In yesterday’s post I outlined what I see as “the species problem” (the existence of discontinuities in nature in one area), outlined the “biological species concept” (BSC), and suggested that the BSC was the best species concept to use when studying that species problem. Let me reiterate that I don’t think there’s a single “right” or “best” species concept—each has its weaknesses (some more than others)—nor do I think there’s a single species problem, either. On page 26 of Speciation, Allen Orr and I list five different species “problems,” though the one that I find most intriguing is the one I mention above. I favor the BSC because I think it is the best one for solving that species problem.
I’ll try briefly today to show why the BSC, which conceptualizes species as those entities whose members are interbreeding among themselves but genetically separated from members of other species by reproductive isolating barriers (RIBs), is the species concept that not only explains the species problem (i.e. the discreteness of nature) but offers a solution to how that discreteness evolves.
It’s actually pretty simple. Two sexually-reproducing and related taxa living in the same area cannot maintain their distinctness unless they have evolved substantial barriers to gene exchange. If all species exchanged genes with their relatives, and did so commonly, then nature would form a continuum: you would not be able to instantly discriminate between a sparrow and a starling, or a gingko and an oak. (Some “species” do have limited gene exchange; more on that later.) The mere observation that related and distinct groups in one location maintain their distinctness means perforce that there are reproductive barriers between them, even if those barriers involve the ecological or developmental inferiority of hybrids that do form between them.
Thus, the discreteness of nature must have some connection to impediments of gene flow between the discrete groups. This may be why Dobzhansky, a geneticist, was the first person to draw this connection. In a paper in Revista di Scienza in 1937, he made this explicit:
Any discussion of these problems [of discontinuities in the living world] should have as its logical starting point a consideration of the fact that no discrete groups of organisms differing in more than a single gene can maintain their identity unless they are prevented from interbreeding with other groups . . Hence the existence of discrete groups of any size constitutes evidence that some mechanisms prevent their interbreeding, and thus isolate them.
For the professionals reading this, let me note that disruptive selection between two types of plants or animals in one area can also maintain them as discrete entities, but this is really a form of reproductive isolation as well, since by definition the intermediate forms are maladaptive under disruptive selection. Maladaptive hybrids constitute reproductive barriers known as postzygotic isolation.
This hybrid inferiority, for example, is the case in benthic and limnetic sticklebacks (Gasterosteus aculeatus) in the lakes of British Columbia, two groups with ambiguous species status. Some consider them different species, but most, like my friend Dolph Schluter, consider them “incipient species” or morphs. They forage in different places in the lake, and eat different food.
Here are females of the two types, showing how different they are (benthic on top, limnetic on bottom: photo by Todd Hatfield):
Regardless of whether we call these forms “species,” though, the point is that these two forms do interbreed in the wild. Why, then, do they still remain distinct? Because, as Dolph and others have shown, the hybrids are at an ecological disadvantage. They cannot forage as efficiently as either the pure benthic or limnetic forms and so leave few offspring. This is a type of reproductive isolating barrier (we call it “extrinsic postzygotic isolation”) that helps keep the benthic and limnetic forms distinct.
This kind of barrier also operates in plants. Several readers have vociferously asserted that related species of plants hybridize profusely in sympatry. And, indeed, plants do seem to hybridize more often than animals (but not as often as everyone thinks; see pp. 40-45 of Speciation). What people don’t consider when asserting this is that if plants really did hybridize profusely, or even moderately, with their relatives in the same area, the groups would no longer remain distinct. Those plants would blur into a single variable taxon. The fact that they do remain distinct despite hybridization indicates pretty clearly that there is some problem with the hybrids, which is, after all, demonstrates reproductive isolation. And indeed, when you investigate these situations, you do find hybrid inferiority. We outlines some cases in Speciation.
One of the groups that’s often said to flagrantly violate the BSC is the oaks (genus Quercus; this is often said of cottonwoods, Populus, as well). On pp. 43-45 of Speciation I dissected this story and found it grossly exaggerated. Boundaries between oaks are not nearly as porous as commonly thought. Further, some of the evidence of “hybridization” between plant species is based on exchange of mitochondrial DNA (mtDNA) or chloroplast DNA (cpDNA) Biologists love to use these types of DNA because they’re easier to obtain than nuclear DNA, and also evolve more rapidly. But we now know that both mtDNA and cpDNA move between species a lot more readily than the vastly greater amount of nuclear DNA, so claiming pervasive gene exchange based on observations of mtDNA or cpDNA alone is a perilous claim, and is known to be wrong in oaks.
The main point is that reproductive isolation is what keeps species distinct in sympatry (i.e., in the areas where they encounter each other and could potentially exchange genes). Without RIBs, nature would be a continuum. Therefore, understanding the origin and evolution of RIBs is equivalent to understanding why nature is discrete in one area. That is why the BSC is the best species concept to use for addressing this particular species problem. What is the origin of species? Under the BSC, that question becomes equivalent to “What is the origin of reproductive isolating barriers between closely related species?”. And that is a much more tractable question. Reducing the problem of speciation—or at least of discrete groups of sexually-reproducing organisms in sympatry—to the problem of the origin of RIBs is perhaps the greatest achievement of the modern synthesis, an achievement that, unlike many others, wasn’t foreshadowed by Darwin.
It’s telling that when evolutionists are studying the origin of species—how new species come to be—nearly all of them adhere to the BSC. That is, they study the origin of reproductive barriers between incipient species. This holds even if those workers adhere to other species concepts. We give an example in Speciation: my friend Kerry Shaw at Cornell is a strong advocate of the phylogenetic species concept (PSC), and has written papers defending it and asserting its superiority over the BSC. Yet in her own research on speciation in Hawaiian wingless crickets (Laupala), Shaw studies the origin of differences in mating song and cuticular hydrocarbons, factors that keep different cricket species from hybridizing in sympatry. This is an implicit admission of the value of the BSC in studying the origin of species in nature.
In fact, I don’t know of a single paper studying the process of speciation in real animals and plants in nature that doesn’t implicitly adhere to the BSC, concentrating on factors that impede gene flow. There may be a few I have missed, but I try to keep up with the literature. This, again, is a tacit admission of the usefulness of the BSC in understanding the origin of those entities we call “species.”
Finally, some species concepts that claim to differ from, and be superior to, the BSC really incorporate the BSC into their assumptions. One of these is the “evolutionary species concept” (ESC), currently the most popular alternative to the BSC and one much beloved by systematists. The ESC considers a species to be a lineage that is evolving “independently of other lineages.”
This concept has even more problems than the BSC. First of all, its adherents never define what they mean by “independent evolution.” If there is even a tiny bit of gene exchange, are lineages still “independent” What about the very common situation within species (an example is different subspecies of birds) when some genes for morphology or behavior are evolving independently in different places, because the birds live in different habitats that select for different morphology or behavior, but the rest of the genome is not subject to divergent selection and so is not evolving independently in those two lineages.
A bigger problem is that of allopatry: when groups can’t exchange genes simply because they are geographically isolated (note: that is not necessarily the same thing as reproductively isolated). According to the ESC, if a few lizards travel to a distant oceanic island on a vegetation raft, and start breeding there, they instantly constitute a new species the minute they set foot (feet?) on the island, because from that moment they are “evolving independently.” Would anyone really want to consider these a new species, though, simply because they land on an island that makes gene exchange with their ancestors impossible? Consider this: nothing biologically important has changed at the moment when those lizards land on the island. Is that really the moment of “speciation”, then?
So one of the main weaknesses of the ESC is that it conflates geographic isolation with genetic isolation. And when the distinctness of taxa (and lineages) really is discernible—in areas where they coexist—lineages evolve independently precisely because they are reproductively isolated! After all, it’s the absence of gene exchange that constitutes “independent evolution.” In that sense, the ESC really puts the phylogenetic cart before the genetic horse. To explain why lineages evolve independently in sympatry, you must explain why there are barriers to gene exchange between those lineages—and that’s the species problem addressed by the BSC.
The common assertion of systematists that they alone—and not those pesky population geneticists—have successfully divorced pattern from process (see, for example, any paper by Quentin Wheeler), is simply wrong. The ESC implicitly requires an evocation of process—the evolutionary process that creates reproductive barriers between lineages.
(A mini-rant about systematics here. I love systematics and think it’s ground zero for nearly all evolutionary studies. You can’t understand much about evolution, and certainly nothing about speciation, unless you understand the evolutionary relationships between species. That’s why I’ve spent a lot of time making phylogenies, and why my most cited paper [Coyne and Orr 1989, Evolution] involves combining phylogenies of Drosophila species with data on reproductive isolation.
Nevertheless, many systematists, especially cladists, seem to have gone off the rails, making dumb and insupportable statements about evolution. I don’t know why this is, since cladism has as its purview one of the most important insights in evolutionary biology: Hennig’s recognition that one could help reconstruct the history of life using shared derived traits (these traits are called “synapomorphies”). Nevertheless, cladists like Wheeler constantly impugn evolutionary genetics and assert that only systematists have the right to construct species concepts. They also claim that their own systematically-based species concepts divorce evolutionary pattern from evolutionary process. As I’ve just shown, they are wrong. The assertion that synapomorphies are the traits to use when constructing phylogenies is a statement about process: those synapomorphies are shared and derived because they’re passed on from ancestors to descendants during speciation! If that’s not a process, I’ll eat my boots.)
I have reached the end of my two-part rant. I won’t convince everyone, of course, but I hope I’ve convinced at least some readers of the utility of the BSC for answering a most important problem of evolutionary biology: why is nature discontinuous rather than continuous? For those who wish to go further, have a look at Speciation by Coyne and Orr, especially chapter 1 and the appendix.
Enough about species. Now on to something really important: boots!