How conflict shapes evolution in poeciliid fishes
Evolving a placenta means provisioning babies after rather than before the egg is fertilized. This change in provisioning changes the venue of sexual conflict, with consequences for the evolution of male morphology, behavior and speciation rate.
You probably think that great discoveries are made in the lab or field, but mine was in the library, in 1987. I was writing a chapter for Meffe and Snelson’s “Ecology and Evolution of Livebearing Fishes (Poeciliidae)” and discovered papers written in the 1930’s and 40’s by C. L. Turner about placentas in the fish family Poeciliidae. This family includes the familiar pet-store fish like guppies, platys, swordtails and mollies. One noteworthy feature of Turner’s work is that that the placenta had clearly evolved more than once. I was more amazed to find that only a small handful of papers had followed up on the discovery. I decided I would describe how mothers provisioned offspring for all species in the family (now around 250). This meant travelling to eight Latin American countries to collect fish and working with collections from 6 museums. I once had my “night in the museum” when I stowed away in the back of a lab in the Smithsonian so I could work all night and dissect more fish.
One day in the 1990’s, after I had a pretty good sense of who had placentas, I was touring a large pet store and realized that none of the livebearers on sale had placentas. It was not because those with placentas were hard to breed. I put some of them in the “hard to kill” category, meaning that they will thrive and multiply with little care. I wondered if it was because it was only those without placentas that had the fancy males that inspire the popularity of these fish in the pet trade.
This observation about who was in pet stores stuck with me but I never acted on it. Bart Pollux pursued it and proved that there really was an association between the elaboration of sexually selected traits in males and the absence of placentas in females 1. He made the connection with Zeh and Zeh’s viviparity-driven conflict hypothesis, which provided the conceptual framework for developing hypothesis for how the venue for sexual conflict should change as females evolve to provision offspring after, rather than before, eggs are fertilized. Rob Meredith and Mark Springer developed the DNA-based phylogenetic tree for the family, including a generous sampling of outrgoups from the order (Cyprinodontiformes) and beyond, which is essential for accurate ancestral-state reconstruction. Andrew Furness mastered the comparative methods necessary to extend Bart’s results so we could address the more specific questions in the current paper. Here we refine the connection between the evolution of the placenta, how it shifts the venue of conflict from pre-copulatory to post-copulatory mate choice, to and how this shift affects male mating strategies and the evolution of sexually selected traits in males. The connection between conflict and the accelerated rates of speciation in lineages with fancy males was an unexpected bonus.
I once thought Robert Trivers’ parent-offspring conflict proposal was among the silliest of ideas because parents and offspring have such a strong interest in each other’s welfare. It is clear to me now that conflict is inevitable and profound in its contribution to evolution. Still, the unfolding story in these fish seems more like science fiction than science because of the emerging connections between the evolution of how mothers provision offspring, how they choose their mates, how male traits evolve, and the rate of speciation. We did not set out to study these phenomena. This is just where the work led us and my colleagues.
URL for the paper:
1 Pollux, B. J. A., Meredith, R. W., Springer, M. S., Garland, T. & Reznick, D. N. The evolution of the placenta drives a shift in sexual selection in livebearing fish. Nature 513, 233-236, doi:10.1038/nature13451 (2014).