54.22 and in parts of China.
00:11:56.26 And, many of the microbiology...
00:12:00.02 the features of the microbiology in the Wood Roach
00:12:02.22 are actually shared with the termites,
00:12:06.13 and so it's thought that many of the
00:12:09.07 microbial processes that arose
00:12:11.28 arose in the last common ancestor of this roach and termites.
00:12:16.08 Now, the termite that I study, Zootermopsis,
00:12:19.07 belongs to this one groups in the Termopsidae.
00:12:21.22 So, over time, we can start to ask,
00:12:24.12 are any of the patterns that we see here
00:12:27.18 present in some of these other groups?
00:12:31.09 Now, if you extract the gut from Zootermopsis,
00:12:34.03 or another termite,
00:12:36.08 and you take a cross-section through that gut,
00:12:38.20 what you'll see is that the insect tissue itself
00:12:40.25 is actually very, very thin.
00:12:43.05 It's only about 10 microns in diameter,
00:12:46.05 so 1% of a millimeter in thickness.
00:12:49.14 The bulk volume of that is comprised by the gut contents,
00:12:53.10 and what you see here, these larger objects,
00:12:56.05 are single-celled eukaryotes called protozoa.
00:12:59.20 Now, historically, until the mid-1990s,
00:13:03.01 this region, this environment
00:13:05.17 was thought to be completely anoxic,
00:13:07.23 so, devoid of oxygen.
00:13:09.20 Many of the microbes that you find
00:13:11.18 in the core regions of this gut are poisoned by oxygen.
00:13:16.21 Here you have this insect,
00:13:18.08 which is living in the aerobic world
00:13:20.09 and wandering around on its six legs
00:13:23.00 in a piece of wood or on a piece of wood,
00:13:27.15 containing microbes which are poisoned by oxygen.
00:13:31.09 The story is actually even more complex,
00:13:33.13 because it turns out,
00:13:35.13 through studies that were performed
00:13:37.05 by Andreas Brune and John Breznak in the mid-1990s,
00:13:40.19 the oxygen actually diffuses across the insect gut wall
00:13:45.03 and then is consumed by biological processes
00:13:48.07 in the periphery of that hindgut,
00:13:50.28 and it's those biological processes in the periphery
00:13:54.07 which lead to the lack of oxygen in the core,
00:13:56.20 which protects some of those oxygen-sensitive microorganisms.
00:14:00.29 So, not only do you find organisms
00:14:03.03 which are unique to the termite gut habitat,
00:14:06.01 that you find nowhere else on Earth,
00:14:07.28 but many of these are poisoned by oxygen
00:14:10.04 and are very sensitive to desiccation.
00:14:12.29 So, their life outside the termite is very, very limited.
00:14:18.20 So, what you have
00:14:22.01 are microbes that are very dependent on their host
00:14:24.14 and, because of their processes,
00:14:26.10 which allow the host to derive nutrition from wood,
00:14:29.10 makes the host very dependent on their microbes.
00:14:33.25 And, when a termite emerges from its egg,
00:14:37.01 it doesn't have these microbes in its gut.
00:14:39.01 It's fed those microbes by other of its littermates
00:14:43.02 or by its parents,
00:14:45.06 and if those microbes don't take hold
00:14:48.04 that termite will fail,
00:14:51.21 and if that termite fails
00:14:54.25 those microbes will also fail.
00:14:57.15 So, when we look at one termite
00:14:59.14 that's walking around on a piece of wood today,
00:15:02.05 we are looking at over 100 million years
00:15:04.26 of having this microbial community
00:15:07.16 passed from one termite to the next termite to the next termite,
00:15:11.14 generation to generation to generation.
00:15:14.04 It's quite a remarkable story
00:15:17.04 of a journey that's been taken
00:15:19.04 between many, many organisms together.
00:15:22.26 So, if we go and look at a little bit of a higher magnification
00:15:26.08 of what's inside the gut,
00:15:29.13 this is what we call a DIC image
00:15:34.04 using a microscope
00:15:36.02 of some of the larger protozoal cells.
00:15:37.29 These are about 60 microns in length,
00:15:40.23 so roughly 20 of these laid end to end to end
00:15:43.27 would be a millimeter of length,
00:15:46.05 and some of these are the primary agents
00:15:48.08 of wood degradation in this termite.
00:15:50.02 You also see some smaller cells
00:15:52.26 which are also protozoa.
00:15:55.13 So, these are single-celled eukaryotes,
00:15:58.26 of which there are about a dozen
00:16:00.27 in this one termite
00:16:02.23 that you find nowhere else in nature,
00:16:04.14 and their closest relatives are in other termites.
00:16:08.04 There are some interesting associations
00:16:10.03 that you find between these protozoa and certain bacteria.
00:16:13.23 For instance, if you look at the surface of one of these,
00:16:16.15 at higher magnification,
00:16:18.11 you'll see that those protozoa
00:16:19.28 are covered with long lines of grooves,
00:16:23.03 and in those grooves you see these little black objects?
00:16:26.15 Those are bacteria.
00:16:29.09 So, the surface of that single cell of eukaryote
00:16:32.23 is arrayed with a very regular group
00:16:36.16 of a very specific bacterium
00:16:39.19 and, without knowing much more about,
00:16:42.07 the notion you might have is that
00:16:44.19 there is something that that protozoan
00:16:47.01 is getting from that bacterium and vice versa.
00:16:50.22 So, there are associations between the microbes
00:16:52.29 that live in the gut,
00:16:54.23 and there are associations with those microbes and their host.
00:16:58.04 So, there are many levels of biological interactions
00:17:00.06 which are occurring in this environment.
00:17:03.03 Another example of a protozoan that has a bacterial association
00:17:10.16 is this organism, which is called Streblomastix strix.
00:17:13.22 The eukaryote, the single-celled protozoan,
00:17:17.10 is actually very, very slender
00:17:19.04 and running through the center of this.
00:17:21.06 That protozoan is covered with a blanket, or a coat,
00:17:25.06 of long, thin bacterial cells
00:17:28.07 that are creating those ridges that you see.
00:17:31.05 We know very little about the interaction
00:17:33.06 between this protozoan and the bacteria
00:17:35.09 and what they're doing for each other,
00:17:37.22 but clearly it's a very specific and interesting interaction.
00:17:42.06 There are many cases of protozoa
00:17:44.27 and the bacteria that occur in these environments,
00:17:47.11 of which we have much more to learn in the future.
00:17:52.04 Now, there's an opening line to a book
00:17:54.26 by the biophysicist Howard Berg.
00:17:57.20 His book is called "Random Walks in Biology",
00:18:00.23 and the opening lines
00:18:03.11 are that biology is wet and dynamic.
00:18:06.10 What does that mean?
00:18:08.01 I've just showed you these still pictures,
00:18:10.02 but I think that the still pictures
00:18:12.12 don't do this environment justice.
00:18:14.25 Really, when you're looking at this environment live,
00:18:17.24 this is now some of that gut fluid
00:18:19.23 which has been diluted.
00:18:21.19 It's even more densely packed than this inside the termite,
00:18:24.02 but if you dilute that fluid and put it on a microscope slide
00:18:26.22 you see some of these protozoa
00:18:29.15 and coursing unamongst them,
00:18:31.15 lots of bacteria which are moving so quickly
00:18:33.22 you can barely focus on them.
00:18:36.12 I can just look at this forever,
00:18:38.26 and you can look at it using different types of microscopy
00:18:43.02 to show different details on some of these cells.
00:18:46.02 The point here is that
00:18:48.11 when I go to work every morning
00:18:50.04 I go to work in what I call a miniature Alice in Wonderland.
00:18:52.23 That it is, just from a naturalist's standpoint,
00:18:55.13 a very wonderful and diverse place
00:18:58.00 that begs lots of questions.
00:19:01.27 So, what is the interaction
00:19:03.29 that termites have with their gut microbes?
00:19:07.10 I want to give you an overview
00:19:09.08 of some of the major things
00:19:11.15 that we've learned over about the last 100 years
00:19:14.00 on the association between
00:19:16.19 the insect and its gut microbes.
00:19:19.00 Now, microbes have a huge challenge in life.
00:19:21.26 The challenge is, how do you eat something
00:19:24.02 larger than your head?
00:19:26.06 If you are the size of
00:19:29.18 one thousandths of a millimeter,
00:19:32.02 how do you gain access to nutrients
00:19:34.19 in a 2x4 or in a big log?
00:19:37.12 So, you have a really wonderful association
00:19:40.01 with an insect that has jaws and grinding mandibles,
00:19:43.12 which are very, very hard,
00:19:45.01 that can then take a large block of wood
00:19:47.09 and grind it into really small particles,
00:19:50.07 and then bring them into the gut
00:19:52.03 in a very controlled and wonderful environment
00:19:54.08 in which these microbes can thrive.
00:19:56.22 Now, in the hindgut, these protozoa that I showed you
00:20:01.03 have enzymes of their own,
00:20:03.02 and enzymes that they recruit from the insect,
00:20:05.14 to start breaking down the polysaccharides in wood...
00:20:08.18 the cellulose and another component
00:20:10.23 which we call xylan or the hemicellulose...
00:20:14.18 and these protozoa perform a very unusual fermentation.
00:20:17.22 It's a fermentation that differs
00:20:20.00 from the one that you use to make sauerkraut
00:20:22.02 or that you use to make beer and wine.
00:20:25.00 What those protozoa do
00:20:27.02 is they break down the hexoses in cellulose,
00:20:29.28 primarily to acetate,
00:20:32.00 so, neutralized vinegar,
00:20:35.05 and that acetate builds up in the hindgut of the termite
00:20:37.22 and is absorbed by the insect.
00:20:39.29 So, the insect is actually absorbing the acetate
00:20:43.21 and using it as its biofuel.
00:20:46.01 It is the source of carbon for the insect
00:20:48.19 and the source of energy for the insect.
00:20:53.00 Now, those protozoa
00:20:55.07 also produce hydrogen gas,
00:20:57.21 so think the 1930s,
00:20:59.27 this classic picture of the Hindenburg blimp
00:21:01.26 over New Jersey, blowing up in fire.
00:21:04.10 It was filled with hydrogen.
00:21:06.01 There's a lot of energy in hydrogen.
00:21:07.21 It's not just combustible;
00:21:09.24 it's an energy source that can be used by different microorganisms.
00:21:13.04 So, in the termite,
00:21:15.10 and in many environments which are non-marine
00:21:17.16 and devoid of oxygen,
00:21:19.17 hydrogen and CO2 is converted into methane
00:21:23.08 by a group of organisms called methanogenic archaea,
00:21:26.29 and this methane is emitted by the insect.
00:21:30.00 It is sort of lost calories.
00:21:31.24 So, as we know, we can burn methane,
00:21:33.24 we use it as a fuel,
00:21:35.24 and that methane which is emitted by the insect, then,
00:21:38.22 is a fuel, a potential energy source,
00:21:40.21 which is lost from the system.
00:21:43.07 So, we can use a form of microscopy
00:21:46.07 to observe these methanogenic archaea in the termite.
00:21:50.07 Several years ago, I was trying to find out,
00:21:54.07 where are those archaea present in the system?
00:21:56.09 And what I learned is that
00:21:59.06 they are colonizing the gut wall of many...
00:22:03.21 inside the gut wall of many termites.
00:22:05.18 So, if you dissect out the gut,
00:22:07.29 you cut open the gut, you wash away all the contents,
00:22:11.05 and you sort of open that up
00:22:13.00 and look at the internal surface of it,
00:22:15.09 you can look for a type of fluorescence
00:22:19.08 called F420 fluorescence.
00:22:21.20 These organisms that make methane contain a vitamin,
00:22:24.04 and when you shine UV light on that vitamin
00:22:26.13 the vitamin turns blue.
00:22:28.16 And so, with a proper microscope,
00:22:30.29 you can start to see a number of different cell types,
00:22:33.18 which are blue,
00:22:35.18 that live on the inside of this gut wall.
00:22:38.12 And, in this image you see that there are
00:22:40.13 three different morphologies of organisms.
00:22:42.10 Now, I'm somebody who likes food,
00:22:43.28 so I like to say that this one long one
00:22:45.29 looks like long, blue spaghetti,
00:22:47.25 the curves rods look like basmati rice,
00:22:49.28 and some of these straight rods look like regular rice.
00:22:53.06 Now, termites emit up to 4% of global methane every year.
00:22:57.03 So, by studying these organisms in their environment,
00:23:00.00 and also culturing them and bringing them into the lab,
00:23:02.18 we can put a face on the process,
00:23:06.00 at a single microbial cell level,
00:23:08.19 for actually a very significant source of global methane...
00:23:12.17 not the most significant source of global methane,
00:23:15.25 but a small but significant source.
00:23:19.28 I like to show this slide,
00:23:23.01 of a paper mache cow,
00:23:25.01 because I knew that when I first got to Caltech
00:23:27.00 I was having some impact on undergraduate life there,
00:23:30.02 because when I talked about termites
00:23:32.22 and processes that occur in a cow
00:23:34.22 the next Caltech Ditch Day,
00:23:36.26 that occurs every spring,
00:23:39.06 the students had made this large paper mache cow
00:23:41.17 and filled it with chocolate pudding,
00:23:44.08 Easter grass, oatmeal,
00:23:47.06 and Easter eggs that were filled with clues
00:23:49.12 on where the students should go to their next puzzle.
00:23:53.21 And, you can see here,
00:23:55.23 the students trying to find those eggs.
00:23:57.28 The point I want to make here is that
00:24:01.11 cows lose about 20% of their electrons in their food
00:24:05.05 as methane.
00:24:07.06 It's a huge waste of energy.
00:24:09.09 And, although termites contain methanogens,
00:24:11.19 and emit methane,
00:24:13.25 it's only a very small amount of this hydrogen and CO2
00:24:16.25 that is lost to the system as methane.
00:24:19.11 On a global scale, it's significant,
00:24:21.22 but, actually, on a global scale,
00:24:23.22 the methane emission by termites
00:24:25.09 would be much more significant
00:24:28.03 if this hydrogen and CO2 was not being consumed
00:24:30.21 by a different group of organisms
00:24:33.14 which we call CO2-reducing homoacetogens.
00:24:36.17 So, many termites contain microbes
00:24:38.28 that completely push these methane organisms
00:24:41.19 out of the picture,
00:24:43.22 or push 90% of them out of the picture.
00:24:47.11 So, many termites will take...
00:24:49.20 have microbes that convert hydrogen and CO2 into acetate,
00:24:52.19 and this acetate then goes into that pool in the gut
00:24:56.05 and is absorbed by the insect.
00:24:58.10 So, up to a third to a fifth
00:25:01.01 of the acetate which is used as the biofuel
00:25:03.22 by these insects
00:25:05.27 is derived from carbon dioxide and hydrogen
00:25:09.02 by way of the activity of those protozoa,
00:25:11.11 and by way of the activity
00:25:14.00 of these organisms here.
00:25:16.02 So, I have long been interested
00:25:18.00 in the interaction between organisms competing
00:25:20.24 for this hydrogen and CO2
00:25:22.26 that make acetate and that make methane
00:25:25.26 from those...
00:25:28.02 to understand how they compete with each other,
00:25:30.01 how has this process come to pass in termites,
00:25:33.25 why doesn't it occur in the cow rumen,
00:25:35.29 and how do these hydrogen consumers
00:25:38.06 interact with the organisms which are producing the hydrogen,
00:25:40.18 the protozoa.
00:25:44.16 So, CO2-reductive acetogenesis
00:25:47.20 is a bacterial activity.
00:25:51.27 The process involves
00:25:54.13 the fixation of two molecules of carbon dioxide...
00:25:58.11 one, two...
00:26:00.26 with four molecules of hydrogen...
00:26:03.20 one, two, three, four...
00:26:08.09 and in the process, those two carbons are joined
00:26:11.07 and reduced to form the acetate,
00:26:13.15 and this metabolism
00:26:15.28 actually yields energy for the bacteria
00:26:17.24 which are performing it,
00:26:19.22 in addition to yielding the acetate
00:26:21.10 which can be used by the insect.
00:26:22.10 So, it's a mutually beneficial metabolism
00:26:26.08 that takes hydrogen produced during this fermentation,
00:26:28.18 turns it into additional fuel for the insect,
00:26:30.25 meanwhile supporting the activity of the bacteria that perform it.
00:26:35.22 But, for years,
00:26:37.19 we did not have a very good understanding
00:26:40.03 about what bacteria in the termite
00:26:42.19 are actually catalyzing this process.
00:26:44.09 We had some ideas, but, over the years,
00:26:47.06 we've been trying to learn more.
00:26:49.10 Now, if you look in the hindguts of termites
00:26:51.23 you'll even see, on some of these protozoa,
00:26:55.05 that there are very abundant spiral-shaped organisms,
00:26:57.24 which can be attached to the protozoa
00:26:59.28 and that can also be seen
00:27:03.10 living and swimming amongst the protozoa,
00:27:06.03 and in most termites these organisms we call spirochetes
00:27:09.10 are some of the more abundant bacteria
00:27:11.11 that you'll see swimming in and amongst these protozoa.
00:27:14.28 If you go to another portion of the gut,
00:27:17.09 maybe you'll see that there are even more
00:27:19.14 of these spiral-shaped organisms.
00:27:21.13 So, starting in the 1990s,
00:27:23.17 scientists at Michigan State and in Germany
00:27:27.02 discovered that these spirochetes
00:27:29.19 are actually very closely related to Treponema pallidum.
00:27:33.28 That's one of the most famous organisms in microbiology.
00:27:37.03 It's what causes syphilis.
00:27:39.11 Actually, all these bacteria in the termite
00:27:42.16 are species that belong to the same genus
00:27:46.13 as the agent of syphilis,
00:27:48.13 and yet you always find these organisms
00:27:51.12 present in happy and healthy termites.
00:27:53.28 But we didn't know what they did because, like syphilis,
00:27:57.13 they had never been cultured in vitro.
00:27:59.28 First observed in the 1860s,
00:28:01.21 over a century went by
00:28:03.26 before we had actually learned about what any of these do,
00:28:06.07 and I would still argue that we are still in our infancy
00:28:09.04 of understanding what the full breadth of the different roles
00:28:11.25 of the hundred or more species of spirochetes
00:28:14.12 that you can see in an individual termite hindgut.
00:28:18.21 But, a number of years ago,
00:28:20.27 I really endeavored for a very long period of time
00:28:23.04 to try to coax one or two of these species
00:28:26.11 into laboratory culture so that we could ask what they do,
00:28:29.12 and I had an idea:
00:28:31.19 maybe some of these are these acetogens
00:28:33.12 that can take hydrogen and CO2
00:28:35.07 and make acetate.
00:28:37.01 The problem with that is that activity
00:28:39.05 was not known to occur in any spirochete,
00:28:42.08 and none of these spirochetes from the termite
00:28:44.07 had been cultured.
00:28:46.01 So, it's an idea, but what you really need to do
00:28:47.24 is get one of these into the laboratory and ask it,
00:28:50.22 are you capable of doing that?
00:28:52.08 And, if not, what do you do?
00:28:55.20 So, what is a spirochete?
00:28:57.25 This is a political cartoon from the early 70s,
00:29:00.29 and will sort of shoot right over the heads
00:29:04.02 of almost all of us,
00:29:05.27 but I still include it because it's a little bit
00:29:08.21 of American history that Richard Nixon's first vice president,
00:29:11.23 Spiro T. Agnew,
00:29:14.15 sort of had to leave office for some misdealings that he had,
00:29:19.16 and this was before even the Watergate scandal blew up.
00:29:22.25 So, when I say spirochete,
00:29:24.26 I'm not talking about a spirochete,
00:29:27.21 but a different organism,
00:29:30.15 and these are bacteria
00:29:33.17 that have a very unusual body plan.
00:29:35.28 So, many bacteria can swim
00:29:38.04 and they have flagella that extend into the extracellular milieu
00:29:42.10 and act like propellers,
00:29:44.25 but spirochetes have flagella
00:29:46.17 that extend not out of the cell,
00:29:49.14 but out past the first membrane,
00:29:52.21 but lie in between the inner and the outer membrane
00:29:55.03 of the bacterial cell,
00:29:58.27 and actually will wrap around the cell, okay?
00:30:02.12 If you look at a cross-section, you can see what I mean.
00:30:05.24 These are the flagella that lie
00:30:08.06 in between the inner and the outer membrane,
00:30:10.04 and when those flagella turn
00:30:12.05 the entire cell becomes a propeller,
00:30:14.12 as opposed to being attached to the propeller,
00:30:17.01 and spirochetes are known to be able to move
00:30:19.11 into very thick, viscous environments,
00:30:22.02 and are sort of the world record holders in the microbial world
00:30:25.07 for being able to wiggle into really thick and tight places.
00:30:29.12 And, all the organisms that have this body plan
00:30:31.10 are also related to each other,
00:30:33.09 so it's both a related group
00:30:35.19 by genetics and by their body plan.
00:30:40.01 So, these are microscopic images
00:30:42.06 of the first termite gut spirochete that was isolated.
00:30:45.29 We call this organism Treponema primitia,
00:30:49.01 and the first thing we wanted to ask
00:30:51.21 was whether it was really a spirochete,
00:30:54.06 and what I want to point out here is that
00:30:56.09 if you look at it with a whole-cell negative stain
00:30:58.05 by transmission electron microscopy,
00:31:00.05 or a thin section,
00:31:02.02 it has these hallmark flagella
00:31:05.18 that are lying in between the inner and the outer membrane.
00:31:08.23 Now, the second thing we learned about Treponema primitia
00:31:11.28 is that it is actually a hydrogen+CO2 acetogen.
00:31:15.11 Hydrogen stimulated its growth
00:31:18.01 and it consumed hydrogen and made acetate
00:31:21.18 in the expected four hydrogen to one acetate stoichiometry.
00:31:25.26 You could also grow this organism
00:31:27.27 under radioactive carbon dioxide,
00:31:29.29 and when you do that
00:31:32.07 it generates radioactive acetate,
00:31:34.21 so it's fixing CO2 into organic carbon,
00:31:39.02 and when you ask,
00:31:41.19 are both carbon positions of acetate labeled?
00:31:44.14 They were.
00:31:46.10 And lastly, there are enzymes associated with this pathway,
00:31:49.17 and this organism exhibits them all.
00:31:52.03 So, it is a bonafide hydrogen/CO2 acetogen
00:31:55.12 and, although a close relative
00:31:57.07 of the organism that causes syphilis,
00:31:59.08 this organism actually plays a key role
00:32:01.17 in the fermentation of food in the termite,
00:32:04.03 and in taking some nutritional value of that wood
00:32:07.04 and passing it back on to the termite.
00:32:10.06 Now, we have been studying this organism
00:32:12.22 for almost 20 years now,
00:32:14.21 and one of the things that we've done
00:32:16.28 is really looked at its genes for this pathway,
00:32:19.10 and used our study of these genes, in red,
00:32:23.15 to do comparative studies in other termites
00:32:26.07 and also in this particular termite and ask,
00:32:29.29 can we learn if this is the only acetogen,
00:32:33.18 or if there are other species,
00:32:35.13 and who are those other species?
00:32:37.25 So, we can take an approach, now,
00:32:39.28 where we can take a look at the diversity
00:32:42.16 of these genes for this pathway in this one termite,
00:32:45.23 but also in members of these two other major subgroups
00:32:48.29 of the termite line of descent,
00:32:51.11 and also in the Wood Roach.
00:32:53.11 And so, we've been learning a lot
00:32:55.16 about the diversity of organisms
00:32:57.18 that can carry out that metabolism
00:32:59.24 in a diversity of different species
00:33:02.25 and actually major subgroupings of insects that eat wood.
00:33:07.25 Now, we've also been able
00:33:11.29 to isolate a second spirochete from Zootermopsis.
00:33:15.04 This one we call Treponema azotonutricium.
00:33:18.28 Now, this organism
00:33:21.06 plays a very different role in the symbiosis
00:33:23.08 with the termite and its hindgut microbes.
00:33:26.01 So, if you think about it,
00:33:28.02 wood is not only tough to eat,
00:33:30.23 it's not a very good source of protein.
00:33:33.10 You know, at best, it's like a potato, right?
00:33:36.29 It's got a lot of polysaccharide,
00:33:38.23 a lot of carbs,
00:33:40.25 but not a lot of nitrogen.
00:33:43.00 So, you can be degrading that wood
00:33:45.06 and providing the calories to the host,
00:33:48.01 but that's only one of the hosts major problems in life.
00:33:50.26 The other problem is to make protein,
00:33:54.04 and so if you ask what's going to
00:33:56.08 limit the ability of this insect that's eating a block of wood,
00:33:58.27 or your home,
00:34:00.25 what's going to limit its proliferation,
00:34:03.15 part of the story is on protein.
00:34:06.10 So, it turns out that some 35 years ago
00:34:10.06 John Breznak, at Michigan State University,
00:34:13.10 discovered that termites contain microbes
00:34:15.25 that can take atmospheric nitrogen,
00:34:17.25 which is bathing all of us in the atmosphere all around us,
00:34:21.01 and can take that and turn it into protein,
00:34:24.09 that can then be fed to the insect.
00:34:27.18 And, this particular spirochete,
00:34:29.26 when we got it into culture in the laboratory,
00:34:32.19 we could show can do that same activity.
00:34:35.28 So, this is one of the organisms that we say
00:34:38.17 can exhibit diazotrophic growth.
00:34:40.18 It can grow with N2 gas
00:34:43.11 as its sole source of eventual protein,
00:34:46.08 and it shows several activities
00:34:48.17 which are associated with that activity,
00:34:51.04 and therefore it's playing a role
00:34:53.13 in taking a very abundant but unusable source of nitrogen
00:34:56.01 around the insect
00:34:57.25 and actually feeding the insect protein-level nitrogen.
00:35:01.29 I'll mention too that this particular organism
00:35:04.29 is unlike the first.
00:35:06.24 It's not an organism that can consume hydrogen
00:35:10.20 and fix CO2 into acetate.
00:35:13.07 It actually degrades sugars
00:35:15.14 and produces hydrogen that it can feed to the other spirochete.
00:35:18.19 So, it plays different roles in this symbiosis.
00:35:23.05 So, I've talked to you about some protozoa,
00:35:28.13 about some methanogenic archaea,
00:35:32.20 and about just some of the many, many bacteria
00:35:35.09 that you can find in a termite.
00:35:38.02 There are many other stories I could tell you,
00:35:40.05 but I want to leave off with my talk
00:35:41.27 by just pointing out that
00:35:46.06 we've talked about these three major groups in this environment.
00:35:49.15 That environment is dominated
00:35:51.11 by members of diverse groups
00:35:53.11 which are very different from the host itself.
00:35:55.28 So, just like the kelp forests,
00:35:57.23 these are environments
00:35:59.28 which are dominated by genetic groups
00:36:02.01 and groups performing physiologies
00:36:03.26 which are very different from sort of the paradigms of biology,
00:36:07.01 and that we learn a lot by studying them.
00:36:09.27 So, I think with that,
00:36:11.15 I'll close this introductory talk
00:36:14.08 on termite gut microbiology.
00:36:16.15 There are many, many general aspects
00:36:18.14 that we could discuss,
00:36:20.00 and of course can go into many other aspects
00:36:22.08 in great detail.
00:36:23.20 And so, I'd like to point out that
00:36:25.28 there have been many research groups and scientists
00:36:28.07 that have been working on termites for well over a century,
00:36:30.25 and I've tried to encapsulate some of their findings,
00:36:33.00 as well as the findings of my own laboratory,
00:36:35.21 into the presentation that I have given you today.
00:36:38.16 Thank you very much.
00:07.2 My name is Jim Estes,
00:09.2 I am a professor of ecology and evolutionary biology
00:11.1 at the University of California in Santa Cruz,
00:13.1 and I'm very happy to be here today
00:16.0 to be talking to you about the ecological function
00:19.0 of apex predators in nature.
00:20.2 In Part I of my lecture,
00:22.2 I provided a conceptual foundation
00:24.2 for what the questions are
00:26.2 and how we have gone about trying to answer those questions.
00:28.3 In Part II, I'm going to give you
00:30.3 a particular case study.
00:32.1 I'm going to focus on sea otters and kelp forests,
00:34.1 and I'm doing this because
00:37.3 this is work that my lab been engaged in
00:39.2 for the last several decades.
00:43.1 So, this is an outline for Part II of the lecture.
00:46.1 Firstly, I'm going to explain or describe to you
00:50.1 the food webs, the key species.
00:52.1 Second, I'm going to tell you a little bit about the approach
00:55.0 that we have used to understanding the importance
00:58.1 of sea otters in these kelp forests ecosystems.
01:00.2 And then, lastly, I'm going to run through some of the findings
01:02.2 from the work that we have done.
01:05.2 The food web: sea otters are the apex predator
01:09.0 in many coastal kelp forest ecosystems
01:11.1 in the North Pacific.
01:13.3 Sea otters feed on sea urchins;
01:15.1 sea urchins feed on kelp;
01:17.0 kelp is what we call a foundation species,
01:18.3 that is, many other species in the ecosystem depend upon it,
01:22.0 either for habitat or for food or for primary production,
01:25.3 so many other species are linked into the ecosystem
01:28.3 by way of the kelps themselves.
01:32.0 The approach:
01:34.0 how have we gone about trying to understand
01:35.2 the importance of sea otters
01:37.1 in these coastal kelp forest ecosystems?
01:39.2 It's actually very simple.
01:41.1 We have used history as
01:44.2 a large natural experiment.
01:46.1 So, the blue line in this illustration
01:48.3 shows the range over which sea otters
01:51.2 historically have occurred in the North Pacific Ocean.
01:54.1 They were abundant across that range
01:57.1 until about the mid-1700s.
02:00.0 In the mid-1700s, the Pacific Maritime Fur Trade began
02:05.1 with the discovery of the New World by the Russians
02:08.1 and the discovery of vast fur resources,
02:11.1 and in particular sea otter resources, across the North Pacific,
02:13.2 and that began a long period of overexploitation
02:17.3 and extinction of sea otters throughout most of their range.
02:23.1 This illustrates the nature of the Pacific Maritime Fur Trade
02:27.1 and emphasizes that the Pacific Maritime Fur Trade
02:30.2 was the perturbation that we have used
02:33.0 to understand dynamic processes in this system.
02:36.2 The blue line is shown again on this slide,
02:38.3 that shows the historical range of sea otters,
02:41.0 and the little red dots are the locations
02:43.2 of known surviving colonies at the end of the fur trade,
02:48.1 which was over in the early part of the 20th century.
02:51.1 At the beginning of the fur trade,
02:53.0 there were probably at least a million sea otters
02:55.1 across the North Pacific Ocean, possibly many more.
03:00.2 By the end of the fur trade, there were well under a thousand,
03:03.1 and those few remaining animals occurred
03:06.1 in a couple of isolated colonies.
03:08.0 These colonies were protected by international treaty in 1912, 1913,
03:15.1 right around that time,
03:17.0 and they began to recover.
03:18.3 Subsequently, animals were taken from these recovered colonies
03:21.1 and they were relocated to other parts of the historical range
03:25.0 in an effort to repatriate the species
03:28.1 throughout its natural environment,
03:29.2 and that's shown by the green dots, here.
03:31.2 So, the red dots and the green dots
03:33.2 represent places that otters have been reintroduced,
03:36.1 and all of the places in between
03:38.2 are places where they once occurred but no longer did occur.
03:43.0 All we have done is simply compare the places where they occur
03:46.0 with the places that they don't occur,
03:47.3 and we have watched places that have become recolonized
03:50.2 and how those ecosystems have changed
03:53.0 as otter numbers have built up through time.
03:56.1 These are the locations where the work has been done:
03:58.3 the Aleutian archipelago,
04:00.2 Southeast Alaska and Vancouver Island,
04:03.1 and, as I mentioned before,
04:06.0 simply, what we have done, very simply,
04:08.0 is look at areas with and without sea otters within these large areas
04:11.2 and we have contrasted places through time
04:13.1 as the abundance of otters have waxed and waned.
04:17.2 So, what are the findings?
04:21.2 Very simply, if you look at places where otters are abundant,
04:24.1 what you see are abundant kelps
04:27.1 and relatively few sea urchins,
04:28.2 and if you go to nearby places where otters
04:31.0 once were abundant but are now gone,
04:32.2 you see abundant sea urchins and virtually no kelps,
04:36.1 as shown on the right here.
04:37.3 Amchitka island... these photographs were taken in the early 1970s...
04:41.3 Amchitka island was a place where otter populations
04:44.1 had recovered to what we think was their natural historical abundance.
04:47.1 Shemya island, which is several hundred miles
04:50.2 to the west of Amchitka island...
04:53.0 otters were exterminated on Shemya
04:54.3 and they had not repatriated or recovered on Shemya
04:58.0 at the time that these photographs were taken.
04:59.2 So, you can see visually here, very clearly and simply,
05:02.2 what the differences are between a system
05:05.2 with and without sea otters.
05:07.2 So, what's going on here?
05:08.2 What is going on here is what ecologists call
05:11.0 a trophic cascade.
05:12.1 That is, otters are having a top-down limiting effect on urchins,
05:16.1 urchins are having a top-down limiting effect on kelps.
05:20.2 By adding otters into the system,
05:22.3 it removes the urchins or reduces the urchins,
05:25.0 thus releasing the kelps from control by urchins,
05:29.0 so we have, in a system with otters, abundant kelp,
05:33.0 and we have, in a system without otters, abundant urchins
05:35.2 and relatively few kelps.
05:39.2 So, that's it, but what are some of the broader implications of this?
05:43.1 Well, the broader effects of this,
05:46.0 as I'm going to tell you about today,
05:48.1 largely spin off kelps and what happens
05:51.1 when we have systems with and without the kelp forests,
05:53.1 and I'm going to tell you about
05:55.2 three or four little vignettes of effects
05:58.1 that spin off of this trophic cascade
06:01.0 that are what we call indirect effects of the trophic cascade.
06:03.2 I'm going to tell you about how that is manifested in the abundance of fish.
06:07.0 I'm going to tell you about how it is manifested
06:10.1 in the behavior of various other consumers.
06:14.2 I'm going to tell you about how it influences
06:17.1 what we call the primary production of the coastal system.
06:21.0 And I'm going to tell you how that feeds back,
06:22.3 or has an influence,
06:24.2 on the physical environment through the sequestration of carbon dioxide
06:28.2 through the process of photosynthesis.
06:33.0 These are some data from a study
06:35.1 that my colleagues and I conducted several decades ago
06:38.3 in which we took baby mussels --
06:43.0 mussels are what we call filter feeders,
06:44.3 and these are young mussels
06:47.1 that were grown out at Friday Harbors Labs,
06:49.0 the University of Washington,
06:50.2 translocated to the Aleutian Islands,
06:52.1 and outplanted to islands with and without sea otters,
06:55.2 and thus to islands with and without abundant kelp forests.
06:57.2 And what you can see here is
07:00.1 the difference in growth rate over a one-year period,
07:02.3 the dark bar showing the growth rate
07:06.2 of these filter feeders in places where otters were abundant
07:08.3 and the light grey bar showing
07:11.2 comparable growth rates and comparable habitats
07:13.1 where otters are absent,
07:15.0 and what you can see from this is the growth rates of these filter feeders
07:17.1 are about twice as high where otters are abundant
07:20.0 compared with where they're absent.
07:22.1 Why is that?
07:23.1 It's simply because the primary production,
07:25.0 the abundance of autotrophs, these photosynthesizing kelps,
07:27.3 is much higher in systems with otters
07:30.0 than in systems without otters,
07:31.3 and therefore this consumer, the mussel in this case,
07:34.2 that is eating material
07:37.1 that is being provided by the primary producers,
07:39.2 grows more rapidly where sea otters are abundant compared with where they're absent.
07:43.2 These are data on the abundance of fish,
07:45.2 again, the dark bar showing information
07:48.1 from where sea otters are abundant,
07:50.1 the light bar showing comparable information
07:52.0 from places where they're absent,
07:53.3 and what you see from this is that
07:56.0 the measures that we have of fish abundance
07:58.1 indicate that they're almost an order of magnitude greater
08:01.0 where otters are abundant compared with where they're absent.
08:03.2 So, simply because these animals depend upon kelp
08:07.0 for habitat and food,
08:09.1 kelp is more abundant where otters are more abundant,
08:10.2 and thus fish are more abundant where otters are more abundant.
08:14.0 These are some data on the diet of
08:18.1 another species of consumer in these coastal ecosystems.
08:20.1 In this particular case,
08:21.2 a seagull, Glacous-winged Gull,
08:23.2 and let me just explain a little bit about what the data show.
08:27.0 In this particular panel, what I'm showing you is
08:30.1 the relative proportion of fish versus invertebrates
08:34.0 in the gulls' diet
08:36.0 between places where otters are abundant,
08:37.3 those are the black data, the black bars,
08:41.0 and places where otters are absent,
08:43.2 those are the light bars, the grey bars.
08:45.1 And what you can see is that when otters are abundant
08:47.3 these gulls feed almost entirely on fish;
08:49.2 when otters are lost from the system
08:52.0 they forgo feeding on fish to feed on the now more abundant invertebrates.
08:57.1 These are some comparable data
08:59.2 on the diet of another consumer in the system,
09:01.1 in this particular case, the bald eagle.
09:03.1 And what you can see here again,
09:05.1 by looking at places with and without otters,
09:07.1 is that eagles eat a roughly even mix of
09:11.2 marine mammals, seabirds, and fish
09:14.2 when otters are abundant,
09:15.3 and when otters are lost from the system
09:17.2 the proportion of marine mammals
09:20.1 and the proportion of fish in their diet goes down,
09:21.3 and the abundance of seabirds goes way up.
09:24.0 So, the overall composition of the major things that they feed on
09:28.1 is linked to the effects of sea otters on this coastal ecosystem.
09:32.2 Lastly, I want to tell you a little bit about
09:36.0 some recent work that we've done on the potential sequestration effect
09:39.0 of this trophic cascade,
09:40.2 that is, the enhancement of primary producers by sea otters,
09:43.3 on atmospheric carbon dioxide.
09:46.0 And why would we think that to be an interesting thing to look at?
09:49.1 Because carbon dioxide is the material that fuels photosynthesis.
09:52.3 If you have a plant species in the system that's more abundant,
09:57.1 one might expect that the rate of photosynthesis
09:58.3 is going to be higher,
10:00.2 and therefore the drawdown of carbon dioxide from the environment
10:03.3 and the surrounding oceans is going to be greater.
10:05.2 So, when we look at this, we find that in fact
10:08.1 the sea otter effect is substantial,
10:10.1 that sea otters are responsible...
10:13.2 a system with sea otters will draw down
10:16.0 about 10% of the overlying carbon dioxide in the atmosphere,
10:19.3 compared to a system without sea otters.
10:22.1 Or, if we put this in a slightly different context
10:24.2 and asked the question,
10:26.2 how much of the increase in atmospheric carbon dioxide
10:29.2 that has followed the onset of the industrial revolution
10:33.1 might this accommodate?
10:36.1 It's about half.
10:38.1 We can put this into dollar terms,
10:40.2 because carbon is something that's been valued
10:43.1 on what we carbon exchanges or carbon markets,
10:45.2 and when we do that, and these data are based on
10:48.1 the value of carbon in the European carbon market
10:51.3 as of 2012,
10:53.2 we see that, in the areas that I've been working,
10:56.2 the standing biomass effect of sea otters on kelp
11:00.1 is potentially worth somewhere between 200 and 400 million dollars.
11:04.1 And the potential sequestration effect of that,
11:07.2 that is, the amount of that carbon that's being put into the bank,
11:10.3 and in this case the bank is the deep sea...
11:13.1 carbon is translocated in some cases to the deep sea...
11:16.2 depending upon how much of that carbon that's fixed by the kelp
11:21.1 goes into the deep sea,
11:23.1 that value may range anywhere up to almost a billion dollars.
11:27.2 So, now I want to change gears
11:29.2 and talk about evolutionary consequences of these species interactions,
11:32.3 and why would I do that?
11:34.1 Because evolution is a consequence of natural selection,
11:37.3 and natural selection is going to be affected by
11:42.2 the strength of interspecies interactions,
11:44.1 and we see strong species interactions in this system
11:46.3 that are a consequence of these apex predators,
11:49.1 in this particular case a sea otter.
11:53.1 So, I'm going to focus on one particular part of this trophic cascade
11:56.2 that I've told you about,
11:58.2 and that is the interaction between the herbivores and the plants,
12:01.1 and how is it that sea otters may have influenced
12:04.2 the evolutionary dynamics between these herbivores and plants.
12:09.2 We can see from this illustration,
12:11.2 and from what I've told you before,
12:13.2 that in systems with sea otters
12:16.2 the strength of the interaction between the herbivores,
12:18.2 that is the sea urchins in this case,
12:21.2 and the kelps is going to be very weak,
12:24.2 and when otters are lost from the system
12:27.2 the strength of that interaction is going to increase substantially.
12:30.2 So, how might we approach the question of,
12:33.1 what were the evolutionary consequences of this interaction?
12:36.1 The way my colleagues and I have done this
12:38.2 is simply by looking elsewhere in the world,
12:40.3 where there is a kelp forest that evolved in the absence of sea otters,
12:44.2 so we chose to do this in the
12:48.0 southwestern temperate Pacific
12:51.1 in the area of Australia and New Zealand,
12:53.1 which has a very physically similar system to the North Pacific
12:56.2 in that it's a cold water system that has fleshy macroalgae
12:59.1 that are very similar to kelps,
13:00.3 but it lacks a predator on the sea urchins in that system,
13:04.2 and the other grazers, like sea otters.
13:07.2 So, the first thing that my colleagues and I did
13:11.1 to try to get some sense of the changes in the strength
13:13.3 of plant-herbivore interactions between these various systems
13:17.3 is that we measured the rate of tissue loss
13:21.2 in fleshy macroalgae on the sea floor to herbivory,
13:24.3 and the way that we did this was we simply took a kelp plant,
13:27.1 we put it on the sea floor,
13:29.0 we stuck another kelp plant next to it in a cage
13:31.2 from which the herbivores were excluded,
13:33.1 and we contrasted the rate of tissue loss over 24 hours
13:37.2 between these experimental and control,
13:40.1 caged and uncaged, treatments.
13:42.2 The data that you see here are the relative differences
13:45.3 between grazing intensity in different parts of the world.
13:48.1 So, on the very far right
13:51.0 you'll see data from Shemya Island,
13:53.1 which I told you before is a place where otters are absent in the North Pacific,
13:57.1 and what you can see there is that the rate of grazing,
13:59.2 as indicated by the black bar, is very high.
14:03.1 If you go over to the far left-hand side of this graph,
14:07.1 what you will see are comparable data done from the exact same sort of experimental protocol
14:11.1 at Amchitka Island, where otters are abundant,
14:13.3 and there what you see is that the intensity of grazing
14:16.2 is virtually zero.
14:18.3 And then if you go to Australia or New Zealand,
14:21.0 in this particular case these are data from
14:23.2 four different marine reserves in New Zealand,
14:26.1 what you see is something that was very exciting to us,
14:28.1 and that is that the intensity of grazing
14:32.1 is much less than it is in systems
14:35.0 where sea otters are absent in the North Pacific,
14:36.2 but much higher than it is in systems
14:40.0 where sea otters are present in the North Pacific.
14:42.0 In other words, the intensity of herbivory
14:44.1 in these southern hemisphere kelp forest systems
14:46.2 is clearly higher than it is in natural systems in the North Pacific,
14:50.1 where sea otters are present.
14:52.1 That led us to believe that there would be
14:55.1 some sort of coevolutionary response in the dynamics
14:58.2 between the herbivores and the plants in this system.
15:02.2 What might we expect to see as a consequence of that?
15:05.1 Well, we knew going into this that
15:08.0 the most likely way in which marine plants
15:10.3 are able to defend themselves,
15:12.2 or the most well-known way in which marine plants are known to defend themselves against herbivores,
15:17.3 is through chemical defenses.
15:19.2 And in the case of brown algae,
15:22.0 the kelps and the things that are related to them,
15:24.0 the common group of compounds that does this
15:27.1 are compounds called phlorotannins,
15:29.0 and I've drawn the molecular structure here of one of those phlorotannins.
15:33.2 There are many other molecules and, categorically,
15:36.3 they seem to pretty much act the same way
15:39.2 in terms of the way that they affect herbivores in those systems.
15:43.0 So, this is an illustration that shows
15:45.2 the composition of the various different plant species
15:49.2 in the northern hemisphere,
15:51.0 in the panel on the top,
15:52.3 and the southern hemisphere,
15:54.3 in the panel on the bottom,
15:56.2 and what it shows is the proportion of dry weight of these plants
16:00.3 that is composed of phlorotannins,
16:03.1 and what you see, in contrast in these two different areas of the world,
16:06.1 is that the composition of the plants in terms of the phlorotannin concentrations
16:09.3 is radically different between the North Pacific, where they're very uncommon,
16:14.0 and the South Pacific, where they're very abundant.
16:16.2 So, the overall average percent dry weight
16:20.1 of phlorotannins in southern hemisphere kelp species
16:23.0 is about 10%;
16:25.0 in the northern hemisphere it's less than 1%.
16:28.1 The next question that my colleagues and I asked was,
16:31.1 how are the herbivores in these two different parts of the world
16:35.0 reacting to these phlorotannins?
16:37.2 Now, this was a little bit tricky because
16:40.2 there are lots of other differences between the plants,
16:42.2 and so it wasn't simply a matter of looking at rates of grazing.
16:45.1 What we had to do was isolate the compounds
16:48.0 and then subject the herbivores to
16:52.1 diets that varied only in the composition of these secondary compounds.
16:55.3 So, what we did is we took a green algae called Ulva
17:00.2 that every known herbivore in the marine environment likes to eat,
17:03.1 it's very poorly defended and very nutritious,
17:05.2 we freeze-dried this stuff, we ground it up,
17:08.2 and we put it into little agar discs,
17:10.2 and that's what you see here.
17:12.0 So, these agar discs are then the grazing model
17:15.1 that we exposed to the various herbivores.
17:17.2 We were then able to manipulate the concentration of phlorotannins
17:21.2 s in these discs
17:24.1 and thereby look at how the phlorotannins, in isolation of everything else,
17:27.2 was influencing the grazing rate of the herbivores.
17:31.0 And all we did was simply build these discs
17:33.3 using different phlorotannin concentrations
17:35.2 from different plants
17:38.2 and then look at how herbivores in the northern and southern hemisphere
17:41.1 responded to varying concentrations of phlorotannins.
17:45.1 And here's an illustration that shows the results.
17:48.1 So, what you see here is a whole bunch of data,
17:51.0 it's fairly complicated in terms of there's a lot of material here,
17:53.2 but keep in mind that the big 'NS' values
17:57.1 are indicative of no effect of the phlorotannins,
18:00.0 and the little stars indicate that there was a significant deterrent effect.
18:04.3 So, all of the data on the left side of the vertical line in the middle, here,
18:09.1 are data from herbivores that came from the northern hemisphere,
18:13.0 and all the information you see on the right hand side of the panel
18:16.1 is from herbivores from the southern hemisphere.
18:20.1 And you can immediately see from this that
18:23.2 regardless of whether the phlorotannins came from southern hemisphere algae
18:27.2 or northern hemisphere algae,
18:29.1 they were deterrent to northern hemisphere herbivores
18:32.0 but largely undeterrent or nondeterrent
18:34.2 to southern hemisphere herbivores.
18:36.2 So, I've just encapsulated this in a simplification of that illustration
18:41.3 to show that in the North Pacific
18:44.1 we see a strong deterrence effect of phlorotannins,
18:48.3 regardless of where the phlorotannins are from,
18:52.1 whether they come from the northern hemisphere or the southern hemisphere,
18:54.1 and in Australasia we see either a weak deterrence or no deterrence effect
18:58.2 regardless of where the phlorotannins were from.
19:01.2 So, based on all of what I have told you,
19:03.3 we have come to this view of the coevolutionary dynamic consequences
19:09.0 of sea otters in the North Pacific.
19:11.0 In the southern hemisphere,
19:13.3 we have a two trophic level system,
19:15.3 we don't have an ecological analogue of the sea otter.
19:18.2 As a consequence, the intensity of herbivory on the plants is high.
19:22.2 As a consequence of that,
19:25.0 the plants appear to have evolved defenses in the form of high concentrations of phlorotannins,
19:29.0 and as a consequence of those high concentrations of phlorotannins
19:32.1 the herbivores, in turn, have evolved resistance.
19:35.2 So, we've had a strong coevolution
19:38.2 of defense and resistance
19:40.2 in the south hemisphere kelp forests.
19:42.3 In the northern hemisphere, we've had a third trophic level
19:45.3 in the form of the sea otter.
19:47.2 The sea otter reduces the herbivore,
19:49.3 thus it breaks this coevolutionary arms race,
19:52.1 and as a consequence what we see are
19:55.2 really poorly defended plants
19:58.1 and we see herbivores that have not developed an ability
20:01.0 to resist those defenses because they've never had to.
20:06.2 So, I've made the argument that there has actually been
20:10.0 important coevolutionary going on in this system
20:12.1 that's a consequence of an apex predator.
20:14.2 What are some of the ecological spinoffs
20:16.2 or other effects that this might have had
20:18.3 on other species and patterns in the system?
20:21.1 I'm going to spend a little bit of time telling you about that now.
20:25.1 So, this is an illustration that shows
20:28.1 the co-occurrence of the abundance of plants,
20:31.1 that is, kelps, and herbivores,
20:33.3 that is, urchins,
20:36.0 in both the northern hemisphere and the southern hemisphere.
20:38.1 So, the panel on the top are
20:41.2 data from Southeast Alaska in the northern hemisphere.
20:43.1 The panel on the bottom are data from New Zealand.
20:47.1 In the upper panel, the filled symbols
20:50.1 are data from places where sea otters are abundant;
20:53.0 the open symbols are data from places where sea otters are absent.
20:57.2 And what you can see in the northern hemisphere is that
21:00.1 when sea otters are present
21:02.1 the abundance of sea urchins is very low
21:04.2 and the abundance of kelps is high,
21:06.2 and when sea otters are present...
21:09.0 or, I'm sorry, absent,
21:11.2 the abundance of kelps is very low
21:13.2 and the abundance of sea urchins is very high.
21:15.2 And in this graph, which we call a state-space diagram,
21:19.0 which shows the abundance of two co-occurring species
21:20.2 in relation to one another,
21:23.0 all the data points occur at the perimeter,
21:25.1 that is, they occur in this sort of hyperbolic relationship
21:27.2 along both of the two axes,
21:29.1 but you never see any place in the North Pacific
21:32.2 where both urchins and kelps co-occur in high abundance,
21:37.2 or very few, and in these particular sites where we sampled, none.
21:40.3 If you go to New Zealand and make the same measurements,
21:43.2 you see a radically different pattern in terms of
21:46.2 the way in which herbivores and plants live together,
21:48.2 and you can see this from the symbols in this illustration.
21:51.3 The symbols are not important,
21:54.0 all that's really important for you to note here
21:56.0 is that this state-space diagram is populated extensively
21:59.2 by points where both herbivores and plants are abundant.
22:03.1 So, this, we believe, is one of the ecological spinoffs
22:06.3 of this coevolutionary arms race that I told you about
22:10.2 that is driven by the existence of sea otters in the North Pacific Ocean.
22:15.1 What about other species?
22:17.0 How might they have been affected?
22:19.1 We aren't terribly sure of this,
22:22.0 but one example that is very intriguing has to do with
22:25.0 what we call the Hydrodamaline sirenians.
22:27.0 So, the Hydrodamaline sirenians
22:29.2 are a lineage of manatee-like or dugong-like creatures
22:33.1 that are fairly closely related to tropical dugongs
22:36.3 in the tropical Pacific.
22:38.2 So, dugongs, as you may know,
22:40.3 as sea grass feeders, and they live in the tropics,
22:43.0 but with the cooling of the poles,
22:46.1 what happened was that a lineage of that family of dugong and sirenians
22:51.1 formed what are called the Hydrodamalines,
22:53.2 and the Hydrodamalines radiated into the North Pacific
22:56.1 and they became kelp feeders.
22:58.1 And what's interesting about this particular radiation of mammals
23:02.0 is that the only place in the world that it occurred
23:05.1 is in the North Pacific,
23:06.3 and the only place in the world where we have flora
23:09.0 that seems to be good for herbivores to eat
23:11.1 is also in the North Pacific.
23:13.2 So, we have imagined, and the argument can be made,
23:16.0 that the evolution of the Steller sea cow was, in fact,
23:19.0 a consequence of the fact that sea otters occurred in this system
23:21.2 and created a food resource that made it possible for them to do this.
23:26.2 Another group that's interesting in this context are the abalones.
23:29.0 The abalones are an old group of gastropod mollusks,
23:33.1 and here are pictures of abalones,
23:35.1 and one of the most interesting thing about abalones
23:37.2 is the tremendous variation in maximum body size across species.
23:42.2 So, you see that here in this illustration.
23:44.0 The figure on the left is a tropical abalone
23:46.2 or a warm water abalone,
23:48.2 Haliotis varia,
23:50.3 and the part of the abalone you see on the right
23:53.0 is a cold water abalone from the North Pacific,
23:55.1 this is the red abalone, Haliotis rufescens,
23:58.3 and you see the radical different in body size.
24:00.3 So, the question is,
24:04.1 how might the evolution of the food resource of abalones,
24:07.1 which are kelps,
24:09.1 influence their body size and the evolution of maximum body size?
24:12.1 And you can see that in this illustration.
24:14.1 So, what this illustration shows is
24:19.1 information on the extant (currently living) abalone faunas
24:23.1 from all the different oceans of the world,
24:26.1 and the data on the maximum shell length
24:29.0 or the maximum body size from these different faunas.
24:31.1 And what you can see is that in Australia, New Zealand,
24:35.3 the Indo-Pacific, the Mediterranean,
24:37.3 South Africa, and everywhere,
24:40.1 the maximum body size of abalones is substantially less
24:43.1 than it is in the North Pacific,
24:46.3 and we believe that this has quite a bit to do with the fact that
24:51.1 the food resources that these abalones have evolved
24:54.1 feeding on is a very nutritious food resource
24:57.2 and that, again, is a consequence of the existence of the sea otters in the system.
25:01.2 So, to wrap up, let me recap
25:04.0 what I have told you about sea otters in kelp forests.
25:06.0 I've told you something about the approach that we have used,
25:08.2 that my colleagues and I have used in understanding the dynamics of this system
25:13.0 and in particular how sea otters fit into those dynamic processes.
25:16.1 We have done that by first modularizing the food web,
25:19.1 focusing on species that seemed to matter
25:22.0 so far as the sea otter is concerned,
25:23.3 and then we have used a perturbational analysis
25:26.1 and in this particular case we've used the North Pacific Maritime Fur Trade
25:29.3 to manipulate the abundance of otters in the system
25:32.1 and to observe dynamic consequences
25:35.1 of their ecological interactions by doing that.
25:38.1 The general findings are that
25:41.1 we have discovered what we call a trophic cascade,
25:43.1 that is, an interaction that starts high in the food web
25:47.2 with this apex predator, the sea otter,
25:49.2 and flows downward through sea urchins and kelp,
25:52.1 that this trophic cascade has what I call serpentine influences
25:56.3 on many other ecological processes and species in the system,
26:00.2 I've given you an overview of a few of those,
26:03.2 and that these strong ecological interactions
26:05.2 have led to natural selection and evolution.
26:10.2 I should acknowledge both my collaborators
26:13.3 and some of the support that we have received for this work over the years.
26:17.1 My collaborators are posted on the left
26:19.3 and the major funding sources for the work that we've done
26:23.1 are listed on the right.
26:25.1 Thank you for your attention and I hope you'll come back and join us for Part III,
26:27.2 which will be an exploration of other large species of apex predators
26:31.1 and other ecosystems.
00:00:13.05 My name is Ian Baldwin and I'm delighted, here, to be presenting Part 2 in a three-part
00:00:18.15 story on how to study the plant ecological interactions in the genomics era.
00:00:24.18 I'm a Director of the Max Planck Institute for Chemical Ecology.
00:00:28.16 And in Part 2, here, I'll be talking about Nicotiana attenuata, the plant that is right
00:00:35.12 here, it's ability to be able to respond to attack from a nicotine-tolerant herbivore.
00:00:42.12 And I just want to remind you this is Part 2 of a three-part series and in the third
00:00:48.04 part I'll be talking about the plant's perspective on sex, seeds, and microbes.
00:00:54.24 In Part 1, I talked about how the Max Planck Institute for Chemical Ecology came about
00:01:03.01 and how it fits into the rich history of the field of plant-herbivore interactions, and
00:01:06.24 how Ernst Stahl, in 1888, really started the field.
00:01:11.19 I also talked about the process of training genome enabled field biologists and how to...
00:01:18.05 how they are trying to phytomorphize themselves and understand what plants are doing with
00:01:23.00 this incredible chemical prowess that they have, and how they use those chemicals to
00:01:28.10 solve ecological problems.
00:01:30.09 I also introduced the "ask the ecosystem" approach, which combines both field and laboratory
00:01:36.02 studies of transgenic plants, and introduced the important process of silencing genes to
00:01:43.15 understand their function at a Darwinian level in an organismic context.
00:01:55.05 These field experiments are conducted with these genetically modified plants in their
00:01:59.16 native habitat in a nature preserve in the southwestern deserts of the United States,
00:02:05.14 in Utah, in a collaboration with Brigham Young University.
00:02:10.04 What I want to do here in Part 2 is talk about this particular interaction that's unfolding
00:02:15.24 to you right here.
00:02:17.22 This is an interaction of the plant that we work, Nicotiana attenuata, and the hawk moth,
00:02:25.24 Manduca sexta and Manduca quinquemaculata.
00:02:28.23 It's a remarkable interaction filmed here in fast motion, fortunately enough, by the
00:02:35.03 team of Volker Arzt from the movie Kluge Pflanzen, and they were so kind for letting us use their
00:02:41.09 This is a remarkable interaction because the plant is chock-a-block full of one of the
00:02:47.01 most toxic compounds for human beings, and for almost any animal with a neuromuscular
00:02:52.17 junction, namely, nicotine.
00:02:54.11 Now, many of us have had an addictive relationship with nicotine as smokers, but if any smoker
00:03:01.23 had ever tried to eat a Nicotiana plant you'd realize just how poisonous this plant is.
00:03:08.21 Nicotine poisons the neuromuscular junction, the acetylcholine receptor called the nicotinic
00:03:15.07 acetylcholine receptor, and that receptor mediates how muscles move.
00:03:21.03 Now, if you were a plant and you wanted to design a chemical defense which would poison
00:03:28.09 animals that moved with muscles, this would be an ideal defense compound to produce.
00:03:33.17 And this is exactly what Nicotiana attenuata and some of the other tobacco plants have
00:03:38.08 done -- they've evolved this molecule.
00:03:40.07 Now, this molecule evolved from two primary metabolic pathways, the NAD pathway and the
00:03:45.21 polyamine pathway, that produced the two rings that both contain a nitrogen and then they're
00:03:50.16 fused together to form the molecule... the molecule nicotine.
00:03:55.11 Nicotine is synthesized, as I said, from these two primary pathways, and its biosynthesis
00:04:00.02 has been worked out by a number of researchers over time.
00:04:03.07 But what is more recent is its understanding of the evolutionary history of this biosynthetic
00:04:09.08 And this was done recently by Shuqing Xu in our department and a number of his colleagues
00:04:15.17 in the informatics group that is involved in assembling the genome of Nicotiana attenuata,
00:04:21.03 which is currently under review.
00:04:22.13 And what Shuqing Xu and colleagues found out was that umm... all of the genes that are
00:04:28.02 involved in nicotine biosynthesis are genes that are part of a whole genome triplication
00:04:35.13 event that happened with the Solanaceae, namely, all the plants that are of the group of plants
00:04:42.03 that are called solanaceous plants: potatoes, tomatoes, eggplant.
00:04:48.06 All went through a genome triplication event.
00:04:50.22 Those extra copies of the genes were therefore given the evolutionary privilege to be able
00:04:56.02 to be combined in novel things other than their primary metabolic pathways.
00:05:00.09 And potatoes and tomatoes and tobacco all produced nicotine, but tomatoes and potatoes
00:05:06.24 produce them at much lower levels -- about three orders of magnitude lower than tobacco
00:05:12.20 Tobacco plants' remarkable ability to produce enormous quantities of nicotine, to really
00:05:17.21 make it defensive, and smokeable, has to do with the ability of the plant to have corralled
00:05:25.11 the biosynthesis of those pathways into the roots, and to have fused the two rings in
00:05:30.16 a very efficient way, and funnel a lot of reduced nitrogen into the biosynthetic pathway.
00:05:36.08 That's described in this paper that is currently under review.
00:05:39.24 Now, nicotine biosynthesis can be inhibited by silencing a single gene.
00:05:45.14 This gene, here, putrescine methyltransferase, which we have silenced by RNAi and been able
00:05:51.13 to produce plants that are relatively nicotine-free.
00:05:55.01 And when you make a plant that's relatively nicotine-free and you take it back out into
00:05:59.06 the native habitat and plant it in some natural habitats, you realize just how effective this
00:06:04.00 defense is.
00:06:05.00 Because every deer, every rabbit, every gopher in the neighborhood finds out about it, and
00:06:11.11 here's an example of a gopher that's coming up, has dug a special tunnel up underneath
00:06:16.13 this nicotine-free plant and is pulling it down to its burrows.
00:06:20.00 So, without nicotine, the plants become quite defenseless and are stripped bare of their...
00:06:27.13 of their phloem by rabbits and other mammal... mammalian browsers them, and usually don't
00:06:32.17 last very long.
00:06:34.16 Now, Manduca sexta, which was gobbling, devouring those plants in that first video that I showed
00:06:39.21 you, is able to do it because it is... well, it basically holds the world's record for
00:06:45.14 nicotine tolerance.
00:06:47.00 If you compare the LD50 -- the lethal dose at which 50% of an experimental population
00:06:52.15 dies -- you realize that even the most hardcore, [unknown], carton-a-day smoking human being
00:07:00.23 still has an LD50 that is 750 times lower than that of Manduca sexta, which is about
00:07:08.18 1500 milligrams per kilogram that it's able to tolerate.
00:07:12.11 Now, it's been known since the '60s that Manduca sexta's tolerance of nicotine is based on
00:07:19.11 a physiology that allows it to excrete all the nicotine that it ingests without any apparent
00:07:26.04 metabolism at... or any apparent effect on its nervous system.
00:07:30.22 How it does that is still very much an active area of discovery, but, as we look at a caterpillar
00:07:38.05 eating a plant, we've been interested in asking the caterpillar, transcriptomically, what
00:07:44.10 is it doing inside of its gut to be able to handle those many human doses of lethal doses
00:07:50.22 of nicotine that it's ingesting almost on an hourly basis.
00:07:55.00 And when you ask the caterpillar, transcriptomically, there is consistently one cytochrome P450
00:08:02.09 which is constantly being regulated in direct proportion to the amount of nicotine that
00:08:06.00 is ingested by the caterpillar.
00:08:07.07 And this is a cytochrome P450 with a long complicated name called 6B46.
00:08:14.11 And you can see it regulates at a high level when it's eating nicotine-containing plant
00:08:18.15 and downregulates when it's eating nicotine-free plants.
00:08:22.02 So, to understand what this particular gene was doing in the caterpillar and why it was
00:08:28.04 being up-regulated every time the caterpillar ate a high-nicotine-containing plant, two
00:08:33.13 scientists in the department, Pavan Kuma and Sagar Pandi, designed a procedure that allowed
00:08:44.06 the study of this particular gene to occur in the natural environment of both the insect
00:08:48.21 and the plant.
00:08:50.03 And what they did was they took that gene, made a double-stranded contract, which is
00:08:53.14 depicted here in yellow in the plant, transferred it into the plant so that was consistently
00:08:58.10 expressing this double-stranded piece of the gene that they wanted to silence, and then
00:09:03.23 they planted it out in Utah and let free-ranging caterpillars feed on them.
00:09:09.16 And, in that process of feeding on these particular plants, the caterpillar ingests double-stranded
00:09:15.04 and then the gene in the caterpillar gets silenced.
00:09:18.19 And in those genes silence caterpillars they were able to understand the function of that
00:09:24.22 particular cytochrome P450, which is up-regulated during the defense process.
00:09:31.08 And what they discovered was really remarkable, but let me show... first show you some data
00:09:35.04 on just how effective this plant-mediated RNAi process is.
00:09:40.08 Here on the y axis is the transcript levels for the particular gene that they're looking
00:09:44.21 at in the various tissues of the caterpillar.
00:09:47.15 And I want you to focus particularly on the midgut, which shows that caterpillars eating
00:09:54.18 nicotine-containing plants have very high levels of that transcript.
00:09:58.14 But if the caterpillars are feeding on a nicotine-free plant, the transcript levels are quite low.
00:10:04.07 But if the caterpillars are feeding on one of these PMRi...
00:10:08.03 PMRi plants that are expressing a double-stranded construct of that cytochrome P450, and those
00:10:14.15 plants contain normal high levels of nicotine, you would expect the transcript levels to
00:10:19.16 be this high, but instead they're that low.
00:10:22.21 And they're that low because the gene is being silenced by that plant... by the plant's food,
00:10:31.01 and the caterpillars are ingesting that gene and that RNAi process is happening in basically
00:10:36.19 free-living, free-ranging caterpillars in the field.
00:10:39.15 It's a remarkable experimental tool that allows us to study plant-insect interactions in nature
00:10:45.04 using genetic tools to manipulate not just the plant, but also the insects that are feeding
00:10:50.01 on the plant.
00:10:51.04 Now, what's remarkable about this story is that it was actually a wolf spider occurring
00:10:56.04 in the natural habitat of the plant that told us the function of this particular gene in
00:11:03.12 the caterpillar.
00:11:05.09 And now I'm going to show you a series of videos and here's a video of a wolf spider
00:11:09.14 attacking a nicotine-free plant and you can see from that video that it just gobbled it
00:11:15.21 So, if the caterpillar is feeding on a nicotine-free plant it has no nicotine in it and the wolf
00:11:21.05 spider finds it as food.
00:11:23.21 Now, here is, in the next video, a spider attacking a caterpillar that is fed on one
00:11:30.01 of these PMRi plants.
00:11:31.14 Now, remember those have are full of nicotine but they are silencing this particular gene
00:11:36.17 in the caterpillar.
00:11:37.18 And you can see from this video that the caterpillar is attacked and eaten as if it was nicotine-free,
00:11:44.06 and this was discovered by the two scientists who had placed caterpillars on plants out
00:11:51.04 in the field, having them feeding on these particular plants that silence the gene in
00:11:55.05 the caterpillar, and all the caterpillars disappeared at night.
00:11:58.12 And the wolf spider hunts at nighttime and that's how they found the wolf spider.
00:12:02.18 Now, here is the key moment, the key observation that allowed them to understand what was going
00:12:08.09 on, because in the next video here is a spider attacking a nicotine-containing plant, that's
00:12:17.01 a normal empty vector wild-type plant, and you can see all it did was go up and palpitate
00:12:22.21 the spider... the caterpillar and then it immediately backed away.
00:12:26.06 And what was going on in that palpitation, that little moment when the caterpillar being
00:12:31.07 assessed by the spider and the spider decided, oh...
00:12:33.15 I'm not gonna eat this, was that the caterpillar was, through its spiracles... caterpillars
00:12:40.16 have 17 spiracles, they are basically the lungs of the caterpillar... caterpillars have
00:12:46.06 all these tubes and that's how they exchange air... and through the spiracle the caterpillar
00:12:51.01 is puffing out a load of nicotine into the face of the caterpillar... into the face of
00:12:57.06 the attacking spider.
00:12:58.06 And that's why the attacking spider jumped away.
00:13:01.11 And what this gene is doing is mediating that process, in a way that we don't really understand
00:13:06.08 biochemically, allowing the caterpillar to basically divert a lot of... some portion
00:13:11.13 of that massive amount of nicotine that's flowing through its gut, that it's excreting
00:13:15.02 out, but then it moves it into the spiracles and it uses it defensively when a spider comes
00:13:20.03 up and says, are you good food?, and the caterpillar then just puffs out this thing of nicotine
00:13:23.23 and repels it, okay?
00:13:26.10 So, that shows you that, actually, the caterpillar, even though it's excreting most of its nicotine,
00:13:32.16 is using it defensively, it's co-opting just a small fraction of what's going through its
00:13:36.19 gut for its own defensive purposes.
00:13:38.09 But, now, what I'm going to tell you, for the rest of this talk, is what happens when
00:13:43.20 the plant recognizes that it's being attacked by that particular nicotine-tolerant caterpillar.
00:13:50.21 Because that recognition process results in six changes in the plant that all involve
00:13:58.07 how the plant deals with a caterpillar that has broken through one of its major defenses
00:14:04.00 and has to figure out something else to do with this guy that's going to eat it, and
00:14:08.18 that's going to make lunch of it.
00:14:10.08 And that recognition process starts right here.
00:14:13.15 And if you look right at that cut leaf edge, there, you can see a little bit of green slimy
00:14:18.10 stuff that the caterpillar is leaving on the edge of the leaf.
00:14:21.19 Now, it turns out it's not doing that intentionally, that's just part of the eating process, it's
00:14:25.13 part of its oral secretions, that's part of the process of masticating the leaves to be
00:14:29.06 able to digest it, but in those oral secretions are a group of compounds that are called fatty
00:14:35.07 acid amino acid conjugates.
00:14:36.24 FACs is what we call them, and the structures of those FACs are right here.
00:14:41.11 They're very simple molecules -- they're just fatty acids esterified to amino acids.
00:14:45.16 There's two of them, there's five fatty acids, and they make basically eight different structures,
00:14:50.04 and those eight structures are what the plant uses to say, aha I'm being attacked by Manduca
00:14:57.24 sexta and I know that it's nicotine resistant in some way or another.
00:15:00.23 And those are...
00:15:01.23 I'm anthropomorphizing but that's basically the message.
00:15:04.20 Now, what I'm going to do... this is, by the way... this fatty acid amino acid conjugates
00:15:09.06 were discovered by Rayko Halitschke in his thesis and published back in 2001.
00:15:13.14 What I'm going to do now is to take you through those six layers of defense, avoidance, and
00:15:19.24 tolerance that the plant goes through when it recognizes this... that it's being attacked
00:15:27.01 by this... this particular caterpillar.
00:15:31.00 And those six layers are both an up and down regulation of direct defenses, a bunch of
00:15:35.23 indirect defenses, an interaction between indirect and direct defenses, tolerance responses,
00:15:41.07 and avoidance responses.
00:15:43.02 So, follow with me and we're going to go through this remarkable journal... journey of what
00:15:47.23 happens to the plant as it reorganizes its metabolism, physiology, to deal with the fact
00:15:54.19 that it's got a predator that it really has to deal with.
00:15:59.11 Now, first I want to talk a little bit about the recognition process.
00:16:02.15 So, umm... we've been able to, because we have these synthetic fatty acid amino acid
00:16:08.23 conjugates, we have the elicitors... we're able to start the interaction between plant
00:16:14.05 and its responses without having to have a caterpillar.
00:16:17.06 So, we simply just take a pattern wheel and we add these oral secretions to spit to the
00:16:21.10 leaves, to the holes that are made in leaves with the pattern wheel, and that elicits a
00:16:25.05 very complicated set of signaling responses.
00:16:28.14 We haven't identified the elicitor... the... the receptor yet for the elicitor.
00:16:32.03 We know the elicitor -- those are the FACs, the receptor is unknown, but that that elicits
00:16:38.12 a very complicated signaling network that involves MAP kinases, SIP and WIP kinases,
00:16:43.19 the jasmonate signaling cascade, and a lot of modulation of that jasmonate signaling
00:16:50.11 cascade through other kinases, the activation of CDP kinases as well, and the perception
00:16:59.04 by other receptors, LecRK, that it basically involves a regulation of jasmonate signaling.
00:17:06.05 And, because caterpillars do not brush their mandibles when they eat a plant, they also
00:17:11.14 contain bacteria and other sorts of bacterial signals, and the plant has to make sure that
00:17:16.18 it's activating a jasmonate signaling cascade and not a salicylate signaling cascade, so
00:17:22.17 all of this signaling has to do with being able to make sure that the caterpillar doesn't
00:17:28.09 fake out the plant with its bacterial signals, but rather generates a nice clean jasmonate
00:17:35.07 response, which activates five out of the six layers that I'm now going to talk to you
00:17:41.03 Now, that was a lot of work, and that work was done by some remarkable group leaders
00:17:48.00 and a remarkable number of talented students that I wish I could talk about in greater
00:17:52.16 detail -- but here are their pictures.
00:17:55.13 It also illustrates another important message that I want to bring up in this talk and that
00:17:59.17 is that interplay between mechanism and function, that if you understand the details by which
00:18:06.00 these responses come about, you have the very tools that you can manipulate genetically
00:18:11.13 to be able to create plants that are not able to show the response, and all of those steps
00:18:17.00 in those signaling pathways have been very useful tools to allow us to be able to manipulate
00:18:22.23 some aspects of these six responses in different combinations, and test them functionally in
00:18:27.15 the field, in the actual habitat in which the plant evolved.
00:18:31.23 Now, let me go through the six responses.
00:18:34.00 The first response was the up- and down-regulation of these, what we call, direct defenses.
00:18:39.07 Now, direct defenses basically can be categorized in two groups.
00:18:43.05 They're either toxins, things that poison animals that eat plants, without poisoning
00:18:49.10 the plant too much, and are specifically targeted against the things that are different between
00:18:54.15 animals and plants, like nervous systems; plants don't have a nervous system, so it's
00:18:58.19 really easy for plants to make nervous system poisons that are not toxic to them, but are
00:19:04.18 very toxic to the animals that want to eat them.
00:19:07.01 So, in addition to toxins, there's also another type of direct defense that are called digestibility
00:19:13.08 They're basically interfering with the main reason why a caterpillar wants to eat a plant
00:19:18.11 in the first place, which is to turn caterpillar protein... plant protein into caterpillar
00:19:23.23 protein, to turn caterpillar... plant energy substances like glucose and sucrose and starch
00:19:30.02 into energy substances that the caterpillar can use.
00:19:33.11 So, that digestibility process can be interfered with lots of different ways.
00:19:40.00 Interfering with all the steps of ingestion and digestion... for example, there are protease
00:19:45.06 inhibitors we're going to talk a little bit about, there are tannins and amylase inhibitors
00:19:48.11 that are basically affecting the digestive enzymes that take apart plant proteins and
00:19:52.21 starches, and make them available to be uptake... taken up by the guts of caterpillars.
00:19:57.24 But there's also abrasives, things that wear down the mandibles and the teeth of the herbivores,
00:20:02.20 because, you know, if an herbivore doesn't have a pair of teeth, a set of mandibles or
00:20:08.18 a set of teeth, it can't chew a plant.
00:20:10.24 And plants fill themselves with silica and other sorts abrasives that just wear down
00:20:15.18 the teeth.
00:20:16.18 And there is no easier way to starve an ungulate than to wear out its teeth, and plants do
00:20:22.17 that all the time.
00:20:23.17 Now, I just want to talk about the down-regulation, as well as the up-regulation, because the
00:20:28.09 first thing that happens when those FACs are recognized by the plant is the plant has an
00:20:34.02 ethylene burst and shuts down the very gene that we silenced to make a nicotine-free plant.
00:20:38.24 And that's in fact the reason why we did it, because we learned from the caterpillar how
00:20:43.17 it was shutting down nicotine biosynthesis in the plant.
00:20:48.02 And it's very clear, now, that since the caterpillar is co-opting a certain portion of the nicotine
00:20:53.13 for its own defense, the plant is most likely down regulating its nicotine production so
00:20:59.00 that the plant... so the caterpillar can't co-opt the extra nicotine it produces.
00:21:02.23 If it was a deer or a rabbit producing... doing the damage rather than a Manduca sexta
00:21:08.14 larvae, nicotine production would be operated 5- or 6-fold and the... you know, the plant
00:21:14.17 would become even more full of nicotine than it already is, so that a single leaf would
00:21:20.00 have the same amount of nicotine in it as half a carton of [unknown] cigarettes.
00:21:24.13 So, that massive up-regulation process is just basically stopped and the... the plant
00:21:30.01 is down-regulating nicotine production when it knows that it's being attacked by a nicotine-resistant
00:21:36.10 Then it produces a whole bunch of other types of compounds, many of which we had no idea
00:21:41.06 what they did.
00:21:42.06 And I just want to talk, just briefly, about a group of compounds called diterpene glycosides.
00:21:47.03 This is some work done by a PhD student who's just finishing enough, Sven Heiling, and he's
00:21:51.06 done some beautiful analytical work characterizing these molecules that were basically unknown.
00:21:56.15 There were 46 of them in Nicotiana attenuata and they are basically produced in the chloroplast
00:22:05.23 by what's called the MEP pathway and the DOX pathway, to produce a basic backbone diterpene
00:22:13.02 structure, and that backbone diterpene structure is depicted there.
00:22:17.10 It's hydroxylated and then sent out to the plant and decorated further by enzymes that
00:22:24.11 add different types of sugars to them -- I'll talk about that a little bit later.
00:22:29.12 But, because this is a secondary metabolic pathway, the main enzyme that's involved there,
00:22:35.22 this NaGGPPS that is highlighted in bold, there, also has three copies, because of that
00:22:43.12 trip... the genome duplication event, and, if you silence the one that's dedicated for
00:22:48.04 the production of these pathways, you can completely take out the whole biosynthetic
00:22:52.03 pathway by one gene silencing step.
00:22:54.20 So, by silencing that particular gene, we're able to make DTG-free plants and if you fed
00:23:01.07 them to caterpillars you can see that the caterpillars basically were able to increase
00:23:06.19 their growth rate almost fivefold when they're feeding on these DTG-free plants.
00:23:11.19 So, even though we had no idea that these were toxic or defensive when we looked at
00:23:17.07 the structures and figured out their structures, when we silence them and produce plants that
00:23:21.05 were where DTG-free the caterpillars told us that, oh... this is really a pretty nasty
00:23:26.17 defense compound.
00:23:28.18 And what Sven has been able to do is to identify all the different enzymes that are involved
00:23:33.22 in decorating them with sugars of various sorts, glucose and rhamnose, here, and then
00:23:40.18 they are malonated in addition, and that's what generates all those 48 different...
00:23:43.19 48 different structures.
00:23:44.20 Now, it turns out that if you look at the... the poop of a caterpillar, the frass that
00:23:50.04 comes out the busi... the other end of the caterpillar after it's eating leaves, Spoorthi
00:23:54.15 Poreddy, who is a PhD student who just finished up, along with Sven and Jianciai Li, have
00:23:59.21 been discovering that there's a very interesting dynamic that's going on in the caterpillar's
00:24:06.13 gut as it's trying to remove particular sugar groups from these DTGs, in a way so as not
00:24:13.07 to expose the toxic backbone, which is toxic to the plant also, but also not remove all
00:24:18.00 of them, which produces other toxic compounds.
00:24:21.07 So, this is a story that is ongoing, we're going... we're still working on it, but there's
00:24:25.22 this wonderful digestive duet that's occurring as the caterpillar is removing certain sugar
00:24:31.03 molecules and putting them back on, and putting other molecules back on to protect it and
00:24:36.02 detoxify this molecule as it goes through -- an example of direct defenses.
00:24:41.03 Now, I want to switch to indirect defenses.
00:24:45.05 Now, indirect defenses are based on a concept that probably every politician knows.
00:24:51.06 Now, here's the basic scenario.
00:24:53.22 Here's the plant.
00:24:54.22 And the plan is attacked by Manduca sexta, which is its enemy, right?
00:24:59.02 Now, Manduca sexta is, in turn, attacked by other predators that are all depicted here,
00:25:04.22 there are six of them right here, and they of course are the predators of the herbivore.
00:25:11.11 Now, anyone knows that the enemy of your enemy is your friend.
00:25:17.02 And that is the basis of how indirect defenses work.
00:25:22.09 Indirect defenses, in contrast to the direct defenses, are signals or traits that the plant
00:25:29.24 produces that help predators or parasitoids find and feed on the herbivores that are feeding
00:25:37.02 on them.
00:25:38.23 And that's what that indirect defense looks... how that works.
00:25:41.23 Now, the way it works in Nicotiana attenuata is that, when Manduca sexta begins to feed
00:25:47.06 on an attenuata plant, the plant recognizes it from those FACs that are in the caterpillar's
00:25:52.07 spit and it activates a series of transcription factors, and it activates the production of
00:25:57.05 a beautiful, volatile bouquet, like a Chanel No. 5 that's released not just from the attack
00:26:02.14 leaf but the entire plant.
00:26:04.15 And it's basically just producing this signal that includes a number of molecules, the most
00:26:10.00 important of which is a sesquiterpene called trans-alpha-bergamotene, and trans-alpha-bergamotene
00:26:15.22 attracts this little predator that's down here called Geocoris pallens, a little predator
00:26:20.13 that lives around in the soil on the plant, and it's basically listening, smelling in
00:26:25.06 the air, and when it senses that molecule it knows there's a caterpillar feeding on
00:26:29.17 a plant somewhere.
00:26:30.23 But that little Geocoris also needs local information.
00:26:34.18 Once it arrives on a plant, the plant is big, the caterpillar could be anywhere in the plant,
00:26:39.07 and it utilizes other compounds like these green leafy volatiles on the top there, and
00:26:43.12 particular... particularly the change in a double bond in those green leafy volatiles
00:26:47.23 that gives it local information and allows the Geocoris to be able to localize where
00:26:52.22 on the plant that particular caterpillar is feeding.
00:26:55.07 And, when it gets there to the caterpillar, it just plunges its beak inside the caterpillar
00:27:00.17 and sucks it out and it does that many times.
00:27:04.03 And so what this process is just like calling the police.
00:27:08.12 It doesn't have to do anything more than simply provide accurate, honest information about
00:27:14.20 where a caterpillar is feeding on it, how it's being attacked, and then the predators
00:27:19.05 take it from there.
00:27:21.10 It's a wonderful evolutionarily stable way of dealing with defense because the evolutionary...
00:27:26.19 coevolutionary loop between plant and herbivore is broken by this predator link.
00:27:33.04 Now, we discovered that thanks to the brilliance, really, of the graduate student in the group,
00:27:38.23 Andre Kessler, who is now professor at Cornell, and he invented a predation assay that allowed
00:27:44.04 us to monitor the behavior of this predator in the field under natural conditions.
00:27:48.13 And the predation assay was beautifully simple.
00:27:51.00 He simply just glued eggs of this Manduca onto the bottom of leaves and used those eggs
00:27:59.03 as a monitor for whether or not the predator had come up to the plant.
00:28:02.24 The predator is a very skittish predator.
00:28:05.16 It's called the big eyed bug... it has big eyes, it pays attention to a lot of things,
00:28:10.03 you can't walk up and see, it runs away... and so you need an indirect way to know whether
00:28:14.06 or not it's been around.
00:28:15.21 And yet, when the predator feeds, you can see that it sucks out the egg and it leaves
00:28:19.23 the egg in a nice state behind, and by gluing eggs onto the plant you can see how many predators
00:28:27.06 have come up and visited the plant.
00:28:29.01 And that predation assay had allowed us to be able to work out the transcription factors
00:28:32.17 that regulate volatile production, which volatiles are important, the long- and short-distance
00:28:36.12 signals, all the details of this particular process.
00:28:39.14 Now, it turns out that these indirect defenses don't work alone; they work in synergy with
00:28:46.09 the direct defenses.
00:28:48.04 So, when the cater... when the caterpillar attacks a plant and it causes the plant to
00:28:52.16 produce this wonderful volatile bouquet that is functioning as an alarm call, bringing
00:28:57.24 in predators from long distances away, that will then attack the caterpillars, there are
00:29:03.05 other things going on too, namely that the plant is also producing compounds that are
00:29:08.24 interfering with the digestive process.
00:29:11.06 And these are the protease inhibitors that Jorge Zavala worked on, and the protease inhibitors...
00:29:16.00 here's a seven-domain protease inhibitor... and what they do is they inter... interact
00:29:20.16 with the digestive enzymes of the caterpillar's gut and keeps the caterpillar from digesting,
00:29:25.06 which means that the caterpillar can eat and eat and eat but it doesn't grow, because it's
00:29:28.15 not getting the nutrients.
00:29:30.03 Now, when a caterpillar goes through the stages from being small to large, it becomes pretty
00:29:36.01 immune to this predator, because it's a bratwurst-sized caterpillar at the end and it pretty much
00:29:41.00 can thumb its nose at this little predator who is trying to attack it.
00:29:44.21 But if the plant keeps the caterpillar in a nice, small, vulnerable stage longer, the
00:29:49.20 indirect defense of the predator works much better.
00:29:52.14 So, it's the synergy between direct and indirect defenses that really helps to bruise the...
00:29:58.02 lower the population of caterpillars.
00:30:01.05 Now, there's another type of synergy that occurs as well, and this is depicted very
00:30:05.08 nicely in some videos by Mary Schuman, who is pretending to be a Geocoris predator, sticking
00:30:10.22 a little blue pin up the butt of the caterpillar.
00:30:13.02 And you can see, on a caterpillar that's feeding on a wild-type plant, a wild-type plant that's
00:30:17.11 full of defenses, it's behaving pretty sluggishly -- it's not moving at all when she's poking
00:30:23.17 it, she picks it up with the forceps, it doesn't do any wagging, it just hangs there limp like
00:30:28.01 a doornail.
00:30:29.02 Now, remember this caterpillar is spending a lot of metabolic energy detoxifying the
00:30:34.13 defenses that are in the leaves, the direct defenses.
00:30:39.01 And it doesn't have a whole lot of energy to fight back when it's attacked by predators.
00:30:45.00 Compare that when Mary tries to poke a caterpillar that's feeding on a protease-inhibitor-free
00:30:50.21 plant -- it's got plenty of energy.
00:30:52.11 It's banging around, it's thrashing, and it's defending itself quite well.
00:30:56.24 And that's another example of the synergy between direct and indirect defenses, is that
00:31:04.00 caterpillars that are feeding on toxic plants are lethargic.
00:31:06.15 They are having to spend a lot of energy detoxifying all those metabolites that are going through
00:31:11.22 them, and that slows them down and makes them much more vulnerable to their predators.
00:31:18.00 We so frequently forget because we eat defenseless plants in our normal food supply, we made
00:31:24.09 them defenseless through our agricultural practices, that we forget that eating native
00:31:28.11 plants that are full of chemicals is actually hard, metabolically demanding work.
00:31:34.24 Now, there's another type of direct defense... indirect defense that I want to tell you about.
00:31:39.08 And that's an indirect defense that occurs in the trichomes, which are these little hairs
00:31:43.03 on the surface of the leaves, and you can see as a little droplet appearing here from
00:31:47.11 this magnification of a trichome on the surface of an attenuata leaf.
00:31:50.22 Now, in the trichome is... is a particular type of compound called an acylsugar.
00:31:55.18 Now, acylsugars were thought to be direct defenses, toxins, and there's a good bit of
00:32:01.00 evidence that they are sticky substances that catch insects and sort of tie them up.
00:32:06.13 But... and this was actually first worked on by Alexander Weinhold in the group, and
00:32:11.23 Alexander characterized the structures of these things, and that these acylsugars basically
00:32:17.02 consists of a sucrose molecule and then on each of the hydroxyl groups of the sucrose
00:32:21.10 molecule is esterified a small, short-chain fatty acid.
00:32:26.03 Here are the characteristics of these short... short-chain fatty acids, and these short-chain
00:32:31.06 fatty acids have the smell of baby barf. they're sort of an unpleasant smell and that's the
00:32:36.15 reason why Alexander actually started the project in the beginning, because he had to
00:32:40.08 take care of the caterpillar colony, and he always thought that the caterpillars smelled
00:32:44.15 fairly bad, and... and noticed that when they were feeding on these leaves they were of
00:32:51.03 course eating acylsugars.
00:32:53.02 And when we took these plants to the field... took plants to the field and noticed what
00:32:57.03 caterpillars did when they first hatch out of their egg, we noticed that these... these
00:33:01.05 acylsugars are not defensive at all, they're in fact the first meal of a caterpillar.
00:33:05.11 A caterpillar hatches out of its egg and it begins to lick these... these tops like they're
00:33:10.07 little lollipops, and they get their first meal, and, in the process of getting that
00:33:15.00 first meal, they end up getting a body odor.
00:33:19.00 And the body odor comes from eating those acylsugars and having those fatty acid groups
00:33:24.16 deesterify and come off the body.
00:33:27.09 And so the caterpillar begins to smell of those baby barf fatty acids that are esterified
00:33:33.12 to those sugars.
00:33:34.13 Now, we were very interested to know whether or not smelling attracted the attention of
00:33:39.11 predators that were on the plants.
00:33:41.04 And so we looked at all the predators that occur on plants and none of them cared about
00:33:45.03 this... these baby barf smells -- they didn't seem to respond more to caterpillars that
00:33:48.23 were scented or non-scented.
00:33:50.02 So, we investigated some more.
00:33:52.08 But it turns out that there was another thing that these compounds did to a caterpillar's
00:33:58.21 body odor.
00:33:59.24 Not only did it change the body odor, but it also changed the smell of its poop.
00:34:04.24 There was a caterpillar just pooping there.
00:34:07.03 And poop, when it happens, when it falls, usually falls according to the laws of gravity.
00:34:16.03 It falls down.
00:34:17.03 It doesn't always hit the fan as... as the metaphor goes.
00:34:20.20 And the caterpillar, when it poops, produces a smelly, fresh, redolent poop that falls
00:34:27.14 directly on the ground, and this is Utah where the ground is hot, it's frequently 50 degrees,
00:34:32.16 and those are short-chain fatty acids, so they immediately volatilize, and after five
00:34:36.20 minutes or so they become scent-less and they no longer have that smell.
00:34:41.01 But for five minutes, when the fresh poop has fallen on the ground, it's providing beautiful
00:34:46.01 information to a whole other group of predators.
00:34:49.23 And those are the predators that are walking along in the ground, the lizards and the ants,
00:34:54.19 and it turns out that the lizards and the ants use that volatile information to know
00:34:59.07 that, oops, there's a caterpillar above them, they can just climb up the plant.
00:35:03.03 And you can take fresh frass and dried frass, or you can just isolate the... that... that...
00:35:09.07 those fatty acids and make your own little perfume, which will be available in duty-free
00:35:13.19 shops soon, and call it the scent of the caterpillar, and you can spray it on the ground and spray
00:35:17.16 it on sticks in front of ant nests, and the ants will just come charging up after you've
00:35:21.23 sprayed them, looking for caterpillars.
00:35:24.06 And so, in the end, these trichomes may well be the first meal for the caterpillar, and
00:35:32.05 they're delicious, sugary lollipops, but in the process of scenting their bodies and scenting
00:35:38.10 their frass, they actually turn out to be evil lollipops because they tag them for predation.
00:35:43.16 And that's just another example of how a plant is utilizing indirect defenses to protect
00:35:51.00 They have very clever ways of bringing in predators.
00:35:54.07 And that was the fourth layer.
00:35:55.23 Now, I'm going to go to the fifth layer, now, and the fifth layer activated by those fatty
00:36:02.06 acid amino acid conjugates that are in the caterpillar's spit.
00:36:05.07 In the fifth layer is a layer of tolerance responses that the plant activates.
00:36:10.15 We had talked earlier in Part 1 about how a plant is a growth machine, fixing carbon
00:36:15.23 dioxide, taking that carbon dioxide, making a whole bunch of metabolites for growth, reproduction,
00:36:21.03 storage, and defense, but at the same time it's also possible to use it to make the plant
00:36:28.10 more tolerant of herbivore attack.
00:36:31.07 Now, until this work, the whole tolerance thing was pretty much a trait-less concept,
00:36:36.01 something that you could look at in populations of plants, but not something you could really
00:36:40.02 nail down to a particular trait.
00:36:42.05 And here we've been able to nail it down to a particular trait.
00:36:45.06 And it came, again, from a field observation.
00:36:47.09 The field observation was that caterpillar-attacked plants, after they plants had senesced and
00:36:53.04 dried out, and then there was another rain, they frequently reflowered -- they produced
00:36:58.00 new flowers after a rain -- but the plants that were not attacked by caterpillars didn't
00:37:02.15 do this reflowering.
00:37:03.16 So, that was an interesting observation.
00:37:05.12 And you sort of wondered, where did these caterpillar-attacked plants get the resources
00:37:09.14 to reflower?
00:37:10.20 This is an annual plant; it should have shut down life, made all the flowers that it could've,
00:37:14.22 and senesced and called it quits.
00:37:16.07 But that's not what they were doing.
00:37:17.21 And I think the answer comes in the life history of the caterpillars that feed on them.
00:37:23.20 Caterpillars go through two stages.
00:37:25.08 They have the eating machine stage, which is depicted right here, where Manduca...
00:37:29.24 Manduca sexta is simply just a larvae trying to consume as much plant material as possible,
00:37:33.18 but then it pupates and molts into this beautiful moth, and it becomes a sex machine.
00:37:39.21 And, as a sex machine, it's no longer eating the caterpillar... eating the plant anymore.
00:37:44.09 And that means that the caterpillar is out of its... out of the concerns of the plant,
00:37:49.13 and the plant, if it had waited and stored resources somewhere else, it was able to reflower
00:37:55.05 and start that whole process over again without having the tissues being lost.
00:37:58.24 And this is what is happening.
00:38:00.19 When... and this is work done by Jens Schwachtje, and his PhD project, and he discovered that
00:38:06.24 the FACs in caterpillar's spit, they elicit a bunkering of photoassimilates into the roots.
00:38:13.20 Now, a plant is a growth machine, right?
00:38:15.22 It's assimilating carbon dioxide from the air and, normally, it would be fixing those...
00:38:20.24 that carbon dioxide into sucrose and sending it from source leaves up to sink leaves to
00:38:25.17 grow more leaf area to make more of a growth machine -- that's what plants normally do.
00:38:30.00 But if they're making more of a growth machine, they're also making more leaves for the caterpillar
00:38:34.03 to eat, grrr...
00:38:35.03 So, you need to stop that process.
00:38:37.12 And when you have a caterpillar on the plant, or you put FACs on a plant, and it doesn't
00:38:42.18 matter where on the plant, the plant, instead of taking that fixed CO2 and sending it up
00:38:48.07 to young sink leaves, it bunkers it down below ground.
00:38:51.15 And it... and Jens was able to show this with some beautiful experiments in collaboration
00:38:56.04 with the Phytosphere Julich, which has a synchrotron, is able to make C-11 carbon dioxide.
00:39:01.09 C-11 has a half-life of 15 minutes, so you have to be right close to the synchrotron
00:39:05.14 -- you can't ship it very far -- and it allows you to look at very short-term partitioning
00:39:10.21 of carbon in a plant after it's fixed and where is it moving and where it moves it around.
00:39:15.14 And here's just some of the data from Jens' work.
00:39:17.23 He was able to show that... up is transport of C-11-labeled CO2 into young leaves, and
00:39:26.03 you can see that it goes... when you just wound and water a plant... and you treat the
00:39:31.14 wounds with water... the fixed carbon dioxide goes up the plant, but if you add spit to
00:39:36.18 the wound it goes down.
00:39:39.08 And it's the specific FACs in that spit that cause it to go down.
00:39:45.13 And he was also able to show that there's a particular subunit of a SnRK kinase which
00:39:49.24 is regulating that.
00:39:51.01 This is this GAL83 subunit that is down-regulated by the FACs.
00:39:55.06 And that's sort of the... the master sink-source regulator, the genetic element that... that
00:40:01.21 is causing this response.
00:40:04.15 And that bunkering, having put that carbon down below ground into the roots, allows the
00:40:09.13 plant to reflower, make bigger flowers, after the caterpillar has gone.
00:40:14.21 So, in many ways this level, this response, this number five, is a man... is the kind
00:40:21.12 of response that Mahatma Gandhi would have against a predator.
00:40:25.17 You just sort of lay low and let it go by, and don't engage in a fight, but just regrow
00:40:32.18 and be able to start again.
00:40:37.24 The sixth layer and the last layer is probably the most intriguing layer.
00:40:42.19 It's a type of avoidance of this herbivore and it's an avoidance response that has...
00:40:50.11 has to deal with a fairly common natural history problem that... that all organisms have.
00:40:55.16 And that is that some of their interactions are with good guys and some of them with bad
00:40:59.00 guys, and sometimes the good guy and the bad guy are a part of the same genome.
00:41:03.00 So, this moth is a good guy -- it's a pollinator for the plant -- but it lays eggs that are
00:41:09.05 bad guys, that grow into little herbivores that sometimes turn into very big herbivores,
00:41:13.12 that are very disastrous for the plant.
00:41:16.00 And the sixth response has to do with... with dealing with this herbivore by dealing with
00:41:22.07 its mother, its pollinator.
00:41:24.21 Now, I told you in session 1 that this is a plant that attracts that pollinator by producing
00:41:32.23 a compound called benzylacetone, which is depicted up there above the flower, and...
00:41:37.16 and what Danny Kessler discovered is that when the moth is attracted by that particular
00:41:44.22 structure of benzylacetone, not only is it attracted because of the nectar, it nectars
00:41:50.09 and then it oviposits.
00:41:51.17 So, nectaring and ovaposition are linked processes; the more they get nectared by and more visited
00:41:58.16 by this pollinator, the more eggs show up on the plant.
00:42:02.08 The eggs of course turn into herbivores and therefore the more pollination services you
00:42:06.20 get, you might end up getting more herbivores, if the other types of defenses I've talked
00:42:11.12 about earlier aren't effective in cleaning out those herbivores and getting rid of them.
00:42:16.13 Now, we were able to silence benzylacetone production and when we do that we know that,
00:42:21.23 if the plant is not producing benzylacetone, it's pretty much ignored in terms of pollinator
00:42:27.19 activity, and also ovaposition activity by the moth.
00:42:32.05 And Danny Kessler, who is a remarkable photographer but also a remarkable observer of natural
00:42:39.06 history, noticed that attacked plants, when you looked at this... let's do it again at
00:42:43.18 this day night transition... that the plants were beginning to produce a different type
00:42:49.18 of flower after they were attacked.
00:42:52.07 They were producing their normal night flowers, but then they started, when they were attacked,
00:42:55.18 producing a different type of flower that was really only opening in the morning.
00:42:59.24 Now, here is the difference between the morning-open flower on the bottom and the night-open flower
00:43:05.12 at the top.
00:43:06.21 The normal flower is the night-open flower, the one here.
00:43:10.18 And you can see that it opens up in the first night open, and it opens and scents and attracts
00:43:15.22 the moth, and then it closes a little bit for the day, and then opens again and attracts
00:43:19.24 the moth again for the second night.
00:43:22.04 The morning-open flower stays closed that first night.
00:43:25.22 It doesn't scent.
00:43:27.04 And it doesn't attract any moths.
00:43:29.04 And then it opens up just slightly in the next morning, and it attracts a different
00:43:35.13 pollinator, and this is the pollinator -- a hummingbird.
00:43:39.10 And the hummingbird has a very nice characteristic that it lays hummingbird eggs, not caterpillar
00:43:47.12 And by switching its sexual system to a different pollinator, asking for a different type of
00:43:53.20 postman to bring gametes to you, the plant has basically solved its herbivore problem.
00:44:00.21 And that's pretty remarkable.
00:44:03.07 So, what I've done is told you about all of these changes that occur in the plant when
00:44:10.10 it perceives these compounds here that are in the spit of the plant... the spit of the
00:44:15.13 caterpillar as it chews on... on the plant, and elicits this very complex defense avoidance
00:44:20.14 and tolerance responses.
00:44:22.10 And what I've also told you, I hope... there's basically three messages in behind this remarkable
00:44:28.22 transition that occurs in the plants when it sees these spit factors.
00:44:33.04 The first, of course, is that direct defense is not the only way of coping with herbivores,
00:44:37.10 and most of our agricultural practices dealing with protecting our crop lands have to do
00:44:42.01 with direct defenses -- insecticides that directly kill the crop press... the crop pests.
00:44:48.10 Now, as we've learned from this story, there's many other ways of dealing with your herbivore.
00:44:53.14 And we should be thinking about how to incorporate some of those many other ways into our cropping
00:44:58.11 systems, because some of them may well be much more evolutionary stable than just using
00:45:02.22 direct defenses alone.
00:45:05.10 The second main take-home message that I want to get from this is this interplay of the
00:45:09.08 importance of knowing mechanism so that you can use mechanisms to be able to manipulate
00:45:16.12 And when you can manipulate function you can begin to ask, in an unbiased way, what is
00:45:21.03 actually happening in nature between plants and insects, and all the other interactors.
00:45:26.23 And the third main message I want you to get from this is that you can observe an awful
00:45:32.02 lot by just watching.
00:45:33.15 Now, this little tautology is something from Yogi Berra, but I think it applies so cogently
00:45:40.14 to biology today, because we don't teach our students how to watch, particularly not natural
00:45:49.06 interactions, anymore.
00:45:50.06 This is not part of our biological training programs.
00:45:53.08 And so much of the innovation that I've just shown you comes from simple natural history
00:46:03.11 So, in the third part... that was the end of the second part, in the third part I'm
00:46:08.02 going to talk about seeds, sex, and microbes.
00:46:11.08 In Part 1, I told you that this is a plant that chases fires, it produces seeds that
00:46:16.13 have to live in the seed bank for hundreds of years before the next fire comes along,
00:46:21.09 and I'm going to be talking about how it uses sex to get the best genetic material, to be
00:46:25.24 able to survive that long-time period of... as it waits for the next germination event,
00:46:33.08 and also how it recruits microbes when it does decide to... to... to germinate in opportunistic
00:46:39.08 mutualisms to help protect it against all sorts of stresses that you could hardly predict
00:46:43.14 if you had been in the seed bank for hundreds of years.
00:46:46.07 So, I want to thank you for your attention, but I particularly want to thank both the
00:46:51.04 funding organizations that make this work possible, the long-term, patient funding of
00:46:56.00 the Max Planck Society, and the grants we received from these wonderful agencies that
00:47:01.02 are so unbureaucratic in their administration, and really promote curiosity-driven science
00:47:06.12 in the best way possible.
00:47:07.23 I want to thank the folks at Brigham Young University, particularly Dr. Larry StClair,
00:47:12.22 Ken Packard, and Heriberto Madrigal, that make this wonderful interaction with that
00:47:17.23 remarkable University work, and allow us to use their Lytle Ranch Preserve as a laboratory
00:47:24.09 to study, for the site of these field interactions.
00:47:27.01 And I want to talk...
00:47:28.01 I want to thank all the people who have provided the stunning pictures and movies, the talented
00:47:34.13 photographers and... and folks in the group who have helped support and make some of these
00:47:40.07 And, particularly, Erna Buffie and Volker Arzt, who are really masters of translating
00:47:47.22 science, making beautiful movies, and allowed us to use many of their outtakes from their
00:47:53.03 movies in this presentation.
00:47:55.08 And, you, for your attention.
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Dr. Ian Baldwin is a professor and director of the Max Planck Institute for Chemical Ecology where he studies the Nicotiana attenuata as a model organism to understand how plants solve ecological problems. Baldwin received his AB in Chemistry and Biology from Dartmouth College in 1981 and started his graduate studies at Cornell University where… Continue Reading
Dr. James Estes is a Professor of Ecology and Evolutionary Biology at the University of California Santa Cruz. He completed his undergraduate degree in zoology at the University of Minnesota, a M.S. in biology at Washington State University, and a PhD in biology and statistics at the University of Arizona. Estes is known for his… Continue Reading
Jared Leadbetter was an undergraduate biology student at Goucher College when he attended a summer course on microbial diversity at the Marine Biological Laboratory in Woods Hole, Massachusetts. It was here that he first became fascinated with the amazing environment of the termite gut. Leadbetter went on to study termite gut microbes for his PhD… Continue Reading
Dr. Margaret McFall-Ngai is a Professor and Director of the Pacific Biosciences Research Center at the University of Hawaii Manao. Her laboratory studies the symbiotic relationship between hosts and microorganisms. She uses the Hawaiian bobtail squid as a model organism and studies its symbiotic relationship with the bacteria Vibrio fischeri. McFall-Ngai uses this binary symbiosis… Continue Reading