Divergence of female & male genitalia can occur in early stages, not only at later stages of speciation (after the accumulation of other reproductive isolating barriers)

Correlated divergence of female and male genitalia in replicated lineages with ongoing ecological speciation. Ryan Greenway et al. Evolution, April 16 2019. https://doi.org/10.1111/evo.13742

ABSTRACT: Divergence of genital traits among lineages has the potential to serve as a reproductive isolating barrier when copulation, insemination, or fertilization are inhibited by incompatibilities between female and male genitalia. Despite widespread evidence for genital trait diversity among closely related lineages and coevolution of female and male genitalia within lineages, few studies have investigated genital evolution during the early stages of speciation. We quantified genital variation in replicated population pairs of Poecilia mexicana with ongoing ecological speciation between sulfidic (H2S‐containing) and nearby non‐sulfidic habitats. These analyses revealed rapid and correlated divergence of female and male genitalia across evolutionarily independent population pairs exposed to divergent selection regimes. Both sexes exhibited convergent evolution of genital traits among populations inhabiting similar habitat types. Our results demonstrate that genital evolution can occur during the early stages of speciation‐with‐gene‐flow, potentially as a result of variation in the intensity of sexual conflict among populations. Our results suggest genitalia may contribute to early stages of divergence, and challenge the generality of previously suggested mechanisms of genital evolution in poeciliids.

Keywords: convergence, genital evolution, reproductive  isolation, Poecilia mexicana, reinforcement, sexual isolation

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Divergence of genital traits has been hypothesized to serve as an effective reproductive isolating barrier when successful copulation, insemination, or fertilization are inhibited or prevented due to incompatibilities between the genitalia of males and females from different lineages [...]. Even though genitalia are among the most rapidly evolving morphological traits (Eberhard 1985), with concomitant implications for the evolution of reproductive isolation [...], the timing and role of mechanical isolation via genital divergence as a barrier to gene flow during speciation remains unclear (Langerhans et al. 2016; Yassin 2016). [...] Few studies have explicitly investigated patterns of genital evolution during early stages of the speciation process [...]. As a result, the question remains whether genital divergence can contribute to reproductive isolation early in the speciation process, or if genital divergence occurs only at later stages of speciation, after the accumulation of other reproductive isolating barriers (e.g., as a consequence of reinforcement upon secondary contact).

[...] Populations of P. mexicana have independently colonized toxic, hydrogen sulfide(H2S)-rich springs in multiple tributaries of the Río Grijalva in southern Mexico (Greenway et al.2014). Sulfide spring fishes are locally adapted and differ from ancestral populations in adjacent non-sulfidic habitats in physiological, morphological, behavioral, and life-history traits(Tobler et al. 2018). Trait divergence includes changes in sexual behaviors(less coercive mating attempts in sulfidic populations; Plath et al. 2003; Plath 2008)as well as aggression and boldness (both reduced in sulfidic populations; Riesch et al. 2009; Bierbach et al. 2017), which could influence genital evolution. Populationsin sulfidespringsare also genetically differentiated from neighboring populations in non-sulfidic habitats despite a lack of physical barriers(Plath et al. 2013). Reproductive isolation between populationsin different habitat typesis in part facilitated by natural selection against migrants, as reciprocal translocation experiments revealed strong selection against migrants from non-sulfidic habitats into sulfide springs, as well as varying levels of selection against sulfidic individuals moving into non-sulfidic habitats (Plath et al. 2013). Additionally, mate choice experiments have revealed significant association preferences for individuals of the same ecotype in non-sulfidic females from populations adjacent to sulfide springs (Plath et al. 2013), which arelinked to adaptive differences in body shape that serve as cues (Greenway et al. 2016). Importantly, neither sulfidic females nor femalesfrom non-sulfidic populations in river drainages lacking sulfide spring populations exhibit significant association preferences, suggesting that reinforcement (i.e.direct selection for assortative mating) may have shaped female association preferences (Greenway et al. 2016). However, the observed strengths of natural selection against immigrants and assortative mating preferences alone are not strong enough to explain the low observed levels of gene flow (Plath et al. 2013), indicating that other reproductive isolating barriers, such as genital incompatibilities, likely contribute to the strong reproductive isolation observed between populations (Bierbach et al. 2017).