Relating speciation

Two issues that face an evolutionary biologist rather sharply are these: the nature of species and how they come to be. When in the period of the fusion of Mendelian genetic and Darwinian evolutionary theory these matters were raised, initially by Dobzhansky, the obvious way to tackle the problem was by making use of th enew science of genetics. Scientists will not tackle a problem for which there are no tools, although they may speculate on problems. But give them a new tool, like Mendelian genetics, and they are off and running.

But this has an unwanted aspect - it can lead scientists to frame the problem solely in terms of the tools. And so it was with the matter of speciation and species. Species were, Dobzhansky informed us, largely terminal stages in the separation of gene pools. Mayr further extended this by defining species solely as populations that were permanently isolated from exchanging genes.

And this is true, for sexual species, although it is not always the case that genes are the mechanism for reproductive isolation. Behavioural and developmental processes can isolate populations while massive differences in genetic structure and alleles can be included within one species. And the nature of the term "population" is suspect itself. A population is a partition of the gene pool of a species (you don't define a species in terms of populations that have no chance of reproducing together, like asparagus and elephants), but what counts as a population, or the reproductive equivalent of a population, the deme, depends on whether they are in the same or similar enough species. Species define populations, and populations define species. Perhaps there's enough shared operational understanding in the various disciplines to make non-tautological sense of the two terms, but on the face of it "population" is merely one unanalysed term defining another.

In our diagram, several speciation modes are undistinguished, in part because what makes them different has nothing much to do with geography. Geography is only important for those speciation modes that rely upon it, like sympatric reinforcement or allopatric drift (i.e., evolution of the genetic structure of the population in isolation). But in chromosomal rearrangements, such as inversions, fusions, fissions, and duplications, geography has no real role to play as a mechanism of speciation, and is only useful as a test afterwards of whether or not speciation is complete enough to count two species where there were one.

Then there are asexual, or mostly asexual, species. Simpson proposed not to call them species because they failed to rely even upon reproductive isolation, while A. J. Cain famously invented the notion of an "agamospecies" for them. But I like Manfred Eigen's notion of a "quasispecies" (from "qua si", as if) in which there is a genetic coordinate in the space defined by the genomes of these beasties that is the default, or "wild-type" (wt), even if no strain of them actually instantiates it, around which all the others cluster. This naturally raises the question why they cluster there, and in the case of viruses, for which he developed the notion, the reason is clear. They cluster about the most efficient utiliser of the host cell resources. In effect, the wt is a fitness peak, and variants that stray too far will be of lowered fitness (unless they cross a fitness valley and start moving up the new slope).

In the case of selectively reinforced speciation, of lowered hybrid fitness, this is also the case. These populations or variants will be maintained by selection for some environmental niche or mode of living. So we can perhaps see that reinforcement of species here is effectively equivalent to quasispecies, only now, being sexual, it is not the elimination of strains that are not near the fitness peak, but of hybrids who are between the peaks.

The same thing is true of host race speciation - here the selection is for the host resource availability. So the common element here is selection, and we can perhaps collapse them into one mode, differentiating them on the basis of what the resources are, ecologically speaking.

Competitive speciation - Darwin's favourite - is likewise a case of selection, but what about karyotypic races and hybridisation? Or sexual selection? In each case, what counts here for fitness is whether there are mating opportunities. If you have a karyotypic difference that happens to match sufficiently with the ancestral karyotype, then speciation does not occur. But if the changes make it harder to mate, then eventually mating with those of similar karyotype is fitter than mating with the parental form. In hybridisation the same thing is true - the hybrid form often cannot easily mate with either parent successfully, so it forms its own species.

Sexual selection is clearly about being able to mate. The major difference here is what does the selecting. Rather than it being the extrinsic environment, it is the intrinsic one. If you cannot find a mate among one morph of the population, but you can with the other, then eventually the lowered fitness of those that try to mate both ways will tell.

And that leaves Vicariant evolution, misleadingly called "allopatric speciation" or speciation by geographical isolation and independent evolution. Originally proposed by Moritz Wagner in the 1860s, it is the form of speciation most defended by Mayr and those in his research tradition. There is selection going on, of course, but not against lowered fitness of some morph or allele or karyotype, but solely selection for local conditions, which forces genetic changes that eventually make it difficult if not near impossible (nothing physically possible is actually impossible in biology) for the now sympatric populations to interbreed. In short, so far as reproductive compatibility is concerned, the two populations just... drift. Selection maintains them at local fitness peaks, but they acquire inadvertent changes that make them reproductively isolated when they get back together, if they do.

I want to propose a notion here I shall call "reproductive reach". Any two populations have a reproductive distance that is locally defined and context-dependent. It determines how much gene flow can occur between them if they are sexual reproducers. And it specifies for any two organisms whether their progeny will be fit enough to continue a reproductive lineage. The acquisition of reproductive isolation depends on whether the conditions leave the two organisms outside the reproductive reach of each other. It need not be absolute, but if the fitness of a progeny of any organism is severely lowered (and having none at all is about as severe as it gets) then that form or variant is outside the reproductive reach of its parent or parents.

Now this has an interesting consequence. A sexual species becomes just a special variety of asexual species. Where the fitness peak on asexual quasispecies is entirely extrinsic, the fitness peak of sexual species can be either extrinsic or intrinsic. It's about, in the end, how many progeny you can have. Quasispecies is the primitive or basal notion of specieshood. Sexuality just adds dimensions to ways of being species. Vicariant speciation relies on local fitness peaks, but put them back in sympatry and it's all about the fitness determined by the reproductive reach of the two organisms involved.

Since we can now say, with Gavrilets, that drift and selection are not mutually exclusive (because, remember, there are fitness ridges in any complex genome space along which a population can take a Brownian walk) I say that all speciation is, indeed, about selection, either ecological, sexual, or developmental. So we can dispense with geography in our taxonomy of speciation altogether, except as an index to differentiate the kind of process that modifies reproductive reach.

Does this make Darwin right and Mayr wrong? Of course not. Darwin was very vague about the modalities and reasons for speciation, and he thought that direct reinforcement of diverging selection mostly drove it. It is entirely probable, as Coyne and Orr document, that Vicariance drives most sexual speciation in animals (but not necessarily plants - or gamete broadcasters in the animal world either. If you sow your seed, so to speak, broadly, then what maintains your isolation will be selective). But geography is a secondary aspect of speciation. And it need not be the most important for all groups of organisms.

So the allopatry-sympatry axis of percentage gene flow is the spindle, as it were, around which myriads of particular processes acquire reproductive isolation by exceeding the reproductive reach of the original genomes. Geography's in there, as are chromosomal rearrangements, and host race speciation, etc. We need to revise our terminology to avoid the useless disputes of the past about what "the" mode of speciation is. What counts in the end is the rather obvious fact that the number of progeny, relative to alternatives, makes a new species.