Copulation behaviour ofGlossina pallidipes(Diptera: Muscidae) outside and inside the female, with a discussion of genitalic evolution

Abstract

If species-specific male genitalia are courtship devices under sexual selection by cryptic female choice, then species-specific aspects of the morphology and behaviour of male genitalia should often function to stimulate the female during copulation. The morphology and behaviour of the complex, species-specific male genitalia of the tsetse fly, Glossina pallidipes Austen, were determined from both direct observations and dissections of flash-frozen copulating pairs; we found that some male genitalic traits probably function to stimulate the female, while others function to restrain her. The male clamps the ventral surface of the female's abdomen tightly with his powerful cerci. Clamping does not always result in intromission. Clamping bends the female's body wall and her internal reproductive tract sharply, posteriorly and dorsally, and pinches them tightly. The male performed sustained, complex, stereotyped, rhythmic squeezing movements with his cerci that were not necessary to mechanically restrain the female and appeared instead to have a stimulatory function. Six different groups of modified setae on and near the male's genitalia rub directly against particular sites on the female during squeezing. The designs of these setae correlate with the force with which they press on the female and the probable sensitivity of the female surfaces that they contact. As expected under the hypothesis that these structures are under sexual selection by female choice, several traits suspected to have stimulatory functions have diverged in G. pallidipes and its close relative, G. longipalpis. Additional male non-genitalic behaviour during copulation, redescribed more precisely than in previous publications, is also likely to have a courtship function. The elaborate copulatory courtship behaviour and male genitalia may provide the stimuli that previous studies showed to induce female ovulation and resistance to remating.

Evolution of genitalia: theories, evidence, and new directions

“…Copulation in various mammals also involves behavior apparently designed to stimulate the female with the genitalia (summary Eberhard 1996; see also Dixson 1998), and some aspects of copulation behavior in rodents correlate with indicators of increased probability of competition with sperm from other males (Stockley and Preston 2004). In addition, the male genitalia of several insects and spiders perform long, highly rhythmic series of taps, or squeezes on membranous portions of the female, that also suggest that stimulation of the female is important; these include a dryomyzid fly (Otronen 1990), a buprestid beetle (Eberhard 1990), a sciarid fly (Eberhard 2001c), several sepsid flies in different genera (Eberhard and Pereira 1996;Eberhard 2001bEberhard , 2003Eberhard , 2005, a pholcid spider (Huber and Eberhard 1997;Peretti et al 2006), some scathophagid flies (Hosken et al 2005), several species of tsetse flies (Briceño et al 2007;Briceño and Eberhard 2009), and the hesperiid butterfly Urbanus dorantes and the katydid Idiathron sp. (W. G. Eberhard unpub.).…”

“…A good example of the possible payoffs from this type of experiment comes from a recent study of the tsetse fly Glossina pallidipes. Males have sexually modified, species specific cerci and other genital structures that clasp the female's abdomen during copulation (Briceño et al 2007). Alteration of the speciesspecific form of the male cerci and of his abdominal sternites elicited changes in post-copulatory female reproductive responses, suggesting that the male structures are under sexual selection by cryptic female choice: ovulation and the amount of sperm arriving in the spermathecae were reduced, and female tendency to remate was increased (Briceño and Eberhard 2009).…”

Experimental demonstration of possible cryptic female choice on male tsetse fly genitalia

“…Several possible mechanisms could have been responsible for reductions in sperm storage. It might be that the male refrained from producing spermatophores or from filling them with sperm, due to a lack of internal female responses allowing him to position his genitalia appropriately at the opening of the spermathecal duct (Briceñ o et al, 2007). Alternatively, males may have successfully deposited spermatophores filled with sperm, but females may have failed to transport the sperm to their spermathecae, or discarded spermatophores before their sperm entered her spermathecal ducts.…”

“…), as would be expected if genital squeezing is under sexual selection. Several portions of the male's genitalia that contact the female have morphological modifications that appear designed to stimulate the female, including the cerci, the surstyli, the inferior claspers, and the abdominal sternite 5 (Briceñ o et al, 2007;Briceñ o and Eberhard, unpub. ).…”

“…The male's cerci rhythmically squeeze the female during much of the copulation (Briceñ o and Eberhard, unpub.). The substantial force exerted by cercal squeezing causes the ventral wall of the female's abdomen to bend inward so sharply and deeply that the entire cercus is generally hidden from view (VanderPlank, 1948;Briceñ o et al, 2007).…”