Something gone awry: unsolved mysteries in the evolution of asymmetric animal genitalia

The great diversity in genital shape and function across and within the animal phyla hamper the identification of specific evolutionary trends that stretch beyond the limits of the group under study. Asymmetry might be a trait in genital morphology that could play a unifying role in the evolutionary biology of genitalia. Here, I review the current knowledge on the taxonomic distribution, phylogenetic patterns, genetics, development, and ecology of asymmetric (chiral) genitalia. Asymmetric genitalia (male as well as female) have evolved from bilaterally symmetric ones (and sometimes vice versa), innumerous times in most animal taxa with internal fertilisation, and especially in Platyhelminthes, Arthropoda, Nematoda, and Chordata. In groups with asymmetric genitalia, chiral reversal (where species carry genitalia that are the mirror image of those in other, congeneric, species) is common, but antisymmetry (both mirror images present within a species) is rare. Although indications exist that, at least in insects, asymmetry evolves as a compensatory response to the evolution of maledominant mating positions, many mysteries remain. Main questions are: (i) is genital asymmetry developmental-genetically linked with other (visceral, external) asymmetries? (ii) is genital asymmetry usually correlated with a change in mating position? (iii) is asymmetry more likely to evolve in response to cryptic female choice or sexually-antagonistic coevolution? (iv) why is antisymmetry so rare and how does chiral reversal evolve? Based on an overview of the taxonomic patterns, I advocate a research program that makes use of the simple, binary nature of left-right asymmetry to test hypotheses for its evolution with experimental and comparative methods. I also provide tables with full or summarised data on (a) genital asymmetry across all animal phyla with internal fertilisation; (b) genera with dextral as well as sinistral species; (c) species with dextral as well as sinistral individuals; (d) genera with symmetric as well as asymmetric species; (e) species with symmetric as well as asymmetric individuals.

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