Mating behaviour and spermatophore morphology: a comparative test of the female-choice hypothesis

Complex, species-specific morphology of genitalia or "paragenitalia" such as spermatophores is traditionally considered an adaptation to prevent heterospecific matings. Eberhard argued against this lock-and-key hypothesis and suggested that elaborate male genitalia evolve through female preference for increased tactile stimulation. He found support for this argument in a cross-taxon comparison of spermatophore complexity among species with different degrees of contact between the sexes during spermatophore transfer. After expanding Eberhard's list of species, we tested the female-choice hypothesis with appropriate controls for phylogeny and using naive human subjects to rank spermatophore complexity. Our results uphold Eberhard's conclusion that the lock-and-key hypothesis does not explain the distribution of spermatophore complexity among taxa; however, they do not clearly support female choice as an alternative explanation. Other factors that may influence spermatophore complexity include environmental stress and whether spermatophores are deposited on a substrate. Because we seldom know what parts of a spermatophore are touched by females, or whether there are spermatophore-associated pheromones, human visual assessment may not always allow accurate judgement of realized spermatophore complexity.