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;

Ovoviviparity and genital evolution: a lesson from an earwig species with coercive traumatic mating and accidental breakage of elongated intromittent organs

“…In female tsetse flies (Diptera: Glossina), eggs are fertilized by spermathecal sperm, as in oviparous dipterans, while a specialized maternal organ nourishes the hatched larvae in the uterus (adenotrophic viviparity: Benoit et al ., ). Male flies use their genitalia as internal courtship devices during mating to stimulate the females (Briceño & Eberhard, , b, ), although their relation to viviparity is unclear at present.…”

Mating Is a Give-and-Take of Influence and Communication Between the Sexes

“…These include the belated acceptance of Darwin's proposal that female mate choice is widespread in nature (Darwin 1871;West-Eberhard 1983;Andersson 1994;Andersson and Simmons 2006); the discovery that male-male competition, courtship, and mate choice continue after mating begins (Eberhard 1985(Eberhard , 1996(Eberhard , 2009Birkhead and Møller 1998); and technical progress allowing the examination of genital behavior inside the body of the female (Briceño et al 2010;Eberhard 2011;Briceño and Eberhard 2015). Another major breakthrough may lie in the realization that as females make mating and fertilization decisions, the changes in their behavior and physiology that effect those decisions provide males with indications about their motivation and attitude.…”

Demonstrating sexual selection by cryptic female choice on male genitalia: What is enough?

“…Experimental alterations of species-specific male cercal teeth (dotted arrows in Fig. 1A) and possible female sense organs in a second species, G. morsitans, also resulted in decreased sperm storage and increased female remating (Briceño and Eberhard 2009b). Similar tests of the effects of the setae on male abdominal sternite 5, by painting over either the setae themselves or the possible female receptors on the dorsum of female abdominal tergite 6, also affected female ovulation and the likelihood of sperm in the female spermathecae.…”

“…Five different tufts and brushes of elongate setae on the male genitalia rub rhythmically against the female during copulation in the morsitans subgenus. These setae lack any ability to mechanically restrain the female, and their mechanical properties correlate with the likely sensitivity of the female surface that they contact (setae that contact female sclerites are more robust, while those that contact female membranes are more delicate), suggesting that they function to stimulate her during rhythmic male squeezing behavior (Briceño et al 2007;Briceño and Eberhard 2017a).…”

“…Females of G. pallidipes mated to males in which the modified lateral tips of his cerci (solid arrows in Fig. 1A) had been removed showed several responses: they were less likely to ovulate; they were more receptive to copulation from subsequent males; sperm were less likely to be present in their spermathecae 9-10 days following copulation; and, when present, sperm occurred in somewhat lower numbers (Briceño and Eberhard 2009a). Complementary experimental inactivation of possible female sense organs in the area contacted by the male's cerci (thus controlling for possible changes in male behavior in the preceding experiments), either by blocking them with an inflexible coating or by damaging them by contact with a hot needle gave similar, generally even more pronounced responses regarding ovulation, sperm transfer, and female remating (control females received nail polish or a hot needle just anterior to the area contacted by the male cerci).…”