Interspecific introgression reveals a role of male genital morphology during the evolution of reproductive isolation inDrosophila

Abstract

22Rapid divergence in genital structures among nascent species has been posited to be an early-23 evolving cause of reproductive isolation, although evidence supporting this idea as a widespread 24 phenomenon remains mixed. Using a collection of interspecific introgression lines between two 25Drosophila species that diverged ~240,000 years ago, we tested the hypothesis that even modest 26 divergence in genital morphology can result in substantial fitness losses. We studied the 27 reproductive consequences of variation in the male epandrial posterior lobes between Drosophila 28 mauritiana and D. sechellia and found that divergence in posterior lobe morphology has 29 significant fitness costs on several pre-fertilization and post-copulatory reproductive measures. 30Males with divergent posterior lobe morphology also significantly reduced the life span of their 31 mates. Interestingly, one of the consequences of genital divergence was decreased oviposition 32 and fertilization, which suggests that a sensory bias for posterior lobe morphology could exist in 33 females, and thus posterior lobe morphology may be the target of cryptic female choice in these 34 species. Our results provide evidence that divergence in genitalia can in fact give rise to 35 substantial reproductive isolation early during species divergence, and they also reveal novel 36 reproductive functions of the external male genitalia in Drosophila. 37 38 39 40 41 42 Prum 2015), the importance of divergence in genital morphology as a cause of RI has been 56 debated (Shapiro and Porter 1989; Masly 2012). 57 Nonetheless, several recent studies in a variety of taxa support the idea that 58 morphological divergence in external genitalia can indeed cause RI early during the speciation 59 process via both mechanical and sensory incompatibilities. One well-characterized example of 60 mechanical incompatibility between male and female genitalia occurs among several species of 61 Carabus (subgenus Ohomopterous) ground beetles, where species divergence in male aedeagus 62 morphology causes substantial damage to the female vaginal appendix during copulation, 63 resulting in reduced reproductive output, damage to the aedeagus, and even female mortality 64 (Sota and Kubota 1998; Nagata et al. 2007; Sota and Tanabe 2010; Kyogoku and Sota 2015). 65 of species divergence. Our test takes advantage of several D. mauritiana-D. sechellia genetic 106 introgression lines that possess small chromosomal segments (~1.5 Mb on average) of the D. 107 mauritiana genome within a predominantly D. sechellia white (w) genomic background (Masly 108 and Presgraves 2007). Pure species D. mauritiana possesses small finger-shaped PLs, whereas 109 D. sechellia possesses much larger goose-headed-shaped PLs, with a long neck and characteristic 110 "beak." Several of these D. mauritiana-D. sechellia introgression lines possess interspecific 111 6 variation in male PL morphology including transgressive variation in PL size, whereas others 112 possess morphology that is similar to D. sechellia w...

Reproductive isolation via divergent genital morphology due to cascade reinforcement inOhomopterusground beetles

“…For the past several decades, mechanical reproductive isolation has been repeatedly criticized owing to a lack of evidence (Shapiro & Porter, 1989) and research has largely focused on other mechanisms of reproductive isolation (Masly, 2012). Recently, however, evidence for mechanical reproductive isolation is growing (Anderson & Langerhans, 2015; Barnard et al, 2017; Frazee et al, 2021; Kamimura & Mitsumoto, 2012; Kubota et al, 2013; Mikkola, 2008; Nagata et al, 2007; Richmond, 2014; Sota & Kubota, 1998; Sota & Tanabe, 2010; Takami et al, 2007; Tanabe & Sota, 2008; Tanaka et al, 2018; Wojcieszek & Simmons, 2013).…”

“…Recently, however, evidence for mechanical reproductive isolation is growing (Anderson & Langerhans, 2015;Barnard et al, 2017;Frazee et al, 2021;Kamimura & Mitsumoto, 2012;Kubota et al, 2013;Mikkola, 2008;Nagata et al, 2007;Richmond, 2014;Sota & Tanabe, 2010;Tanabe & Sota, 2008;Tanaka et al, 2018;Wojcieszek & Simmons, 2013).…”