Species-specific behavioral differences in tsetse fly genital morphology and probable cryptic female choice

Abstract

A long-standing mystery in morphological evolution is why male genitalia tend to diverge more rapidly than other structures. One possible explanation of this trend is that male genitalia function as “internal courtship devices,” and are under sexual selection by cryptic female choice (CFC) to induce female responses that improve the male’s chances of fathering her offspring. Males of closely related species, which have species-specific genital structures, are thought to provide divergent stimulation. Testing this hypothesis has been difficult; the presumed genital courtship behavior is hidden from view inside the female; appropriate experimental manipulations of male and female genitalia are often technically difficult and seldom performed; and most studies of how the male’s genitalia interact with those of the female are limited to a single species in a given group, thus limiting opportunities for comparisons of species-specific structures. In this chapter, we summarize data from morphological, behavioral, and experimental studies of six species in the tsetse fly genus Glossina, including new X-ray recordings that allowed visualization of events inside the female during real time. Species-specific male genital structures perform dramatic, stereotyped, rhythmic movements, some on the external surface of the female’s abdomen and others within her reproductive tract. Counting conservatively, a female Glossina may sense stimuli from the male’s genitalia at up to 8 sites on her body during some stages of copulation. As predicted by CFC theory, these movements differ among closely related species; some of the species-specific male genital structures that are apparently designed to stimulate the female move with different rhythms against different portions of the female’s body in different species. In no case does female morphology show signs of counter adaptations to avoid or reduce male stimulation or to fit mechanically with male structures, as predicted by some alternative hypotheses to explain rapid divergent evolution of genitalia; for most male structures, the corresponding portion of the female is featureless and uniform in different species. Experimental modifications of one species-specific genital structure (the cercus), and of the possible female sense organs in the portion of the female that this male structure contacts during copulation, elicited female reproductive responses in two species (reductions in sperm transport, ovulation, and resistance to further copulations) that could result in cryptic female choice favoring this male structure.