Microscale laser surgery reveals adaptive function of male intromittent genitalia

Abstract

The leading hypothesis for the evolution of male genital complexity proposes that genital traits evolve in response to post-insemination sexual selection; that is, via cryptic female choice or sperm competition. Here, we describe a laser ablation technique for high-precision manipulation of microscale body parts of insects, and employ it to discern the adaptive function of a rapidly evolving and taxonomically important genital trait: the intromittent claw-like genital spines of male Drosophila bipectinata Duda. We demonstrate experimentally and unambiguously that the genital spines of this species function to mechanically couple the genitalia together. The excision of the spines by laser ablation sharply reduced the ability of males both to copulate and to compete against rival males for mates. When spineless males did succeed to copulate, their insemination success and fertilization rate were not statistically different from controls, at odds with the post-insemination sexual selection hypothesis of genital function and evolution. The results provide direct experimental support for the hypothesis that genital traits evolve in response to sexual selection occurring prior to insemination.

Experiments with genitalia: a commentary

“…Finally, female re-mating and ovulation were both affected by male genital morphology in one group where these female responses were checked [26,27]. In sum, a failure to find an effect on sperm precedence and sperm transfer use does not justify rejection of post-copulatory sexual selection on genitalia [22] (nor does a similar finding with respect to copulatory courtship rule out post-copulatory sexual selection [10]). …”

“…Interpretations based on incomplete sets of alternate hypotheses A second problem shared by some of the current crop of studies [21,22,28] is that the interpretations of results failed to discuss the possibility that male genital structures are under sexual selection to stimulate the female. Given that the first thorough discussion of sexual selection and genital evolution emphasized this hypothesis [3], these omissions are surprising.…”

“…Often these variables have been measured when females mated with males that differ in genital morphology or behavior [10][11][12]15,16,[19][20][21][22]25]. Although sperm transfer and paternity are relevant, they provide an incomplete picture of possible genital functions.…”

“…However, the relative importance of three different types of sexual selection (sperm competition, cryptic female choice and sexually antagonistic coevolution) is debated [4,7,8]. Recently, there has been a welcome burst of experimental studies designed to test these hypotheses by checking the effects of male genital morphology and behavior on male reproductive success [9][10][11][12][13][14][15][16][17][18][19][20][21][22][23][24][25][26][27][28]. Given that many of these studies share important shortcomings, and because there is likely to be further work on this topic (after all, there are probably millions of species showing rapid genital divergence), it is useful to discuss them critically to help researchers formulate hypotheses and interpret results more precisely.…”

Experimental coevolution of male and female genital morphology

“…Sexual selection is widely believed to be responsible for this pattern of rapid and divergent evolution [1][2][3] , and there are a growing number of studies to support this view. The size or shape of a male's genitalia can influence his ability to engage the female in copula [3][4][5] , deliver his ejaculate to her reproductive tract 6,7 , or gain paternity of offspring she produces 8,9 . Male genitalia can therefore be subject to sexual selection.…”