A self-aggrandizing post concerning a paper on speciation I wrote with Allen Orr

What is an old, retired scientist to do but look back on his career and find satisfaction on the good ideas he had? (I just finished a great novel in which a superannuated Cuban musician does the same thing.) In line with that, reader Nick called my attention to a two-year-old video by Zach Hancock lauding a paper I wrote with my student, Allen Orr, as “one of the ten most influential papers in evolution.”

First, though, in April I bragged about another video by Zack Hancock (a professor at Augusta University) that put my book Speciation (also co-written with Allen Orr), as one of the ten most influential books in evolutionary biology (we were #10). I have to admit that I consider this book my most significant accomplishment in science, as it distilled the field of speciation down to a research program that succeeded in influencing research in the origin of species. It took us six years (each) to write.

I rarely look at Speciation now, though, for when I do I realize that when we wrote it I was at the top of my neuronal game, able to read, write, and synthesize far better than I do now. And when I open it and sample a page or so from the chapters I wrote, I think to myself, “Who is that guy? He was really savvy?!” I could not write it now, nor will either of us revise it.

But Zack had another video that I missed,  one on the ten most influential papers in evolutionary biology. And again Allen and I made the list, coming it at #9 with the paper below we published in 1989 in Evolution. Note the dedication to Bruce Grant, under whom both of us studied at William and Mary (click title to read the paper):

I’ll add that this paper was at first rejected by Evolution on the grounds that we could not use the method of correlation that we did, but the reviewer simply didn’t understand that method (it’s not rocket science). We argued with the editor, something I’d never done, and the paper was accepted.

Zack chooses papers in the field that have been cited more than a thousand times. and I’ll let him explain the findings in his video below (the discussion of our paper goes from 5:23 to 7:51).

A few corrections. To determine the relative divergence time between pairs of species or taxa, we used published data using genetic distance determined by gel electrophoresis; we did not “sequence genes”.  The purpose of the paper, as Zack says, is to determine how reproductive barriers between species arise with time by looking at the degree of reproductive isolation (measured only as hybrid sterility/inviability or as mate discrimination) between groups and correlating that with electrophoretic genetic distance.

Also, Zack emphasizes the “reinforcement” aspect of the paper (I’ve put that conclusion in bold below), but that is only one finding—granted, a nice one. But the overall conclusions are several-fold, as the paper’s abstract notes below, including the relative rates of evolution of postzygotic isolation versus one form of prezygotic isolation (mate discrimination) as well as showing early evolution of male versus female postzygotic isolation, which explains the phenomenon of “Haldane’s Rule“, a generalization first noticed by J. B. S. Haldane in 1922, but neglected until I took it up in 1985.  This rule, pointing out the greater preponderance of sterility and inviability in heterogametic (XY or ZW) hybrids than in homogametic hybrids (XX and ZZ) is still subject to investigation and controversy, but has been a central focus of the genetics of speciation since 1985.

Here’s the abstract of our paper with the “reinforcement” finding shown in bold. Note the other findings, too:

To investigate the time course of speciation, we gathered literature data on 119 pairs of closely related Drosophila species with known genetic distances, mating discrimination, strength of hybrid sterility and inviability, and geographic ranges. Because genetic distance is correlated with divergence time, these data provide a cross-section of taxa at different stages of speciation.

Mating discrimination and the sterility or inviability of hybrids increase gradually with time. Hybrid sterility and inviability evolve at similar rates. Among allopatric species, mating discrimination and postzygotic isolation evolve at comparable rates, but among sympatric species strong mating discrimination appears well before severe sterility or inviability. This suggests that prezygotic reproductive isolation may be reinforced when allopatric taxa become sympatric.

Analysis of the evolution of postzygotic isolation shows that recently diverged taxa usually produce sterile or inviable male but not female hybrids. Moreover, there is a large temporal gap between the evolution of male-limited and female hybrid sterility or inviability. This gap, which is predicted by recent theories about the genetics of speciation, explains the overwhelming preponderance of hybridizations yielding male-limited hybrid sterility or inviability (Haldane’s rule).

Finally, Allen and I continued to collect data as new studies became available, eventually expanding the study to 171 taxon pairs—an increase of 41% in the amount of data. The results, published in Evolution in 1997, were similar to those of the earlier study, but stronger because they were based on more data. You can read the paper by clicking below.

Since electrophoretic analysis of species divergence is largely obsolete—everyone uses DNA sequencing now—the whole paper can’t be repeated with modern methods, but what has been done is analysis of a subset of species, and, as I recall (I’m not going to look up the papers), the results to date support those of our 1989 and 1997 papers.

A scientist is lucky if he or she has more than one or two good ideas in their career, and by that I mean an idea that influences their field in a substantial way. I’ve had about three, one of which is the analysis embodied in these two papers. And I have to pay tribute to Allen Orr (now retired, too); fiercely intelligent and hard-working—more a colleague than my graduate student. Both of us are honored to be included in the lists ten books and ten papers discussed by Hancock. Josh and Esther Lederberg, W. D. Hamilton. Ronald Fisher, Sewall Wright—that is fancy company!