What Causes Speciation?

 
The latest issue or Science magazine contains a number of articles on speciation.

The one that most interests me is Schluter (2009), a paper that discusses mechanisms of speciation. Schulter begins with ...

It took evolutionary biologists nearly 150 years, but at last we can agree with Darwin that the origin of species, "that mystery of mysteries" (1), really does occur by means of natural selection (2–5). Not all species appear to evolve by selection, but the evidence suggests that most of them do. The effort leading up to this conclusion involved many experimental and conceptual advances, including a revision of the notion of speciation itself, 80 years after publication of On the Origin of the Species, to a definition based on reproductive isolation instead of morphological differences (6, 7).

I've heard this a lot recently but it doesn't make sense to me. How could the evolution of reproductive isolation be selected?

The main question today is how does selection lead to speciation? What are the mechanisms of natural selection, what genes are affected, and how do changes at these genes yield the habitat, behavioral, mechanical, chemical, physiological, and other incompatibilities that are the reproductive barriers between new species? As a start, the many ways by which new species might arise by selection can be grouped into two broad categories: ecological speciation and mutation-order speciation. Ecological speciation refers to the evolution of reproductive isolation between populations or subsets of a single population by adaptation to different environments or ecological niches (2, 8, 9). Natural selection is divergent, acting in contrasting directions between environments, which drives the fixation of different alleles, each advantageous in one environment but not in the other. Following G. S. Mani and B. C. Clarke (10), I define mutation-order speciation as the evolution of reproductive isolation by the chance occurrence and fixation of different alleles between populations adapting to similar selection pressures. Reproductive isolation evolves because populations fix distinct mutations that would nevertheless be advantageous in both of their environments. The relative importance of these two categories of mechanism for the origin of species in nature is unknown.

Is there an expert on speciation out there who can explain this? I understand how two incipient species can adapt to different environments and become morphologically distinct but I don't understand how this kind of adaptation leads to selection for reproductive isolation. This is a problem that we discussed earlier [Testing Natural Selection: Part 2].

The second mechanism is even more difficult for me. I understand how chance mutations can arise and become fixed but to my mind this isn't natural selection. It's speciation by random genetic drift. It's just an accident that the mutations being fixed in the separated populations happen to lead to reproductive isolation.

Schluter tells us that mutation-order speciation is "distinct from genetic drift." He seems to refer to it as "selection" of some sort without explaining why. ("The unidentified component of speciation, if built by selection and not genetic drift, could be the result of either ecological or mutation-order mechanisms.") He says that the mutations that give rise to reproductive isolation are "advantageous" in both populations but they just happened to occur in one of them and not the other. Again, the question is what sort of mutations favoring reproductive isolation would be "advantageous," and therefore selected?

If the mutation arises later on in the other species will it sweep to fixation and remove the reproductive isolation barrier?

It's not clear to me that we have identified the mechanisms of reproductive isolation in a large number of examples. Schluter seems to agree,

The most obvious shortcoming of our current understanding of speciation is that the threads connecting genes and selection are still few. We have many cases of ecological selection generating reproductive isolation with little knowledge of the genetic changes that allow it. We have strong signatures of positive selection at genes for reproductive isolation without enough knowledge of the mechanisms of selection behind them. But we hardly have time to complain. So many new model systems for speciation are being developed that the filling of major gaps is imminent. By the time we reach the bicentennial of the greatest book ever written, I expect that we will have that much more to celebrate.

Given our lack of knowledge how can biologists be so confident that Darwin was right? How do they know that most speciations are due to natural selection and not random genetic drift—especially since drift and accident seem to be intuitively more likely?

Is this an example of adaptationist bias or is there really lots of evidence to support speciation by natural selection?

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Schluter, D. (2009) Evidence for Ecological Speciation and Its Alternative. Science 323: 737 - 741 [DOI: 10.1126/science.1160006]