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Looking under the light pulse: an integrative case study on the mating behaviors of Caribbean sea fireflies (Crustacea, Ostracoda, Cypridinidae)

Abstract

Some of the most extreme and diverse phenotypes in nature are mating behaviors. Poised to be an engine for biodiversity during the speciation process, and some of the most rapidly evolving traits, these extreme phenotypes are widely studied at the whole organism-level, yet intractable at other levels of biological organization due to their inherent complexity as an emergent property. Although we have a strong theoretical understanding of the ecological processes that contribute to the diversification of these behaviors, we have few studies able to resolve how evolution acts on the genome to generate such diversity. Our understanding of the genetic basis of behavior is much more limited than other phenotypes, and even more so when we wish to understand how behaviors diverge between species. In this thesis, I present a series of integrative studies dissecting the contribution of important proteins on the phenotypic evolution of mating behaviors, focusing on the fantastical displays of Caribbean ostracods (affectionately, "sea fireflies"). Males of ~100 species use secretions of bioluminescent, mucus-like proteins to attract females, creating diverse patterns that vary between species and guide females towards individuals during the mating spree. I present evidence that functional and molecular divergence of these proteins contributes to changes in their light-producing function. In theory, this links to mating display structure, as it may influence the visible duration of individual bioluminescent secretions. By analyzing in vivo and in vitro differences in protein function, I find that the evolutionary lability of this display duration may be constrained by its underlying mechanisms. Differences in these mechanisms contribute to the overall form of single pulses within a mating display, and molecular patterns of evolution point towards both purifying and diversifying selection acting on protein function. Lastly, using artificial playback experiments, I present further evidence that male displays influence female behavior, supporting the idea that these signals may be under sexual selection but not necessarily important in sea firefly speciation. Together, these data lend credence to the hypothesis that key genes can be hotspots of evolutionary divergence during species radiation but that their effects might be contingent upon other constraints, showcasing how diverse evolutionary forces are important in the evolution of behavior.

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