Coyne versus Carroll

The stage is set. The arena is packed. The two men enter the ring. In one corner, Sean Carroll, the developmental biologist. In the other corner, population geneticist Jerry Coyne . . .

OK, maybe that's a bit over-dramatic, but Jerry Coyne has a critical review of Sean Carroll's Endless Forms Most Beautiful in this week's issue of Nature. After the customary praise of Carroll's accessible writing and mentioning the importance of evo-devo, Coyne questions Carroll's thesis: that the majority of important phenotypic evolutionary innovations are due to changes in gene expression rather than protein sequence. Coyne critiques Carroll's position as mere inference:

"Carroll first notes that dissimilar species can in fact be genetically similar: 'Mice and humans have nearly identical sets of about 25,000 genes' and 'chimps and humans are almost 99 percent identical at the DNA level. Since the sets of genes are so widely shared, how do differences arise?' His answer is the evolution of non-coding regulatory elements: whether you are a man or a mouse apparently depends solely on your promoters and enhancers. But the underlying statistics are deceptive; even a 1% difference in DNA sequence implies a substantial difference in protein sequence. We now know that humans and chimps have different amino-acid sequences in at least 55% of their proteins, a figure that rises to 95% for humans and mice. Thus we can't exclude protein-sequence evolution as an important reason why we lack whiskers and tails."

What can we make of this obvious difference in opinion between two very well respected researchers? Well, for one thing, they are approaching biological evolution from two drastically different perspectives. Carroll is trained as a developmental biologist, and has been extremely influential in the burgeoning field of evo-devo. Coyne, by contrast, studies the genetics of speciation and tends to favor selectionist explanations for the origin of species (as opposed to neutral or population structure type hypotheses). Coyne's work is much more quantitative, whereas Carroll tries to unravel developmental pathways. I am not saying one approach is better than another, only that they are different and lead to different ways of thinking about the similar questions.

Also, Carroll seems to bring this criticism onto himself when he "presents his vision of the field without admitting that large parts of that vision remain controversial." If this is the case (now may be a good time to mention that I have yet to read the book), it may appear to the general public, to whom this book is intended, that a consensus has been reached and Carroll's view is universal.

While I definitely think that some evidence points to the importance of regulatory changes in evolution, we do not know what the relative roles of gene expression and protein sequence play in the evolution of development. Even untangling these two aspects of development can be difficult as changes in the protein sequence of a transcription factor can lead to regulatory changes in genes in downstream pathways. I'd say it's definitely an area of active research, and I do intend to read Carroll's book.

As a point of contrast, check out this review by PZ Myers.