Individual and synergistic effects of male external genital traits in sexual selection

Abstract

Male genital traits exhibit extraordinary inter-specific phenotypic variation. This remarkable and general evolutionary trend is widely considered to be the result of sexual selection. However, we still do not have a good understanding of whether or how individual genital traits function in different competitive arenas (episodes of sexual selection), or how different genital traits may interact to influence competitive outcomes. Here, we use an experimental approach based on high-precision laser phenotypic engineering to address these outstanding questions, focusing on three distinct sets of micron-scale external (nonintromittent) genital spines in male Drosophila kikkawai Burla (Diptera: Drosophilidae). Elimination of the large pair of spines on the male secondary claspers sharply reduced male ability to copulate, yet elimination of the other sets of spines on the primary and secondary claspers had no significant effects on copulation probability. Intriguingly, both the large spines on the secondary claspers and the cluster of spines on the primary claspers were found to independently promote male competitive fertilization success. Moreover, when large and small secondary clasper spines were simultaneously shortened in individual males, these males suffered greater reductions in fertilization success relative to males whose traits were altered individually, providing evidence for synergistic effects of external genital traits on fertilization success. Overall, the results are significant in demonstrating that a given genital trait (the large spines on the secondary claspers) can function in different episodes of sexual selection, and distinct genital traits may interact in sexual selection. The results offer an important contribution to evolutionary biology by demonstrating an understudied selective mechanism, operating via subtle trait interactions in a post-insemination context, by which genital traits may be co-evolving.

A developmental atlas of male terminalia across twelve species of Drosophila

“…It was shown that in D. ananassae and its close relative, D. bipectinata , these spines are used to grasp the female genitalia to initiate copulation, and thus are important for precopulatory sexual selection ( Polak and Rashed, 2010 ; Grieshop and Polak, 2012 ; 2014 ). However, they also reduce the female fecundity, probably due to wounding during copulation ( Grieshop and Polak, 2014 ; Rodriguez-Exposito et al, 2020 ). Similarly, it was shown that the male anal plates of various species couple with the female oviscape to facilitate genital coupling ( Jagadeeshan and Singh, 2006 ; Kamimura and Mitsumoto, 2011 ; Yassin and Orgogozo, 2013 ).…”

Non‐visual cues and indirect strategies that enable discrimination of asymmetric mates

“…bipectinata , and D . ananassae ) with altered non‐intromittent genital spines fail to achieve copulation and have reduced pre‐ and post‐mating success (Grieshop & Polak, 2014 ; Polak & Rashed, 2010 ; Rodriguez‐Exposito et al, 2020 ).…”

“…Although not tested empirically for FA, similar issues with mating are known in other species. Drosophila melanogaster males that lack melanin in sex combs are impaired in their ability to grasp the female while mounting them (Massey et al, 2019), while males of other Drosophila species (D. kikkawai, D. bipectinata, and D. ananassae) with altered non-intromittent genital spines fail to achieve copulation and have reduced pre-and post-mating success (Grieshop & Polak, 2014;Polak & Rashed, 2010;Rodriguez-Exposito et al, 2020).…”