In the late 1990s, mounting experimental evidence for rapid evolution of traits related to fertilisation seemed paradoxical given that matching of male and female traits is required for successful reproduction In a paper published in Nature in 2000, Sergey Gavrilets showed, through a simple mode, that continual change is expected in such traits whenever females suffer a loss of fitness from having too many compatible males. Seventeen years after the paper was published, I spoke to Sergey Gavrilets about his interest in this topic, memories of carrying out this work, and what we have learnt since about evolution of reproductive barriers.
Citation: Gavrilets, S. (2000). Rapid evolution of reproductive barriers driven by sexual conflict. Nature, 403(6772), 886-889.
Date of interview: 6 July 2017 (via Skype)
Hari Sridhar: What was your motivation for doing this study?
Sergey Gavrilets: I think in 1999, I went to Europe for the summer, and spent a month in Italy working with Carlo Matessi, an Italian theoretician on models of non-random mating. From there, I moved to Utrecht in the Netherlands to work with Gerdien De Jong on modeling genotype-environment interactions. And when I went there I carried with me, as summer reading, a book called Endless Forms – Species and Speciation edited by Dan Howard and Stewart Berlocher. It had a long list of papers on speciation including a couple on sexual conflict. I knew about sexual conflict before, through Bill Rice’s paper in Nature in 1996. I think that made some splash. He also had a couple of reviews, one in Evolution and another one, but I couldn’t really connect and really see what he was talking about from a theoretical point of view.
Sexual conflict was first discussed a long time ago, in the 70s, by Geoff Parker, but it was just a curiosity. Everything changed after Bill did his groundbreaking experiments with Drosophila in mid-90s. After that, there was an explosion of interest. But as I said, I couldn’t really understand what Bill was saying. I mean, he’s a good friend now and collaborator and we’ve been working a lot with him. But his writing style is too academic to my taste and was something where I’ve always had problems. So, at that time, I knew about his work, but didn’t really understand the logic. Bill had a paper in that book too, which, again, I found difficult to understand. But Dan Howard’s short article in the book basically explained everything in a way I could connect to the theoretical thinking that I’ve been always using. I think I started reading that book when I was still in Italy, and then I moved to the Netherlands, and I remember reading that particular chapter that Dan wrote, and everything kind of became clearer almost immediately. I think it was in July, probably. Once I saw the logic, the model immediately materialized, and I think it took maybe one week to produce the model, and a few more weeks to write the paper. I think I had the paper ready by mid-July. I then went to the ESEB evolutionary biology meeting in Barcelona and met Göran Arnqvist. I went to his talk on sexual conflict, and later gave him my article and asked him for comments, which he gave. I think I then submitted it right away, like in September, after I got back from the conference. It was very quick.
HS: Did you, at that point, know Bill Rice and Dan Howard?
SG: I was a postdoc in Davis in the early 90s, Bill was passing through and I interacted with him. He remembers me, but I don’t remember much about that interaction. And then in 1998 both of us were interviewing for the same position in Santa Barbara. He got it and I didn’t. I knew Dan Howard’s name but I don’t think I met him at that time. Later, he too became a friend.
HS: Stepping back a bit, how did you get interested in theoretical evolutionary biology?
SG: It was a long time ago. I think I first heard about it I was still in high school. I was thinking about education and stuff and physics was the area I was most inclined to. So I went to study in Moscow State University, in the physics faculty. But I got bored with physics very quickly. I switched to biophysics but got bored with that too. In the Soviet Union at that time, it was five years and a half of studies. So it was kind of intermediate between Bachelor’s and Master’s degree. By the fifth year, I was already doing mathematical ecology models, and I was hired by an agricultural research institute as a statistician and that’s how I got into genotype-environment interaction. The Soviet Union was an enormous country with diverse climate, and because of the socialistic economy, we wanted to do everything planned, and we would plant one variety and hope that it would work across all the time zones. So, yeah, I moved from theoretical physics to biophysics to ecology and evolutionary Biology; that was the chain of events.
HS: I want to ask you about the people you acknowledge – C. R. B. Boake, M. B. Cruzan and G. McCracken. How did you know these people and how did they help?
SG: They were all, at the time, my colleagues in the Department of Ecology and Evolutionary Biology. I’ve, subsequently, had papers with Christine Boake and Mitch Cruzan, but not with Gary McCracken. I suspect I was just asking them to comment on the manuscript, fix the English, and stuff like that.
HS: Did you write the paper when you were back in the US?
SG: I think so, but I’m not sure. I remember that I was doing the equations when I was still in Utrecht.
HS: Did this paper have a relatively smooth ride through peer review? Was Nature the first place you submitted it to?
SG: Yeah. I submitted it to Nature and I think it was pretty smooth. Yeah. It was my best experience with Nature. I suspect that Bill Rice was one of the reviewers. I should probably ask him. The reviews were quite favorable.
HS: At the time when the paper came out, do you remember how it was received?
SG: It was not easy at that time to see the reaction. Now, you can see it quite quickly by the number of downloads and the social media reaction. I suspect it was known immediately because I was invited to a couple of big meetings on social conflict. I didn’t check how quickly citations started to show up.
HS: Do you have a sense of what this paper mostly gets cited for.
SG: First, that it was the first paper on this subject. Geoff Parker had written something a long time before but the approach he used was completely different. He was using game theoretic stuff. On the other hand, Bill Rice’s ideas were always about the dynamics. I think my paper was the first one to study the dynamics and the model there was very simple. The couple of cool graphs also helped.
HS: What kind of impact did this paper had on your career?
SG: I think it was an important paper. It was published in Nature. It was kind of my first step into the sexual conflict field. After that I’ve written, maybe, 10 different papers on this topic. I’ve worked a lot on sexual conflict. My collaborations with Bill Rice have been very fruitful. Also, a year or two after that, I got involved in a big collaborative project with Dan Howard – Bill was also a co-PI– and we got a big grant from the NSF. Through this, a number of other collaborations got established. Yeah, so it is an area where I think my name is known, the theoretical foundations of the field of sexual conflict.
HS: It’s now 17 years since this paper was published. I wanted to ask you to revisit the main conclusion of this paper and reflect on where you stand with regard to what you said in the paper at that point. I’ll read out the relevant sentences: “continual change in [male and female traits involved in reproduction] at a constant speed is expected whenever females (or eggs) experience fitness loss from having too many compatible males (or sperms). The plausibility of runaway coevolution increases with increasing population size.”
SG: The situation is quite different now. Two years ago, Bill Rice and I edited a collected volume on sexual conflict, The Genetics and Biology of Sexual Conflict, and I wrote a review chapter for that volume on the theoretical literature on sexual conflict. The conclusion that I was getting there, from a theoretical perspective, was that there are at least six different types of dynamics that can happen in models of sexual conflict. The Nature paper identified only two of them – continuously coevolutionary change and random drift along the line of equilibrium. Subsequent work produced a number of other things. And then, in terms of Bill’s idea about sexual conflict being “an engine of speciation”, I think I end my review paper from two years ago by saying that, yes, indeed, it’s an engine of speciation, but it works only under the right conditions. If conditions are not right, the engine will just stall. So, the story, of course, is much richer today.
HS: You say “One way to test [whether high species richness in resource-rich environments is caused by evolution of reproductive barriers driven by sexual conflict] is by comparing the degree of reproductive isolation between natural or laboratory populations that have been maintained for some time at different densities. The hypothesis that rapid speciation is driven by sexual conflict predicts that reproductive barriers will be stronger between populations with high densities than between populations with low densities. Another prediction is that the number of species in a clade should positively correlate with species abundance. It remains to be seen whether these hypotheses are supported by data”. Have the experiments you suggested been done, and to what extent are these hypotheses supported?
SG: Well, yeah, there was actually a paper also in Nature three years later, in 2003, written by Martin and Hosken. The title is The evolution of reproductive isolation through sexual conflict. Basically, that paper tested my predictions experimentally, using fly populations, and they confirmed the predictions. Also, in the recent review paper that I just mentioned, I looked at some other literature. It, kind of, goes all over the place, which is now expected because, even from a theoretical perspective, there are number of different dynamics that you can expect.
HS: Have you ever read the paper after it was published?
SG: Well, I think I used the pictures from the paper on a couple of occasions. But no, not really. I would not say that I read it carefully.
HS: Would you count this paper as one of your favorites?
SG: It depends on what you mean by favourite. From the point of view that I had a paper in Nature, yeah, that was pretty cool. From the point of view of being proud of doing something challenging: no. I think everything was quite straightforward. It was a matter of sitting down, writing some equations and solving them. It was not like a big theoretical challenge that you were proud of to be able to solve. It was straightforward.
HS: What would you say to a student who is about to read this paper today? Would you guide his or her reading in any way? Would you ask them to read certain other papers along with this? Would you add any caveats to keep in mind when reading this paper published 17 years ago?
SG: Well, it’s a short and simple paper. You don’t really need to have a strong theoretical background to read it. So, it may be a good read for students. As far as caveats are concerned, again, I mentioned the review paper, where we show that dynamics are much, much more complicated, in a theoretical perspective. I think there are also some good lessons there about the way science is done. You can come up with a cool idea that generates an explosion of interest. The whole story of sexual conflict – the initial appearance of the idea, and then, after 20 years, after one generation, a reappearance and explosion of interest – is a good story for students.
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