EEB 122: Principles of Evolution, Ecology and Behavior?

Lecture?20. Coevolution

https://oyc.yale.edu/ecology-and-evolutionary-biology/eeb-122/lecture-20

This is a Proboscis fly that lives in South Africa?and it pollinates flowers. 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. The fly?is not at all closely related to moths, and that flower is not at all closely related to orchids. So this is convergent evolution.?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. It is a?coevolutionary story.

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

• Now the tight genetic definition of coevolution is this. In one species you have a change in a gene, and 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.?

• It's hard to do experiments since?we don't?know what the genes are that involved. We can see the phenotype, but we have difficulty inferring the genes. There are some cases that are well documented in rusts, rust fungi inhabiting wheat;?such as?Ustilago hordii.

• Another kind of coevolution is phylogenetic. 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--to see if the trees can be laid right on top of each other.

• If you have one group of?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.?

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?each other?in order to generate a well-functioning hypercycle.?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.?

• Every single important biochemical step and morphological structure inside the cell is tightly co-adapted, so that form matches function, throughout the cell.?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. 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.

• At a slightly higher level in the cell, you can find co-adaptation 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, such as?electric eels.

• 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.?

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. According to biologists,?coevolution?usually?refers to the mutual adjustment of the genomes of separate species.?

It's arbitrary as?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.?

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, as presented?in mitochondria and chloroplasts.

• These tight symbioses are really major transitions in the process of being born. 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.?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.

• That performance can vary among units, and therefore natural selection is starting to act on the new unit. 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.?

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.

• 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.?

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?in that large chunk of the tree, which is called the ecdysozoa.?

• For?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?sperm.

• It?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.

• They get into the eggs of all of them. They can feminize male hosts, when Wolbachia gets into Armadillidium, an?isopod?and a crustacean,?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.

• It?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. 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.

• 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.?

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?because now there's a new Sex chromosome.

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 with?the same Wolbachia in it. They have learned how to manipulate the Sex ratios and mating success of their hosts?and haven't been domesticated.?

There has been a?period of?15 hundred million years since?mitochondria?first started getting into the eukaryotic lineage.?It probably took some time to resolve conflicts and really to integrate the mitochondria into the eukaryotic lineage.?

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.

• Ecological interactions, that favor strong coevolution and specialization.

• Parasite host interactions, which?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.

• Another interaction that favors specialization is mutualism, where you have interactions that are already positive, or becoming positive. They have symmetrical impacts on reproductive success, and these things are living in intimate contact for?their life cycle. Evolution is not always about competition. Evolution can be about both sides profiting from the interaction and that ends up in a mutualistic relationship.?

So the relative evolutionary potential basically is determined first by generation time and?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.?

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.?

• 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.

• 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?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.?

Leigh Van Valen is a paleontologist?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.?There's some slight evidence that?species may?have started to live a bit longer. But, broadly?this claim is correct. Things have not gotten better at persisting, over the last 500 million years. Everybody is running as hard as they can and they're just staying in place; their fitness is not long-term improving.?

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.?

Let's start with mimics and models. In Batesian mimicry,?the noxious one is going to be the model, and the edible one is going to be the mimic.?

• On Madagascar there aren't any models, and the male and the female look the same in this species. But 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 other things, depending upon where they are, in Africa.

• It takes a lot of genes to turn something like that into something like that,?you have to have a whole bunch of coordinated changes to make it into the other one.?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.

In Mullerian mimicry you have a process whereby things that all taste bad evolve to look like each other. They're making it easy?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.?

Now a tight symbiotic relationship is?between dinoflagellates, that are called zooxanthellae, and their corals.?

• 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 producing photosynthate; and these are the starches that it's accumulating.

• The dynoflagellates, which by the way look like this when they're out in open water; they're really quite lovely. They?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, only?about .2 into growth and 25 into respiration. So they've been almost completely domesticated.?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 1/10th?of their energy from feeding directly; they get most of it from photosynthesis?and then?put a little bit of it into growth. They put a lot of it into their calcified skeleton--so basically?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.?

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.?

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.?

Now for a macroevolutionary, coevolutionary story. Leafcutting ants?form huge colonies. The chamber that they can form 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. They take them into?underground chamber, where they chew them up and they feed them to a fungus. And they domesticated this fungus 50 million years ago. It?is a?domestication event.?

• 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.

• That's not what the leafcutter ants did. They have a pathogen that can attack their own?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've evolved a special morphological pouch in which they carry this bacterium.

• And 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 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.

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. It's not absolutely precise, but these things match up pretty well.?

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.?

• 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?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.

• 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. 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. So it started causing a cascade of effects, through the ecosystem. There were epizootics,?epidemics that?happens in populations of wild animals.

• There were some?indirect consequences. So over a lot of the infected area, tsetse flies disappeared?since 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.

• 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 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.?

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.?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.?

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.

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.?