Principles of Evolution, Ecology and Behavior

E&EB 122 - Lecture 20 - Coevolution

Chapter 1. Introduction [00:00:00]

Professor Stephen Stearns: Welcome Orgo survivors, and others. I stuck this slide up, sort of outside the framework of the regular lecture, and I did so just to indicate that if you go through the scientific literature, you can probably find a neat case of coevolution, with some kind of beautiful biology in it, coming out every week. This one came out last week.

This is a Proboscis fly that lives in South Africa, and it pollinates flowers. And you can see that it has evolved a very long proboscis, and the flower has evolved a very long nectary, and it looks, in fact, very much like Darwin’s orchid, and that moth called Praedicta, that Darwin predicted would have a long proboscis. But this is a fly. This is not at all closely related to moths, and that flower is not at all closely related to orchids. So this is convergent evolution.

And I think you’ll remember, in reading the book, that there was a neat alternative hypothesis posed in the book saying, “Hey, it wasn’t about the coevolution of the flower and the moth. There’s a spider that sits on the orchid, and when the moth flies in, the spider tries to eat the moth; and so the moth kind of evolved a long proboscis so that it wouldn’t touch that flower with anything but a ten-foot pole. Okay? So that was an alternative hypothesis, and there’s actually some evidence for that in the case of the orchid on Madagascar.

But in the case of this interaction, which is in Cape Province in South Africa, with a fly and something that is not at all an orchid, the data indicate that, in fact, a coevolutionary story works just fine; and that looks to be what’s going on. The longer the nectary, the more likely the pollination; the longer the proboscis, the greater the energetic reward–and the two things feed back and forth to each other.

So this indicates actually that Darwin’s original idea was probably correct. And I would note that in the case of the orchid on Madagascar, the fact that there’s a spider doesn’t really mean that Darwin was wrong in generating his story, it just means that there is also something else going on.

Okay, so. We spent the first part of the course talking about microevolution. We spent the second part of the course talking about macroevolution. And today and Monday, we’re going to talk about coevolution and evolutionary medicine as two areas in which micro and macroevolution interact in generating explanations of things.

And I think that you’ll probably see, if you think about it, that in almost any reasonably complicated or large-scale biological pattern, both things have been involved; both micro and macroevolution. There’s been some things that have been changing slowly and some things that have been changing quickly.

Chapter 2. Definitions of Coevolution and Intra-organism Analogies [00:03:20]

Now the tight genetic definition of coevolution is this. In one species you have a change in a gene, and that–excuse me for missing this; I was doing proofreading this morning; there should be ‘t’ there–it stimulates an evolutionary change in a gene in the other species, and that change in the other species stimulates another change in the first species; so that you have kind of a gene for gene succession in time. One thing happens here; that stimulates something here; that stimulates something here.

That is the tight genetic definition of coevolution. If you could demonstrate that, I think everybody would agree, hey, you nailed it, it’s really there. It’s hard to do. The reason it’s hard to do is that we don’t normally know what the genes are that involved. We can see the phenotype, but we have difficulty inferring the genes. There are some cases of this that are well documented in rusts, rust fungi inhabiting wheat; Ustilago hordii is one of them. So, you know, pathogens of crop plants are things where this kind of coevolution is well documented.

Another kind of coevolution is phylogenetic. So you use tree thinking to try to infer what’s been going on. And you look at closely interacting organisms–pathogens, parasites, pollinators, things like that–and you see if the trees can be laid right on top of each other.

Or, if you have one group over here–so you have, say, the pathogens over here and you have the hosts over here–you see if the trees line up and touch each other at the tips. That would indicate–without any crosses, so you don’t see any lines kind of crossing over when you line them up–that would mean that the trees have exactly the same topology, and that every time the host speciated, the pathogen speciated. And if you see crossing lines, it means that a pathogen has jumped from one host to another. So that kind of approach gives you another definition of coevolution, and another tool for trying to infer it.

Now before I get into coevolution proper, I want to talk a little bit about co-adaptation, because co-adaptation actually contains within it a message that’s of general significance for coevolution. Right at the beginning of life, the first replicators had to co-adapt in order to generate say a well-functioning hypercycle; they had to co-adapt to each other. And at the level of the cell, when you’re looking at key molecules in the cell, all these interactions have co-adapted to each other.

So, for example, the ribosome here is in green, and you’ve got the mRNA coming into it like a ribbon, and you’ve got–the transfer RNA is pulling in the amino acids out at their tips, into the reaction center of the ribosome. And that brings the amino acids into close juxtaposition where an enzyme can operate on them to join them, and then clip them off of the incoming tRNAs, which then go on out, back into the cell to do their job again, and the protein grows out here.

Well, this is a rough sketch of the structure of the ribosome. It’s actually more complicated than that, and it has really a beautifully sculpted reaction center in the middle of it. And the message from this is that every single important biochemical step and morphological structure inside the cell is tightly co-adapted, so that form matches function, throughout the cell.

And the reason that’s the case is that these things are processing reactions that happen thousands of times a second, and that therefore accumulate to have big effects over the lifetime of the organism. If you’ve got something in you that is going to happen say 50 billion times in your lifetime, and you get a very, very tiny, 1/1000^th of 1% change in it, that then accumulates 50 billion times, you have a massive result at the end of your life. So that things that are happening down at that level are driven by high frequency interactions. And the frequency with which things interact is one of the key elements of coevolution, in general.

If you look at a slightly higher level in the cell, you can find co-adaptation going on again. The axons that run into nerve fibers have different lengths, so that the signal coming from the brain will arrive at things that need to be coordinated at the same time. The muscles in electric eels have been turned into storage batteries, and the axons that run from the brain have had their lengths modified, so that they hit the different cells in the storage battery at exactly the same instance, so that the electrical charge goes out, all at the same time.

A four- or five-foot electric eel can kill a horse; that’s how much electricity they can store up. But they can only do it because it’s released exactly at the same time. If it dribbled out, it wouldn’t take the horse down; or the naturalist exploring the shallow river in South America. Right?

Same kind of thing in your brain. There’s very tight co-adaptation between your retina and its projections into the visual cortex at the back of your brain. So these connections have been sculpted by evolution so that the re-creation of the external world, in your head, is precise. And this has gone on in every organ of your body in one way or another. So the integration of the organism is achieved by co-adaptation of its parts.

That’s not precisely the gene for gene kind of interaction between species, that people think about in coevolution, but it is a gene for gene interaction in the determination of those organ systems. A gene changes over here, and another gene has to change over there. It’s just that the process is going on inside a single genome, rather than in two different genomes.

So that’s not normally what biologists mean by coevolution. It usually refers to the mutual adjustment of the genomes of separate species. And that’s kind of arbitrary I think, and the reason I think it’s arbitrary is that we now conceive of the organism as kind of a babushka doll of nested levels of hierarchies that have been assembled over the course of the evolution of life, and that things that we now see as being integrated organisms, earlier, were independently evolving systems, and at that point the coevolution, that we now see as co-adaptation, was actually coevolution sensu strictu.

Chapter 3. Symbioses and Parasites [00:10:37]

So I’m now going to talk about some intercellular symbioses. And the reason I picked intercellular symbioses as the first example of real coevolution is that these things are very intimate coevolutionary interactions. And you can see that in mitochondria and chloroplasts of course.

Then there’s this wonderful and interesting critter called Wolbachia, that does lots of things to arthropods. The whole issue of the symbiosis of algae in reef building corals contains a lot of beautiful biology, and some interesting puzzles. And in all of these cases the interacting parts are really closely connected. Okay? So there’s been a lot of evolution at the level of intercellular metabolism.

And I think that these tight symbioses are really major transitions in the process of being born. So one of the issues in a major transition is whether or not you have a change in the pattern of genetic transmission. And in these cases independent genomes are getting aligned, and in the extreme case of mitochondria or chloroplasts, they actually have the same pattern of transmission as the maternal nuclear genomes, of the host. Okay? So previously independent things are being integrated.

Conflicts are being at least partially resolved; although there are traces of these conflicts–as I told you earlier, there are mitochondrial cancers; mitochondria do occasionally get out of control. And there are things like the petite mutation in yeast, which is a mitochondrial issue. And then this new more or less well integrated unit has a performance.

That performance can vary among units, and therefore natural selection is starting to act on the new unit. So at the formation of the eukaryotes, when the mitochondria came in, you had a new unit, and then it was going to perform with respect to other such units, depending on how well the mitochondria were adapted to the nuclear genome; and that’s a coevolutionary process.

Okay, so with mitochondria you’ve got all kinds of communication and coordination going on. The cell membrane of the previously independent purple sulfur bacterium, out here, now has within it an inner membrane that has got all kinds of biochemical machinery on its surface.

And this is where the citric acid cycle takes place, where electrons go down the electron transport chain, making ATP, and in the process letting a few protons leak out into the cytoplasm, which cause oxidative damage. So if you are worried about eating your blueberries and drinking your pomegranate juice, it is because mitochondria leak protons and basically create hydrogen peroxide in your cytoplasm, and hydrogen peroxide is highly oxidative and can do damage in the cell; and there’s lots of kinds of repair machinery to deal with that.

This process here of exporting energy to the cell and getting information and substrate into the mitochondrion is a tightly coordinated one, and there have been lots of modifications to the mitochondrial membrane to make it an appropriate filter for the transport of goods, in and out. So it’s been heavily modified by coevolution.

Now, Wolbachia. Wolbachia are very cool bacteria. They’re cytoplasmic parasites. They live in the cytoplasm of arthropods. So they occur in insects and crustacea. They sometimes occur in nematodes. They seem to be able to get into things, generally speaking, in that large chunk of the tree, which is called the ecdysozoa.

And if you just think about the interests of the Wolbachia, it can only get into the next generation if it is in a female, because it is transmitted, like other cytoplasmic organelles, only through eggs and not through sperm.

Now this creates some issues for Wolbachia, because if they end up in a male, they’re dead. So they have evolved some interesting ways out of that. They can induce parthenogenesis, in some species. So they will take that female and they will make her asexual, and then she makes only female babies.

So they get into the eggs of all of them. They can feminize male hosts, in pill bugs–so Armadillidium, the little pill bug that you can find turning over logs–it’s an isopod and a crustacean–and when Wolbachia gets into Armadillidium, basically it takes males, and it has developed a method of interfering with its sex determination process and development, so that anything that’s got a Wolbachia in it will grow up to be a female.

Now, as Wolbachia–and by the way, this creates a huge reproductive advantage for those females, and they start to spread through the population. They’re not suffering the twofold cost of sex. They’re only making female children. They spread, and they take over the population. And then, because there aren’t any males in the population, and it’s still a sexual species, Armadillidium goes locally extinct; being driven to extinction by the selfish cytoplasmic parasite that it has.

And the response of some, but not all, Armadillidium populations has been clever. They have cut out the sex determining part of the bacterial chromosome and put it into their nucleus and spliced it onto one of their own chromosomes, so that there is now vertical transmission of that selfish, sex-determining element. They don’t really care very much about the rest of the bacterial genome that’s been causing all this problem.

The only thing that’s really critical is that they got the sex determining part out, and they spliced it into their nuclear genome, through a process that we don’t really understand. All we can see is that we can observe, in some populations, that today that’s the case.

This means that the conflict has been removed, at least for that sex-determining element, because now it’s being vertically transmitted through both the male and female line, because it’s in a nucleus. So the conflict disappears, and a 50:50 sex ratio is re-established; well after awhile, because now there’s a new sex chromosome. Okay?

So now you have three sex chromosomes, rather than two, for awhile, and so there’s a bit of chaos in sex ratios. And then that stabilizes; you get back to 50:50 sex ratios. And then it gets infected by Wolbachia, and the whole thing starts over again. And in some cases you can take the genome of a Armadillidium pill bug, and sequence it, and you can find four or five fossilized, sex determining chunks of DNA, that have been stuck into it. So there’s an interesting coevolutionary process going on there.

In fruit flies and drosophila, they cause reproductive isolation, and they do that by cytoplasmic incompatibility. That means that a fruit fly is only going to be able to have offspring, if it’s mating with a Wolbachia infested fruit fly, if it’s got the same Wolbachia in it. So Wolbachia are biochemical geniuses and developmental geniuses. They have learned how to manipulate the sex ratios and mating success of their hosts, and they really haven’t been domesticated.

And this is kind of interesting if you go back to the whole issue of well what happened when mitochondria first started getting into the eukaryotic lineage? Was there a period 15 hundred million years when this kind of stuff was going on? Probably was. It probably took some time to resolve conflicts and really to integrate the mitochondria into the eukaryotic lineage.

Chapter 4. Principles of Coevolution [00:19:09]

So when we think about that overall process of interacting genomes, as I mentioned the frequency of interaction is really quite important. You’re not going to get tight co-adaptation of two different species unless they interact with each other very frequently.

If they’re only interacting with each other occasionally, then there’s a lot of stuff going on, outside of the interaction, that has costs and benefits, that is going to be tweaking the interaction traits in other directions. So it’s got to be a very consistent and persistent process, to result in tight co-adaptation. So frequency is important.

And then, of course, when they interact it must make some difference to reproductive success. Then there’s the issue of relative evolutionary potential: who’s got the bigger population size; who has the shorter generation time; who has more genetic variation? Those things are certainly going to help determine the outcome. And then there’s this issue of the Red Queen, which I will come to.

So there are some kinds of interactions, ecological interactions, that favor strong coevolution and specialization. Parasite host interactions, especially where the–this is normally a case where the whole live cycle is completed on a single host; plant/herbivore and predator/prey interactions, where you have got a fairly narrow range of species that are being eaten by the herbivore or by the predator.

And there’s one here–pandas just eat bamboo, and therefore that sixth appendage, the panda’s thumb, which is there for handling the bamboo shoot, has evolved. Sage grouse basically just eat sage–they’re herbivores–and sage has an awful lot of upsetting biochemistry in it. If you were to go out into the American West and try to live for a week on sage, in the Great Basin, you would become very sick. Sage grouse do it just fine. They’ve got all kinds of–it’s probably Cytochrome P450s that are the enzymes that are denaturing the plant products that would make us sick.

But the one which is really kind of sad and funny is the aardwolf. The aardwolf is a hyena that has specialized on eating ants and termites; that’s the only thing it eats, as an adult. Baby aardwolves grow up with milk, from mom. And my friend, Tim Clutton-Brock, has watched the weaning process in an aardwolf, where mother is trying to convince baby to switch from milk to ants. [Laughter] And baby is not happy. Those ants do not taste good. And fortunately baby probably doesn’t realize that this is the rest of life; from here on out it’s ants, all the way through. Okay? So that’s real specialization.

Another interaction that favors specialization is mutualism, where you have interactions that are already positive, or are becoming positive. They have symmetrical impacts on reproductive success, and these things are living in intimate contact for most or all of their life cycle. And mutualisms are very interesting and they make wonderful natural history, but they also carry the message that where it’s a win-win situation, evolution is not always about competition. Evolution can be about both sides profiting from the interaction and doing better because of it, and that ends up in a mutualistic relationship.

So the relative evolutionary potential basically is determined first by generation time; second by sexual mode. Sexual partners can evolve more rapidly than asexual partners, and the partner that therefore has more genetic variation, for the interaction trait, will evolve more rapidly. So to some degree we kind of predict how the coevolutionary process will occur.

Now the Red Queen, which comes from Through the Looking Glass, by Lewis Carroll–and I’ll go into that a little bit more–is the idea that there is an open-ended struggle that results in no long-term reduction in extinction probability.

Here’s an example of a Red Queen process; there are many. But this would be a host/parasite interaction. And what you see here is generation time for things that have about the same generation time. Okay? So we have a host and a parasite that have roughly the same generation time.

This is the frequency of an allele. And these are interaction alleles. So these are genes that are determining how well that parasite will do on this host, and how well this host will resist that parasite. And what’s going on here is that when a certain host allele goes up to high frequency, that turns out to be one that this orange parasite allele can attack very well. And so the host has gone into a state that’s susceptible to parasite attack; therefore that parasite allele increases in frequency.

But, because that parasite allele is going up here, it’s killing a lot of hosts up here, that host allele drops in frequency. As soon as that one drops in frequency, it makes the host less susceptible, and the parasite allele drops in frequency. And you can see there’s a lag, there’s a lag time between the two. Here it’s sketched at about two or three generations. So this light rectangle here is indicating where the host is not having a problem, and the grey rectangle is indicating where the host is having a problem.

So Leigh Van Valen is a paleontologist at the University of Chicago who came up with the Red Queen hypothesis in 1973. And he claimed that in fact it’s not just hosts and parasites; he claimed all life on earth is in fact caught up in a coevolutionary web of interactions. And his evidence for that is that the long-term extinction rate is constant. If you look over the Phanerozoic, if you look over the last 550 million years, the probability that a species will go extinct, within a given period of time, has remained roughly constant.

There’s some slight evidence that maybe species have started to live a little bit longer. But, you know, broad brush, this claim is correct. Things have not gotten better at persisting, over the last 500 million years. So in some sense I think Leigh’s claim is probably true. Every time a species on earth tries to get a leg up, some other species compensates. So this is where that term comes from. This is an illustration from Through the Looking Glass by Charles Dodgson (Lewis Carroll). This–Alice is a pawn on a chessboard, and Alice is supposed to, in this mental game, march down the chessboard and get turned into a queen, when she reaches the end.

And the Red Queen, who is next to her, says, “Alice, this is a game in which you run as fast as you can and you can only stay in place.” So it’s like one of those nightmares that you have, where you’re running as fast as you possibly can, and you can’t get away. That’s Leigh Van Valen’s metaphor for evolution: everybody is running as hard as they can and they’re just staying in place; their fitness is not long-term improving.

Chapter 5. Coevolutionary Mimics and Models [00:26:56]

Now I’d like to give you a few striking outcomes of coevolution. I’m going to do butterfly mimics, reef-building corals, leafcutter ants, and rinderpest. And each of these is making a slightly different kind of point, but each of them involves some absolutely stunning natural history. So let’s start with mimics and models.

And these guys are, by the way, all from the Peabody Museum Collections. So, you know, if you love butterflies, you can go over and talk to the invertebrate curator at the Peabody Collections, and he can pull out tray after tray after tray of thousands of beautiful butterflies. We had one of the great butterfly biologists here, Charles Remington. And he was buddies with Vladimir Nabokov, who not only wrote Lolita, but was a lepidopterist, and so we’ve got some Nabokov butterflies in the collection as well. I don’t know if any of these are from Nabokov. Okay?

So in Batesian mimicry you’ve got an edible model that evolves to resemble a warningly colored noxious species. Okay? So actually what’s going on–I’ve actually misphrased that a little bit. The noxious one is going to be the model, and the edible one is going to be the mimic. Sorry about that. I’m going to go back and correct that. So the mimic is good to eat and the model is bad to eat.

And on Madagascar there aren’t any models, and the male and the female look the same in this species. But as you go out, through Africa, you find that in different places in Africa there are different nasty tasting models, and the female turns into something that looks very much like them. So this thing has evolved into all of these other things, depending upon where they are, in Africa.

Now this is not simple. It takes a lot of genes to turn something like that into something like that. And when you go into a neighboring race–it’s still in the same species; the males are still looking like that–you have to have a whole bunch of coordinated changes to make it into the other one.

So what’s happened is that these genes have been pulled together, onto a chromosome, and turned into a super-gene complex, which has been inverted so that it doesn’t recombine, and they’re inherited as a package.

Now in Mullerian mimicry you have a process whereby things that all taste bad evolve to look like each other. Can anybody tell me why things that all taste bad might evolve to look like each other? What’s the advantage in that? Yes?

Student: [Inaudible]

Professor Stephen Stearns: Right, exactly. So basically what they’re doing is they’re making it as easy as possible for the predator’s learning process to figure out that all things that look like this taste bad. They’re reducing the mistake rate, in the things that are learning not to eat them.

So these are the Heliconia butterflies of South America, and they live all on passion fruit vines. So there’s a big radiation of different species of passion fruit in South America, and these butterflies all lay their eggs on those different species of passion fruit, and where they overlap, the different species have evolved to look like each other.

So what we have here is Mullerian mimicry going on here, and here; and we have Batesian going on–excuse, me, this is all Mullerian; this is Batesian mimicry. So Mullerian is everybody distasteful. This is a Batesian mimic of all of these distasteful models. This is a Batesian mimic of all of these distasteful models; and so forth.

So, those are pretty precise adaptations. I mean, if it gets to the point where a good naturalist really has to puzzle for awhile to identify whether you’re looking- dealing with the model or with the mimic, and has to really know their details of morphology, it means that natural selection has precisely adjusted virtually every part of the body, so that the mimic really looks like the model.

Chapter 6. Coevolutionary Domestication [00:31:29]

Now a tight symbiotic relationship is between- is the one that’s between dinoflagellates, that are called zooxanthellae, and their corals. And there are also–so here is a coral. And, by the way, there are also zooxanthellae living in the lip of this giant clam.

So this giant clam and the coral are both farming algae. And the algae are photosynthesizing and delivering photosynthate, to the host. And you can see here the chloroplast of one of these algae, and its body is in here, and it is producing photosynthate; and these are the starches that it’s accumulating.

Now the relationship goes something like this. The dynoflagellates, which by the way look like this when they’re out in open water; they’re really quite lovely. And remember, these are some of the guys that have so many membranes around their chloroplasts, because they’re the result of three or four ingestion events over evolutionary time.

If they produce say 250 joules of energy, through photosynthesis, they export 225 of it to the corals; and they only put about .2 into growth and 25 into respiration. So they’ve been almost completely domesticated. Pig farmers have been trying for hundreds of years to get pigs that would be this efficient, for humans, and these corals have turned these dinoflagellates into a energy conversion machine that’s just incredibly efficient, from their own point of view.

The corals, of course, have tentacles, and they will feed on zooplankton and stuff which is out there, but they only get about 1/10^th of their energy from feeding directly; they get most of it from photosynthesis. And then what they do is they put a little bit of it into growth. They put a lot of it into their calcified skeleton–so basically you’re looking at where reefs come from; this is how a reef is produced–and then they lose quite a bit to respiration and to the mucus that they produce in their feeding. So they’re getting about ten times the energy from their symbiotic algae as they are from direct feeding.

Now one of the implications of this is this is why you do not find reef-building corals deeper than 20 meters. It’s because there’s not enough light for the algae, any deeper than 20 meters. Okay?

Now the crazy thing about this system is that a baby coral has to acquire the algae in each generation, and the algae exist as independent species. So the algae are actually incredibly phenotypically plastic; they have a free-living form, and they have a domesticated form, and they can reproduce both ways.

And that’s very interesting because from the point of view of the algae, the free-living form is the source and the domesticated form is a sink; and it’s therefore puzzling to see how it was that the corals were able to engineer the algae. There’s got to be some kind of coupling of the cycle so that what goes on in the coral feeds back into the free-living form; otherwise you couldn’t get this tight adaptation. They’re re-domesticated in each generation, in the coral.

Okay, now for a macroevolutionary, coevolutionary story. How many of you have been in the Tropics and have seen leafcutting ants? Four or five, six. These guys are great, and they form huge colonies. The chamber that they can form is the size of this dais up here. It will be three or four feet high, and if you’re out in a rainforest, the cutting activities of the workers will actually clear all the leaves off the trees, over the chamber, right to the canopy; so you kind of exist in a well in the forest, where the ants have essentially punched right through, 200, 250 feet up, taking out all the leaves.

And they take them down, into their underground chamber, where they chew them up and they feed them to a fungus. And they domesticated this fungus 50 million years ago. Okay? Humans figured out how to domesticate wheat 10,000 years ago. The ants domesticated the fungus 50 million years ago. They’re the first farmers; well the corals probably did it earlier. Okay? But this is another domestication event.

So they cultivate this fungus clonally. The fungus can’t reproduce sexually, in the colony, and it looks like it’s been asexual ever since it was domesticated. It’s a monoculture. Now in human agriculture, a monoculture is incredibly vulnerable to plant diseases. Having a continent covered by a single strain of wheat, or a single strain of sorghum, or a single strain of sugarcane is a bad idea, because pathogens will evolve onto that particular monoculture genotype, and they can go through in an epidemic and wipe the whole thing out. So having a mix of genotypes in agriculture is a very good idea.

Well that’s not what the leafcutter ants did. They have a pathogen that can attack their own–okay?–and it’s also a fungus. So there’s another fungus that can come into the colony and take over their own fungus. But to fight it, they cultivate a bacterium, and they use that bacterium as a defense against the enemy fungus. And they have a- they’ve evolved a special morphological pouch in which they carry this bacterium.

And you’ll notice that because it’s a bacterium, it has a short generation time. So they have the coevolutionary arms race matched up in terms of timing. They have a bacterium that can evolve as fast, or faster, than the fungus that infects them. So they have not only domesticated their food supply, they’ve also invented a health delivery system to keep it healthy; they have a pharmacy.

Now if you look at the macroevolution of this system, what you see here basically is the phylogeny of the ant, the phylogeny of their fungus, and the phylogeny of their parasite, over here. And the thing that I want you to notice is that although it’s not absolutely precise, these things match up pretty well. So the parts that are in blue–I mean, sometimes you find a few more parasites, hitting a few more cultivars, but roughly speaking if there’s a branch at a certain point in the tree, it is a branch for all three things. It’s not precisely matched, but it’s pretty close. This is an amazing system.

And when Ulrich Mueller, who has worked on it–and this is actually– he’s a co-author on this paper. He’s a professor at the University of Texas in Austin. When he visited and gave a talk on it, I asked Ulrich, “How did you come to this system?” And he said, “Well, about twenty-five years ago I took an OTS course, and we were sitting there in Costa Rica, and we played the 50 Questions game, and my question was about leafcutter ants.” And that’s his career. Okay? Questions have profound influence.

Chapter 7. Consequences of Coevolution and Conclusion [00:39:43]

Okay, rinderpest, the final one in this series. The point about rinderpest is this. I’m giving you this example to show you what happens when evolution has not occurred; and that gives you a feel for what has happened when evolution has occurred. Okay? So this is the rinderpest pathogen. It’s a virus, and it attacks cattle, buffalo, eland, kudu, giraffe, bushbuck, warthogs and bush pigs; those are all ungulates. So it is attacking one clade on the mammalian tree; they’re all things that have two hooves.

And it evolved in Asia, and it came into Europe through human invasions, repeatedly. So things in Asia and Europe had evolutionary experience of rinderpest; they’d been exposed to this disease. However, things in Africa had not, and it got into Africa probably either when the Italians went into Somaliland, or when General Gordon brought in some Russian cattle when he went to relieve Khartoum; so in the 1880s rinderpest got into Africa, and it came in because Europeans were bringing cattle in with them. And by 1890, it had crossed the Sahara, and gotten into Southern Africa.

So there were some direct consequences. It eliminated–in the 1890s it took out most of the domestic cattle and wild buffalo, and many related bovids. This caused enormous famine and disruption in the humans who were living in Africa and who either had domestic cattle or nomadic cattle. So, you know, the Masai really got hammered by this.

Only one species went extinct–it was a species of antelope–but the distributions of all of the other wild ungulates in Africa were altered, and they remain altered to this day. They’re springing back in some areas, and there are now vaccines for rinderpest that are being used on domestic cattle in places like South Africa. So the distributions are altering, but you can still see the signature of the event.

People lost food supplies, and there was an outbreak of endemic smallpox, while this was going on. So it started causing a cascade of effects, through the ecosystem. There were epizootics–an epizootic is like an epidemic, except it happens in populations of wild animals.

So there were epizootics in 1917/18; so right at the time of the outbreak of the World Flu Epidemic, people in Africa were also getting hammered by another outbreak of rinderpest hitting their animals. 1923; 1938 to ‘41. This is the kind of habitat in which rinderpest was spreading.

There were some interesting indirect consequences. So over a lot of the infected area, tsetse flies disappeared, and the reason tsetse flies disappeared is that they make their living off of wild ungulates. So if there aren’t any wildebeest or giraffes around for the tsetse flies to eat, they will disappear from the area. Now they require trees and bushes as their habitat, and herbivores for their food.

Now when the herbivores disappeared because of rinderpest, the tsetses lost their food, but their habitat sprang up, because there weren’t ungulates eating the bushes that the tsetse flies would live in. When things like wildebeest disappeared, the lions got hungry, and there were outbreaks of man-eating lions. So in the 1920s, during a rinderpest epidemic, there was one lion that killed 84 people.

When I first went to Queen Elizabeth National Park, in 1992, there were people living in the park, squatters living in the park, and they would try to get to the store at Park Headquarters, on a bicycle, and the lions had learned that it was possible to separate that blob on top of this funny two-wheeled thing, from what was moving so fast. And so like pussycats chasing balls of twine, they had gotten into knocking over bicycles and eating people, and there had been thirteen people who had been killed in the two months before we arrived, in Queen Elizabeth National Park. That kind of thing still goes on.

So the lions contributed to the abandonment of big areas, and thickets of brush grew up. So the ungulates went down, and the people pulled back, and the bushes grew. Now when the ungulates developed some immunity to rinderpest, and they moved back into the abandoned farming areas, they then became hosts for tsetse flies that could now live in the new bushes. Okay? So you see rinderpest goes in, and it changes a bunch of stuff ecologically, and it changes the geography of Africa.

And the flies transmit sleeping sickness; so they do that, by the way, both in the ungulates and–sleeping sickness is a real problem in domestic cattle, as well as in people. And so the humans really pulled out of this area, and they remained absent even after the lions switched back to eating the ungulates.

If you go into the Serengeti, just west of Seronera, there is a valley between Seronera and Lake Victoria, which is called The Valley of Death, and that’s because of the sleeping sickness that’s endemic in the valley; and that’s an example of what happens in this process. And by the way, we call these areas now, to a certain extent, the National Parks of Africa. So if you wonder why those parks are where they are, in part it’s due to the history that I just told you.

So rinderpest changed the ecological structure of at least half a continent, for about a century. The consequences were pretty bad, and they were only kind of predictable in retrospect. Nobody had the knowledge, when General Gordon relieved Khartoum, with a few Russian cattle in his supply train, that they were carrying a virus that would do this to a whole continent. Okay? I think that this is one of those places where we have to be extremely modest about how much we understand about ecology and evolution. Bad shit can happen.

So the same thing happened in the New World when Europeans, who were relatively resistant to smallpox and measles and things like that, brought with them their diseases, and that is why they were able to overthrow the Aztec civilization. If you ever ask yourself, how the heck did a couple of hundred Conquistadores wipe out an Aztec army of 100,000, the answer is the Aztecs were all sick and dying, and by the time the Conquistadores got to Mexico City, from Vera Cruz, the epidemic had spread ahead of them; and that happened all over the New World and all over Polynesia.

So the point of this basically is we want to compare what happened in Africa with what did not happen in Asia and Europe. The Eurasian ungulates have a long evolutionary history with rinderpest, and the ones that we see there are the ones that are not extinct; they made it. Okay? And if we summarize coevolution as a whole, there are lots of things that coevolve. It’s not just species that are coevolving with each other; it happens at many scales. And that means that other living things are among the most important elements of the selected environment.

So you shouldn’t think of organisms as being faced only by challenges of temperature and rainfall and stuff like that. Really, once life got going, the different species on the planet became each other’s most important interaction partners. Part of this is running just as fast as you can to stay in one place; and this Red Queen concept is probably particularly appropriate for the virulence resistance paradigm, and for the evolution of sex as an adaptation against parasites.

And as the rinderpest example shows us, the extent of coevolution is particularly strikingly revealed when you see a foreign species invade another continent after a long period of isolation. Okay.

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