The evolution and diversity of intra-male sperm translocation in Odonata: a unique behaviour in animals

Abstract

Behavioural diversity is a basic component of biodiversity, with implications in ecological interactions at the intra- and interspecific levels. The reproductive behaviour of Odonata (dragonflies and damselflies) is unique among insects and conditioned by the anatomical separation between the male’s reproductive organs and the intromittent organ. Prior to mating, males must translocate sperm from the genital pore in the ninth abdominal segment to the seminal vesicle located ventrally in the second abdominal segment. This behaviour, exclusive to odonates, is known as intra-male sperm translocation (ST). Here, we review the literature on ST and use phylogenetic comparative analyses to investigate the evolution of ST within the Odonata. Information on ST was compiled for 176 species, with the commonest variant being ST once per mating, after tandem formation (66%). Other variants found were ST involving precopulatory genital touching (10%), ST by the male alone before tandem (16%) or after copulation (5%), and repetition of ST during the same copulation (3%). The precopulatory genital touching might have evolved to detect female receptivity. ST before tandem formation might be favoured when mating opportunities are scarce and copulations are brief. ST after mating might be favoured if males need to be ready to copulate fast. Finally, repeated ST could have evolved through postcopulatory sexual selection in males with limited sperm removal ability, as a means to improve their sperm competition. The most plausible scenario for the evolution of ST is that the ancestors of the Odonata produced a spermatophore and attached it to the body, leading towards the evolution of the secondary genitalia in males. Our study emphasises the role of behavioural diversity to understand behavioural evolution.