Advances in Genetics (eBook)

Once landing on a fruit fly-colonized food patch, females are almost immediately courted by males (Wertheim et al., 2006). Despite the lack of conspicuous solicitation behavior by females, males are drawn to them and display intense courtship. Male courtship consists of approaching the female, mostly from the back, tapping her abdomen, extending one wing, and vibrating it to produce a song, circling the female while doing so, extending his proboscis to make contact with the female genitals and ultimately swinging his abdomen at the female to attempt copulation (reviewed by Yamamoto & Koganezawa, 2013). While this ritual is required by the female to accept mating, it can also become detrimental to her. At high population densities, intense male courtship harasses females. If she stays, she will have reduced fecundity and early mortality, probably due to disruption during oviposition and exhaustion resulting from constantly decamping (Markow & Manning, 1980; Partridge et al., 1987). If she leaves, she has reduced access to food and increased exposure to predators (Wertheim et al., 2006). Males are however not completely indiscriminate and exert a choice on which females they preferentially court (Long et al., 2009). In this section, we will review the mix of cues that signal female attractiveness. We will then see that attracting males allows females to sample the self-reporting cues that males display during courtship. Finally, we will review our knowledge of the genetics and neurobiology underlying the female decision to accept mating.

Cues signaling a female’s attractiveness are most likely honest signals of her fecundity. Otherwise, over an evolutionary time-frame, males who mate with less-fecund females will be selected against and the alleles that support such decisions will decrease in frequency. Males given a choice between different females prefer the larger ones, which have higher life-time fecundity (Long et al., 2009). Size appears as an honest indicator of fecundity probably reflecting the size and thus capacity of the ovary, which occupy most of the female abdomen. Size is however constrained by the cost of exposure to heightened male harassment leading to reduced lifetime fecundity (Byrne & Rice, 2006; Long et al., 2009). Interestingly, the sex appeal of size is social context-dependent. The presence of other females matters to individual females because harassment is only focused on larger females when smaller females are present (Long et al., 2009), and between the male suitor and the target of his affection suggesting that flies are capable of social comparisons (Turiegano et al., 2012). Because larger females require longer courtship by males in order to accept mating (Turiegano et al., 2012), it is possible that female size might relate to receptivity.

What exactly makes size attractive is unknown; it could affect the amount of smell a female can produce, or affect her gait. Size is regulated by the insulin pathway, (Wu & Brown, 2006). Choosiness could be also experience-based; the frequency and intensity by which a female is courted could influence her choosiness. This renders it difficult to assign a precise genetic contribution to this sex-appeal factor. To our knowledge, mate preference assays with blind males experimentally exposed to a small and a large female have not been performed but this experiment would help sorting these issues.

The way a female moves, or does not move, contributes to her attractiveness. The Shibire temperature-sensitive mutation (Shits) causes temporary paralysis at higher temperature but normal locomotion at room temperature (Grigliatti et al., 1973). When Shits females are temporarily immobilized by application of restrictive temperature, they are courted half as much as at the permissive temperature (Tompkins, Gross, Hall, Gailey, & Siegel, 1982), showing that female movement stimulates male courtship. It is however difficult to separate the effect of female size, movement pattern, and gait as perception of all these cues are affected by male blindness. The recent identification of motion detection neurons in the visual system and the existence of tools to assay their specific function may help resolve this issue (Maisak et al., 2013). Moreover, part of the attractiveness of female movement appears to come from the noise it produces as female movement generates acoustic signals that arouse males (Ejima & Griffith, 2008). There is, however, nothing sex-specific in this signal as the noise made by males also enhances male arousal.

What exactly in the movement of females triggers male courtship? Dopamine is a regulator of overall locomotor activity levels. Reduction in amounts of dopamine by application of a pharmacological inhibitor of tyrosine hydroxylase, an enzyme controlling the final stage in the synthesis of dopamine, does slow down females but was not associated with a change in male courtship (Wicker-Thomas & Hamann, 2008). These data suggest that the overall level of locomotor activity is not the parameter of interest in female movement, but rather her gait or pattern of activity. Female activity patterns are indeed different from those of males: in isolation females constantly modulate their activity pattern, showing bouts of start and stop motion, whereas males have a steadier more constant walking pace (Belgacem & Martin, 2002, 2005; Gatti, 2000; Martin et al., 1999). This difference in locomotion is controlled by a small cluster of neuroendocrine insulin-producing neurons in the pars intercerebralis (PI), a neurosecretory center sitting atop the brain midline (Belgacem & Martin, 2002). Feminization of these neurons in an otherwise male results in female-like pattern of locomotor activity (Gatti et al., 2000). Ablation of the insulin-producing neurons in the adult stage (ablating too early results in abnormal development) gives males a female pattern of activity, but has no effect in females indicating that female movement is the default state (Belgacem & Martin, 2002, 2005). The PI regulates locomotion via insulin circulating throughout the body because transplanting these neurons in the abdomen of a male is sufficient to feminize locomotor activity (Belgacem & Martin, 2002). The insulin signal targets the corpus allatum (CA), a gland located in the first thoracic segment, as demonstrated by the necessity of the insulin receptor in the CA for male mode of locomotor activity (Belgacem & Martin, 2007), and ablation of the CA results in female-like pattern of activity in males (Belgacem & Martin, 2005). CA is likely to control locomotor activity via differential release of juvenile hormone (JH) in males because feeding males with a JH inhibitor gives them a feminized pattern of locomotor activity (Belgacem & Martin, 2002). Insulin-producing cells in the PI control JH expression by the CA. Sexually dimorphic activity is thus controlled by a neuroendocrine axis composed of the PI and the CA. The last-known output of this pathway is JH but because this hormone has multiple physiological effects, it remains unknown what the final output controlling locomotor activity is.

That sexually dimorphic locomotor activity of females is important for their attractiveness has, however, not yet been demonstrated. If masculinization of PI neurons confers male-typical locomotor patterns, females with a male gait should be less attractive than control females. However, this experiment would not tease apart the role of acoustic cues produced during walking and the visual cue of movement.

Looks are not everything, and are not necessary for female attractiveness, since flies can mate in the dark (Gailey, Lacaillade, & Hall, 1986). Bastock and Manning (1955) noted that although males orient toward females, they do not perform any courtship behavior at a distance >5 mm. Computer-mediated observation shows that males and females interact at a distance of 2.5–3.5 mm (Branson, Robie, Bender, Perona, & Dickinson, 2009). It appears that close proximity cues “release” further courtship steps (Bastock & Manning, 1955),which are probably chemicals perceived via the olfactory or gustatory system (Gailey et al., 1986; Krstic, Boll, & Noll, 2009; Trott, Donelson, Griffith, & Ejima, 2012). Furthermore, transfer of female chemical extracts either by blowing air through a chamber containing females into a chamber (Averhoff & Richardson, 1974; Shorey & Bartell, 1970) or placing extracts on a piece of filter paper (Tompkins, Hall, & Hall, 1980) can trigger males to initiate courtship toward nearby flies. This indicates that female volatiles can confer momentary attractiveness to flies of any sex.

What are the attractive chemicals produced by females? Flies display hydrocarbon molecules at the surface of their body, called cuticular hydrocarbons (CHC) (Everaerts, Farine, Cobb, & Ferveur, 2010; Farine, Ferveur, & Everaerts, 2012; Ferveur, 2005; Jallon, 1984; Levine, Billeter, Krull, & Sodhi, 2010; Yew, Cody, & Kravitz, 2008; Yew et al., 2009). There are between 30 and 50 species of CHC and most are sexually dimorphic in either presence or amounts (Ferveur, 2005; Jackson, Arnold, & Blomquist, 1981; Jallon, 1984; Yew et al.,...