Does side matter? The evolution of asymmetric genitalia in livebearing fish
Final Report Abstract
Asymmetry, the departure from the standard bilaterally symmetrical body plan that most multicellular animals have, is a phenomenon that has attracted the attention of biologist for a long time. Most departures from bilateral symmetry are not by design but rather a result of instability during development. In fewer cases, morphological bilateral asymmetries clearly are adaptive. Yet, adaptive asymmetry is a relatively rare evolutionary phenomenon that is still poorly understood. Its investigation has the potential to be highly informative in terms of furthering our understanding of how selection acts on developmental processes and how adaptive traits are shaped by natural or sexual selection. Genital asymmetry is a particular case of adaptive asymmetry that has evolved multiple times in independent groups. However, its evolution is poorly understood, mostly because most species with asymmetric genitalia are not polymorphic. This means that within species, either a left- or a right-sided morph is solely present. The one-sided livebearer fish and the four-eyed fish are members of the Anablepidae family, and both, left and right-sided individuals can be found within populations. This provides a very good opportunity to explore the causes and consequences of the evolution of genital asymmetry. The main goal of the proposed research was to (1) map the evolutionary changes in genital asymmetry of Anablepidae fish into a genome-wide phylogeny, (2) determine if genome-wide divergence between left-sided and right-sided morphs of Anablepidae fish is evolving in natural populations, (3) determine if direction of genital asymmetry is heritable, and (4) explore if genital asymmetry affects mating success in these fish. This project made important contributions to a better understanding of evolution in the family Anablepidae, as we could show that: 1) The mode of asymmetry (i.e., antisymmetry versus directional asymmetry) in males has evolved at least three times in the genus Jenynsia and that female asymmetry has evolved once in the genus Anableps (Aim 1). 2) There are a few cryptic species in the genus Jenynsia. 3) Genital asymmetry correlates with mating behavior and some morphological traits, but otherwise, it is not globally associated to other asymmetric traits. 4) There is little genomic differentiation between left- and right-sided morphs in species within the family, but there are a few sites with elevated outlier Fst values that might be associated to causal loci (Aim 2). 5) The is no evidence that the direction of asymmetry is inherited, but at least in one species of Jenynsia, the pattern of inheritance is not completely random (Aim 3). 6) The variation in mating success is evident across species in the genus Jenynsia, despite that they show a coercive mating system, suggesting that post-copulatory sexual selection plays an important role in these species. In summary, we used a combination of approaches to determine the mechanisms involved in the evolution of genital asymmetry in fishes of the family Anablepidae. We found that asymmetry itself, and the direction of departure from symmetry has evolved multiple times within the family. We also found that the direction of asymmetry is most likely randomly determined, rather than inherited, explaining the maintenance of this polymorphisms in natural populations. Finally, we found that there is variation in mating success across species within the family, suggesting that post-copulatory mechanisms might play a role in the determination of paternity in this group of fishes with coercive mating.
Publications
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(2019). Asymmetry in genitalia is in sync with lateralized mating behavior but not with the lateralization of other behaviors. Current Zoology, zoz019
Torres-Dowdall, J., Rometsch, S. J., Aguilera, G., Goyenola, G., & Meyer, A.
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(2019). Molecular and morphological convergence to sulfide-tolerant fishes in a new species of Jenynsia (Cyprinodontiformes: Anablepidae), the first extremophile member of the family. PLoS one
Aguilera, G., Terán, G.E., Mirande, J.M., Alonso, F., Rometsch, S. J., Meyer, A., & Torres- Dowdall, J.
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(2020): The direction of genital asymmetry is expressed stochastically in internally fertilizing anablepid fishes. In: Proceedings. Biological sciences 287 (1930), S. 20200969
Torres-Dowdall, J., Rometsch, S. J., Kautt, A.F., Aguilera, G., & Meyer, A.
