Revisiting an old paper

I was just reminded that in 2020 Hari Sridhar interviewed me about what is perhaps my most cited paper (1561 times to date, though my book Speciation with Allen Orr was cited almost six times as often), and certainly one of the few good ideas I’ve had in my life (the paper was also co-written with Orr). You can see the paper by clicking below, and there was a followup paper in 1997 with the word “revisited” tacked on the title below; that was written since new genetic-distance data had appeared.

Here’s the good idea as it came out in the interview:

HS: You were interested in Drosophila and the genetics of Drosophila right from the time of your PhD. What was the motivation for this particular piece of work?

Jerry Coyne: Well, the motivation is implicit in the paper. I was interested in the genetic basis of reproductive isolation in Drosophila. I realized that there were a lot of data out there on the genetic distances between different closely-related species of flies as measured by electrophoresis, and from reading a lot of the old literature – Patterson & Stone (1949, Univ. Texas Publ. 4920: 7-17), and The Genetics and Biology of Drosophila book series ‑that there is an immense amount of data on the crossability of flies, their sexual isolation, the sterility and viability of hybrids. And it came to me one day in Maryland – I can still remember this – that you could combine that different data using electrophoresis as the estimate of divergence time, and then the other parameters as estimates of the degree of reproductive isolation. By doing that, you could get some kind of estimate of the time course over which reproductive isolation evolves. After that, it was just a matter of compiling that data. It took a long time because it’s all in different places – papers, books and stuff. Nobody had thought to put them together before. It was just a matter of compiling the electrophoretic data with the crossability data and then seeing what came out of that. That was the motivation.

one more Q&A:

HS: At the time when you did this work, did you anticipate, at all, the kind of impact it would have on the field? Do you have a sense of what it mostly gets cited for?

JC: Yeah, it gets cited for the reason that we wrote it, actually. Well, two things. First, It gives an idea of the time course of speciation. But also, the result showing that sympatric species get reproductively isolated much more quickly, in terms of pre-zygotic isolation, than allopatric species, was unanticipated. It supports the idea that there’s either reinforcement or reproductive character displacement. I just said, well, let’s look at these data. Then we went back to all the original papers and looked at the ranges to see whether the species lived in sympatry or not. That was a lot of work too because, a lot of the time, range data is not presented as ranges.You have to look at where the flies were captured and, sort of, get an idea of whether the ranges overlapped or not. Those two aspects of the paper were important. Remember, the paper is incomplete because it leaves out a number of forms of reproductive isolation that could be very important in nature, like post-mating pre-zygotic isolation, sperm competition, ecological isolation and temporal isolation. Those aren’t included, because there’s no data. But the support for reinforcement that we showed, the high degree of pre-mating isolation between sympatric species as opposed to allopatric pairs, stimulated, stimulated, I think, work on reinforcement. Even in my own laboratory, my student, Daniel Matute, worked on reinforcement, I think, partly because of the data from this original paper. So it had a number of influences on the field. I don’t know how important it is. It’s a novel approach. It’s one that you can’t really us with most species because of the lack of crossability data. There have been a few other studies. Leonie Moyle did a similar study in tomatoes, I think, and Tamra Mendelson did a study on darters collecting information on genetic distance. The problem with darters and all other groups is that you just don’t have the ability to do laboratory crosses that you have in Drosophila. So Tammie was limited to about 12-13 species.

I’m sorry to say that I haven’t kept up diligently with other folks’ followup work, as there are more papers building on this one (e.g. here, here, and here). In general, I think, they’ve supported our main conclusions, especially the cool one that sexual isolation (mate discrimination) appears to evolve more quickly between groups that experience some period of “sympatry” (living in the same area) after speciation has begun. That in turn supports the idea of “reinforcement”: that if there is a reproductive penalty to hybridizing (e.g. producing hybrids that are sterile or weak), natural selection will build up mate discrimination so that the production of hybrids is less likely. (The idea is that you leave more of your genes to future generations when you produce healthy, conspecific hybrids, so any gene that favors mating with your own species will be favored.) And indeed, we found a strong pattern of heightened sexual isolation among species that are sympatric rather than allopatric (“geographically isolated”).

I liked the original idea of using genetic-distance data to figure out the time course of speciation (or rather, aspects of speciation: mate discrimination and hybrid sterility/inviability) because speciation is often very slow and reconstructing the process (and seeing if there are any generalizations to be made) can be done only by using proxies of divergence time, which in our case was the “genetic distance” calculated using gel electrophoresis. As I note in the interview, gel electrophoresis is pretty much dead, and DNA sequencing of fly species is the way to go.