Coyne and Orr on Darwin

I've been inspired to write a semi-substantive post by Prof. Rob Skipper who has started an excellent new blog about the history and philosophy of biology.

I saw that one of his "must read" biology books is Speciation by Jerry Coyne and Allen Orr. I'm not sure it would make my top ten, but mainly because I'm not sure I could make a top ten. If you're interested in speciation then of course you have to read it.

Anyway, I'm currently taking a course here at IU in the bio dept. on speciation with Prof. Loren Rieseberg and we're using the Coyne and Orr as our central text. Needless to say, I find Coyne and Orr's discussion of certain things a bit one sided. They focus their discussion of speciation around the biological species concept and the evolution of reproductive barriers. This is fine as one perspective on speciation research and certainly provides the foundation for a robust and productive research program on speciation, but it leads to an inordinate emphasis on genetics and a dismissal of a group of issues related to the ecology of speciation, namely sympatric speciation, disruptive selection etc., not to mention speciation in asexual organisms. Moreover, their emphasis on the BSC proves difficult to operationalize in the case of many allopatric species because such an emphasis relies on studying the evolution of isolating barriers that "actually or potentially prevent gene flow in sympatry" (57).

Enough with these petty complaints. My real problem with the book is that they tend to misrepresent Darwin. One of the most glaring misrepresentations is in chapter 3 where they quote a passage from the Origin that seems to show that Darwin was a proponent of allopatric speciation in addition to sympatric speciation. However, they leave a big chunk of the quote out and throw in some ellipses. Interestingly, the bit of the quote they throw out is quite important to the issue at hand. It reads: “For the area will first have existed as a continent, and the inhabitants, at this period numerous in individuals and kinds, will have been subjected to very severe competition.” (107) To make a long story short, "very severe competition" for Darwin was more important as a cause of speciation than geographical isolation and therefore it is not clear how much support the actual quote gives to the idea that Darwin was a proponent of allopatric speciation.

An even bigger problem I have with the text is Coyne and Orr's treatment of postzygotic isolation. The term 'postzygotic isolation' refers to isolating barriers that act after the zygote has been formed. Included under this label are things like hybrid inviability (hybrids have developmental issues) and hybrid sterility, amongst others. Coyne and Orr frame their entire discussion of hybrid sterility around Darwin's inability to explain how hybrid sterility could evolve.

The problem goes like this: organisms that are sterile could never be selected for because they don't have any offspring. Therefore, how could this type of isolating barrier evolve by, or in the face of, natural selection?

Coyne and Orr call this "Darwin's dilemma". Darwin's explanation had to do with an analogy between hybrid sterility and grafting. The ability of two plants to be grafted together depends on the evolution of incidental differences between the plants that are to be grafted. Coyne and Orr claim that this just won't do because grafting doesn't occur in nature but hybrids do: "differences causing one plant to reject a graft from another can evolve unopposed by natural selection because grafting does not occur in nature." (247) As we'll see, however, the current answer to Darwin's dilemma, the one that Coyne and Orr endorse, involves the restriction of hybridization.

After considering models of the evolution of hybrid sterility that invoke chromosomal rearrangements (which turn out not to work in populations of N=~50), Coyne and Orr triumphantly announce the solution: genic incompatibilities a la the Dobzhansky-Muller model. The D-M model is rather obvious and goes like this: if two species evolve long enough without any gene flow between them, suppose in allopatry, then when they come into contact with each other, the probability that their hybrids will be sterile is proportional to the amount of time they have evolved independently. This makes a lot of sense. It is very unlikely that after only a short amount of independent evolution, two populations would have accumulated enough of the "correct" genetic differences to prevent their hybrids from reproducing yet after lots of independent evolution, equal to that between different orders for example, it seems ludicrous to suggest that fertile hybrids, or in fact viable hybrids or even a successful mating, would occur.

This is all well and good, but it turns out that Darwin came up with the same explanation! Of course Darwin didn't phrase it in terms of epistasis, but his explanation was pretty similar to the D-M model.

Darwin thought of hybrid sterility as analogous (or the same very thing) as the ability of two species of tree to be grafted to one another. Darwin said that "sterility is not a specially acquired or endowed quality, but is incidental on other acquired differences." (245)

Darwin spends the majority of this chapter discussing the results of different crosses in terms of the sterility of the hybrid offspring. Crosses between varieties of the same species generally result in fertile hybrids (e.g. 269) whereas hybrids have never "been raised between species ranked by systematists in distinct families" (257). Darwin then concludes:

"It is not surprising that the degree of difficulty in uniting two species, and the degree of sterility of their hybrid-offspring should generally correspond, though due to distinct causes; for both depend on the amount of difference of some kind between the species which are crossed. Nor is it surprising that the facility of effecting a first cross, the fertility of the hybrids produced, and the capacity of being grafted together...should all run, to a certain extent, parallel with the systematic affinity of the forms which are subjected to experiment; for systematic affinity attempts to express all kinds of resemblance between all species." (277, italics added).

If we take systematic affinity to be indicative of time since divergence for Darwin, which I think is certainly right, then here we have Darwin saying that the likelihood of two species/varieties producing fertile hybrids depends on the time since their divergence.

Now Darwin doesn't think that this is a strict rule as he is careful to point out several counterexamples where fairly distant relative produce fertile offspring and varieties produce sterile ones. But this seems to be expected: it seems as if in some small number of cases, the "correct" changes did not occur in the two lineages during their independent evolution that would prohibit the production of fertile hybrids, and vice versa for varieties of the same species.

Of course, it's not clear how one would square Darwin's explanation with his model of sympatric speciation. But I think this might be possible. I just can't do it here.

Now certainly I don't think that the D-M hasn't "advanced" our understanding of the evolution of hybrid sterility. Clearly the incorporation of genetics and the development of quantitative models have allowed for a more sophisticated and "complete" account of hybrid sterility and have allowed us to subject the qualitative theory to more rigorous test. I'm just pissed Coyne and Orr were so quick to dismiss Darwin.