Evolutionary basis of intermale sexual behavior by multiple pheromone switches in Drosophila
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Abstract
We have identified a Drosophila species which exhibits spontaneous and robust intermale sexual behavior. D. santomea males distinguish conspecific sexes but court both vigorously and seldom attack. Elevated intermale courtship stems from at least three evolutionarily derived pheromonal changes. In males, the sexually monomorphic cuticular pheromone 7-tricosene promotes rather than inhibits courtship and the courtship-inhibiting olfactory pheromone cVA is reduced 84-92% compared to close relatives. The third switch is in D. santomea females, where cVA suppresses rather than promotes sexual receptivity. Female cVA aversion and male cVA reduction may have co-evolved to maintain efficient intraspecific mating but prevent hybridization with the sympatric sibling species D . yakuba . High intermale courtship and low cVA also co-occur and appear selectively derived in a distant monomorphic species D. persimilis , implying pheromonal and social behavioral convergence. Changes in pheromone valence and levels may therefore explain the recent evolutionary emergence of intermale sexual behavior in Drosophila .
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A potential evolutionary explanation for the derived male cVA reduction in D. santomea was lacking until our unexpected discovery of a second sexual valence switch (and third pheromonal change in total), this time in the behavioral response to cVA by females. cVA promotes mating receptivity in D. melanogaster females (89, 130, 131) but has the opposite effect in D. santomea. The switch may be related to interspecific sexual dynamics between D. santomea and D. yakuba at their geographic boundary in São Tomé. D. yakuba males court D. santomea females vigorously (120, 121) and rare (sterile) F1 hybrid males can be collected within the sympatric zone (116–118). Thus, we speculate that the D. santomea female cVA valence switch arose due to ongoing selection pressure to maintain reproductive isolation from D. yakuba (122). If this …
A potential evolutionary explanation for the derived male cVA reduction in D. santomea was lacking until our unexpected discovery of a second sexual valence switch (and third pheromonal change in total), this time in the behavioral response to cVA by females. cVA promotes mating receptivity in D. melanogaster females (89, 130, 131) but has the opposite effect in D. santomea. The switch may be related to interspecific sexual dynamics between D. santomea and D. yakuba at their geographic boundary in São Tomé. D. yakuba males court D. santomea females vigorously (120, 121) and rare (sterile) F1 hybrid males can be collected within the sympatric zone (116–118). Thus, we speculate that the D. santomea female cVA valence switch arose due to ongoing selection pressure to maintain reproductive isolation from D. yakuba (122). If this explanation is correct, it would imply that D. santomea females use the high level of cVA on D. yakuba males as a sex- and species-identifying cue to ward off unwanted advances from heterospecific suitors (though we cannot exclude that D. yakuba courtship song is also used by D. santomea females for species discrimination) (61–63). This female aversion to cVA may have led in turn to reduced cVA production by D. santomea males under sexual selection pressure (140).However, two other evolutionary scenarios are also possible. D. santomea males may have initially reduced cVA abundance due to neutral drift or to pheromonally distinguish themselves from D. yakuba males (141), which in turn may have pressured D. santomea females to develop cVA aversion by sexual selection operating in the reverse direction. Alternatively, D. santomea female cVA aversion and male cVA reduction may have evolved simultaneously, potentially in genetic linkage (142). In any of these scenarios, the ultimate outcome would still be an elegant pheromonal mechanism which maintains efficient intraspecific mating in D. santomea while minimizing unfit hybridization with D. yakuba. Interestingly, a similar sexual reversal from cVA promoting to inhibiting female receptivity has been reported in one other drosophilid, the agricultural pest D. suzukii (143), whose males show fully eliminated cVA production (144). The evolutionary circumstances and selection pressures leading to D. suzukii cVA changes are unclear, however, as are potential consequences for intermale social behaviors.
Providing three independently compelling hypotheses for the evolutionary basis of this behavior is very much appreciated. Observation of these mating behaviors in their natural context (São Tomé) would both strengthen these hypotheses and may provide crucial ethological data to distinguish between them.
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