14. Species and Speciation
EEB 122: Principles of Evolution, Ecology and Behavior?
Lecture 14.?Species and Speciation
https://oyc.yale.edu/ecology-and-evolutionary-biology/eeb-122/lecture-14
What is a species? How do they originate? What kinds of experimental evidence or observational evidence do we have to back up the claims about how they originate? What's going on during speciation, from the point of view of genetics; if we track the genes through the process of speciation, what do we see? And then there are some special issues: asexual species and cryptic species.?
We have wild diversity in the world. There's lots of different kinds of organisms?in discrete groups, separated from other such groups, and in many ways: appearance, behavior, ecology, genetics.?Ernst Mayr?profoundly influenced this kind of biology.?His definition of what a species is--this is from a version of a book that he wrote in 1963, but he had been working on this idea from about 1942, and his idea was that a species is a group of actually or potentially inter-breeding natural populations that are reproductively isolated from other such groups. It's the capacity for reproducing together that unites the members of a species, and it's the inability or the lack of opportunity to reproduce with individuals of other populations that marks the separation between species. There are cases where it doesn't apply. As a matter of fact, I think that biology has a profound capacity to erode the categories invented by humans.
There are isolating mechanisms that are common, they fall into three categories, and they look a little different in plants and animals.?
The first category is pre-mating or pre-zygotic isolation, and in plants that's often determined--not always but often--by pollinator behavior and flowering times, and in animals it is determined by mating behavior and gamete release. So here we have actually a place where sexual selection?connects into speciation, because who you choose as your mate is going to determine whether there's an opportunity for interspecific hybridization or not.
It is?an issue about mate choice, which is at a higher hierarchical level than the issue of should I choose my mate for resources or good genes or sexy sons or something like that.?Should I choose a mate, because in mating with that individual I will form hybrids or I will form members of my own species?
The second class of isolating mechanisms occurs a bit later; it's post-pollination or after insemination. And in plants there are--and actually in many algae and ciliates--there are self-incompatibility mechanisms. These are actually put in place through recognition molecules.?There's a lot of mate choice which is going on at the level of the sperm finding the egg and the egg sitting there and deciding, "Do I want this one or not?" Throw that one away and take another one. And these are mediated by well understood enzymatic reactions and protein structures; bindin and lysine. The self-incompatibility argument in plants basically has to do with the costs of inbreeding, and the costs of selfing.
And the arena in which that takes place is after the pollen grain lands on the style of the flower and starts to grow down the style, towards the ovary of the flower, the tissues that are in the style are checking out that particular pollen grain?as it grows down towards the eggs, and that is where the self-recognition is implemented. If its pollen is coming from that same plant, it'll get killed at that point.
After fertilization occurs, post-zygotic isolating mechanisms basically have to do with viability, survival and fertility. So hybrid inviability or infertility is a common thing, once two species have diverged to a certain extent. The commonest one is the mule,?a cross between a donkey and a horse, and mules are sterile. The same is true for ligers, crosses between lions and tigers.?In?fact female ligers do breed successfully with male lions. Male ligers are sterile.
However, at this stage, often fairly distantly related plants are able to hybridize. It's usually not across the boundaries of genera or families, but sometimes you can get plants from two genera hybridizing with each other, which may be an indication that the classification has been wrong. But plants generally hybridize a lot more easily than animals do, and it may have something to do with the differences in their developmental complexity. Usually the reasons for hybrid inviability in animals are developmental abnormalities.?
Species can be separated by various mechanisms and at various stages in the process of reproduction. Mayr gave us a biological species concept of?isolation. And there are plenty of others now. What each of these definitions does is try to define a species from a slightly different biological starting point. And what they're trying to do essentially is get the most general and useful definition that they can.
The recognition concept basically is based on mating systems. So species are things that will decide to mate with each other; that's Hugh Patterson's.
The phylogenetic species concept,?there are various ways of looking at the Tree of Life and deciding what on it constitutes a species.?Joel Cracraft said it's a cluster or organisms that are distinct from other such clusters, within which there's a pattern of ancestry or descent.
Back in '78 Wiley said that a species is a lineage of ancestor-descent populations that maintains its identity from other such lineages and has its own evolutionary tendencies and historical fate.?If you're looking at a phylogenetic tree, what he's saying is there's a start and a finish on a branch and?duration through time.
Back to the genetic cluster species concept, which is one that Jim Mallet put forth. Basically it says if you can get a lot of genetic data on the things that you're looking at, and you plot them out into gene space somehow, and you find that they form distinct clusters, then each separate cluster is a separate species.?
So we've got these concepts.?Why do they distinguish between?concepts and criteria? Because after all criteria are concepts. This is because they were trying to achieve kind of a local clarity in what they were talking about. So the?concepts?are more or less?general statements?about how you might go about thinking about?what a species is, and the?criteria?are?rules of thumb to decide?whether a thing is a species or not. So you can think of the concepts as being?abstract?and the criteria being?practical.?
So one would be, why are the things separated? Is there initial separation? And of course if we want to go into it, we can look at the causes, but maybe the most important thing is just that they're separated, not why.
We can look at whether the species is cohesive in some sense; there are different definitions of cohesion, but one is, is there genetic mixture? Are they breeding with each other? So cohesion has something to do with the biological species concept.
Another is that--are the organisms in the populations that we're looking at monophyletic? Basically monophyly asks?do they all share a common ancestor??And then there's the issue of distinguishability; can we actually tell them apart? Now when we get down to cryptic species,?you'll see that they are indistinguishable, except at the genetic level. We can't look at them and see any difference. But for many things these will be useful criteria.?
And here are a few criteria that could be applied to any concept.?
The things in monophyletic groups share a common ancestor, and that common ancestor is not the ancestor of any other group, and there aren't any things that are descended from that ancestor that aren't in this group. So it's really everything that came from that common ancestor. So birds all appear to have shared a common ancestor that split off from basically a group of dinosaurs, back in the Cretaceous; possibly a little earlier, in the Jurassic. Mammals all split off earlier from a group of organisms whose later descendents then included the dinosaurs, but also many other things in that grade.
In contrast to a monophyletic group, a paraphyletic group is a group that doesn't contain all the things that are descended from the most recent common ancestor of its members. There's some other things that descended from that common ancestor that are out here.?For example, if you call fish a natural group, you're making a mistake because the tetrapods are descended from the same ancestors as the ancestors of everything you want to call a fish. So the amphibians, the reptiles,?the birds and the mammals are also things that we ought to call fish?by that definition. In the reptiles, the birds and the mammals are missing.
Then we have polyphyletic, which is another kind of a mistake, and a group is polyphyletic--the word referring to that group is a mistake--if the things in it are descended from several ancestors that are also the ancestors of things that are classified into other groups. So, for example, all the stuff that Linniaeus called worms was highly polyphyletic. It included the mollusks. It included therefore the octopuses and the squid. The Old World Euphorbiaceae and the New World Cactaceae?are?fairly distantly related from each other and they have converged on Cactus-like forms, and they have closest relatives that don't look anything like a Cactus. So if you ever make a group like that, that would be polyphyletic.?
Species concepts and criteria were reconciled by Kevin De Queiroz.?Kevin wanted to stop all of the squabbling about the concepts and try to move the research on by more or less trying to resolve that, and do so in a constructive way. Basically asks?if we can agree that species are entire population level segments of lineages?from origination to extinction.?So they have duration in time, and they're at the level of a population, and we could map them onto a Tree of Life.?
They're marking stages in the existence of a species, and they don't actually determine whether the species is a species yet. If?you actually go through what's going on as a species starts to evolve, on the Tree of Life, and you mark off these species criteria,?you have a good species?by the time you've stepped through all your criteria.
What are they? There's separation and?cohesion, and the cohesion can be genetic and caused by actual or potential interbreeding. It can be cohesion of recognition; so everybody who is a potential mate can recognize each other as a potential mate. It can be a cohesion of viability and fertility. So there's post-zygotic compatibility; very important to include a lot of plant species there.
Then there can be ecological cohesion. So these things are living in the same habitat, at the same time, behaving as an ecological unit, and very probably doing so because they are actually inter-breeding. By the way, this business of remaining separate?in the same place?is a good criterion for two separate species.
Another criterion is monophyly; so they share a single most recent common ancestor. And then you can distinguish them either through fixed morphological differences or as a phenotypic cluster in phenotype space--this is a more quantitative thing than the quantum differences of distinct morphology--or they could be a genotypic cluster, in a genotype space.?
I'm now going to lead up to a bit on the genetics of speciation. Gene trees often differ from population trees. There are splits in gene trees that can start occurring before the population splits, and that can continue to occur after the population splits.?It's quite possible that that last common ancestor for the genes will be deeper in time than the last common ancestor of the species; and that's because species have lots of genes.
Then as these genetic differences accumulate, later in time they will be reproductively isolated from each other. If two individuals of the two species did meet, they would not be able to have viable grandchildren. Reproductive isolation can occur at three different stage, but?It's likely that the sequence in which reproductive isolation is acquired is actually the reverse of the sequence that I laid it out. So it would be first post-zygotic isolation; then post-fertilization isolation; and then finally pre-zygotic isolation, with recognition that the two things are different.?
If we look into the genome, and this has been done best with Drosophila, because it's such a good model organism.?Chung-I did this actually with simulans, Drosophila simulans, Drosophila mauritania, and the two sexual races of Drosophila melanagaster, which are in Africa.
Chung-I Wu?said if we look across a genome,?there's gene flow between two populations at lots of places in the genome as speciation just is starting to get going. At this stage we have populations or races. They've got different kinds of adaptations. There isn't any reproductive isolation, and between these three loci there's lots of recombination; the three loci are actually capable of moving back and forth.?
Then, in the second stage, there starts to be some block to gene exchange, and here we are at a level where we're getting a transition between a race and a species, or between a race and sub-species, with some degree of reproductive isolation, and at this stage the populations could fuse or they could diverge. But these blocks here, that you're seeing, are indicating portions of the genome where there isn't any exchange anymore.
So the idea here is that the origin of reproductive isolation?at the genetic level?is a gradual process.?It starts in parts of the genome, and it continues, and while it is developing, there's some still some gene exchange going on, at certain loci. And the?parts where the exchange is still going on are the parts that aren't having big impact on hybrid inviability or mate recognition. The parts that are starting to get frozen up are the parts that have to do with any of those three levels of separation.
When reproductive isolation is complete, then all of the genes are free to diverge. So here the populations are beyond the point where they could fuse but--and they're a good species--but there's a still little bit of hybridization going on, that you can pick up, and here they're completely separated and there's no gene flow anymore.?
Chung-I Wu?looked through the genomes of these species to see at how many places were there genes that were diverging, and what were those genes coding for??
So the differences between the two sexual races of Drosophila melanagaster, which are really quite recently separated,?perhaps 50 or 100,00 ago,?are all in sexual behavior. That's things like how fast does the male vibrate his wings.
And Stage 3,?back?maybe 500,000 years,?we are starting?to pick up lots of sterility and inviability or female sterility genes, and changes in genital morphology so that lock/key mechanisms are incompatible.
And then finally when you get this divergence here, which is back at one to two million years, basically you just see a lot more genes in these categories; sterility and inviability accumulate.
How does a new species actually come into existence??As you've seen from Chung-I Wu's analysis, initially there are only a few genes that are changing. So even though you have 35,000 genes in the genome, speciation might be driven by four or five, and that's what might allow it to occur fairly quickly. And then after reproductive isolation, the changes in those genes mean that all the others will diverge. So a good criterion for a species is that?they remain separate when they're living in the same place and encountering each other at the same place and the same time.?
In the '40s, '50s and '60s over speciation,?a lot of that argument is about?geographic speciation. Darwin emphasized?allopatric?speciation. Gulick, who worked on the speciation of snails in Hawaii and Polynesia, emphasized allopatric speciation.?Sympatric and?parapatric?speciation?are things that came in, in the '60s and '70s.?Allopatric means allo-patric, different places; sym-patric, same place; para-patric, next to each other.
In allopatric speciation you have an original population. There's some geographic or geological barrier that forms. They then start to diverge in isolation and then after they might come back together they won't breed again, because they've diverged so much.Many other things that can?form barriers. Mountain ranges can go up, and when they do, river basins can change,?drainage?basins can change. Things can become reproductively isolated when they fly out to an oceanic island, and so forth.?
So the classical large-scale example of this is the ratite birds. Those are the flightless birds of the Southern continents, and they include the Ostrich, the Cassowary, the Emu, the Kiwi, the Elephant Bird of Madagascar, the Moas of New Zealand. And arguably those are all birds that originated from a common ancestor that was on Gondwana, and when Gondwana broke up through plate tectonics, these just rode around on the plates. They never flew and they never swam.
Parapatric speciation means next door, right next door.?This is thought to have been actually how the Galapagos finches might have speciated on a single island. So some of them might have simply gone up the mountain, while others stayed down on the coast.?
You can breed individuals of?Leopard Frog?from Connecticut and New York. Frog has a range that goes from Canada to Georgia, and if you try to breed individuals from Quebec with individuals from Georgia, they won't. But all along the way you can make the crosses, which means that it is possible in principle for a gene from Quebec to end up in Georgia. So according to the biological species definition, it's a species, but in fact it's in the process of splitting up.?
Sympatric is particularly interesting because the controversy over this was so violent. The idea?is that it's possible for a population, where all of the organisms are living in the same general place and encountering each other at the same general times, to split according to ecological processes that are going on in that little area.
The initial example was a fruit fly called?Rhagoletis?that switched from living on apples to living on cherries, where the apple trees and the cherry trees were all in the same orchard.?And because the offspring were imprinted on the smell of the fruit in which they grew up, when they grew up, they tended to go to that same kind of fruit, and because mating took place on the surface of the fruit, they became reproductively isolated and they started to diverge.?
There have been attempts to cause speciation to happen in the laboratory. They have mostly been with short-lived fruit flies.
If you do divergent selection in allopatry--so you split a population in two and you don't let any gene flow occur between them, and then you select strongly on one trait in one direction in one population, and in the other direction in the other--you can actually cause reproductive isolation to evolve; you can do that in a couple of hundred generations. If you select them in the same direction in allopatry, that doesn't seem to work.
If?you destroy the hybrids, when they are in sympatry, and you divergently select in sympatry, that usually works. So you can start the speciation process in the lab, in sympatry, by destroying any hybrids between the two things that you're trying to make diverge, and selecting those two things in different directions, morphologically.
But if you divergently select without destroying hybrids, that almost never works. So there is an experimental biology of speciation, and there is a literature on that. This is something that's particularly been done in Spain, by the way.?
Sympatric speciation can occur rapidly if you have divergent selection to different habitats, and you couple that with preferential mating with your own ecological type. So this kind of classical?ecological speciation hypothesis?has mostly been applied to fish, and it's been applied to sticklebacks living in lakes in British Columbia, and it has been applied to cichlids living in lakes in Africa.?
Here are two cichlids that are recently derived from the same common ancestor and often classified into the same species. They are Tilapia?living in a lake in Cameroon. There are basically two clusters with a few intermediates. There are some little males and females, and there are some big males and females, and you tend to find the small ones in deep water and the big ones in shallow water.
You can see that you only get the small ones in deep water, and there are a few of the big ones in deep water, but most of the big ones are in shallow water. You'll notice--by the way, it's darker in deeper water, and you'll notice that the ones that are the small ones living in deeper water already are evolving bigger eyes, and there's starting to be some reproductive isolation between these.
So this is a circumstance in which there is a different ecological habitat; there are different foraging and sensory specializations that are needed in the deep habitat than in the shallow habitat. These guys are probably feeding on snails on the bottom, and these are probably feeding on plankton in mid-water. There is good reason for these two not to cross, because the intermediate phenotypes aren't?ecologically as good, they don't perform as well in eating snails or in foraging for zooplankton.?
?Now we saw that these species criteria work fairly well for a certain range of organisms, but then there's also the genotypic cluster thing, and that really solves a problem with asexual and cryptic species.?
One context where it's useful actually is with bacteria. Bacteria that all live in the gut, enteric bacteria, gut flora,?are?proficient at horizontal gene exchange. There's about 30% of their genome that they exchange back and forth?freely, so that there's a lot of recombination going on across most of this tree here. But the housekeeping genes of these bacteria don't exchange horizontally so well.
There's a core group of genes, and they are the genes that are responsible for energy metabolism and the construction of ribosomes and cell walls and stuff like that, that actually form a core that doesn't participate in horizontal gene exchange. And if you just concentrate on that core of genes, you get a perfectly good phylogenetic tree. It forms a gene cluster. If you include the 30% that are being horizontally exchanged, the whole thing gets very fuzzy. So that gene cluster definition is good in bacteria, if you concentrate on the core genes, which are housekeeping genes.?
Cryptic species are common in some groups of salamanders. Cryptic species are also common in the algae that coral farm. So reef-building corals have endosymbiotic commensile algae that they farm, and the strain of algae and the strain of coral have a lot of cryptic diversity. You look at it and you can't tell the difference from the outside.?Tetrahymena?is a ciliate, and there are ten morphologically, completely indistinguishable forms that had a last common ancestor about a hundred million years ago.?However they have diverged a tremendous amount in their DNA sequences, and interestingly even though they look exactly the same, the proteins that build those structures have diverged.?
The criteria to logically distinguish two different species, are separation, cohesion, monophyly and diagnosibility.?The genes that are involved in speciation start off few in number. You might only need to be influencing some aspect of hybrid inviability or some aspect of mate choice and behavior; perhaps just changing the frequency of wing fluttering or something like that. But then, over time, the number of genes involved increase, and other kinds of reproductive isolation mechanisms evolve. And then there are these very cryptic species that can only be distinguished as clusters in genetic space.?
