Adaptive, but not condition‐dependent, body shape differences contribute to assortative mating preferences during ecological speciation

Abstract

Assortative mating is critical for reproductive isolation during speciation; however, the mechanisms underlying mating preferences are often unknown. Assortative mating can be mediated through preferences for condition-dependent and adaptive ("magic") traits, but rigorously testing these hypotheses has been impeded by trait covariation in living organisms. We used computer-generated models to examine the role of body shape in producing association preferences between fish populations undergoing ecological speciation in different habitat types. We demonstrate that body shape can serve as an adaptive trait (variation in head size between populations) and a condition-dependent signal (variation in abdominal distention among individuals). Female preferences for stimuli varying in only one aspect of body shape uncovered evidence for body shape as a magic trait across population pairs, but no evidence for body shape serving as a condition-dependent signal. Evolution of preferences only in females from one habitat type as well as stronger preferences in sympatric nonsulfidic as opposed to allopatric nonsulfidic populations suggests that reinforcement may have played a role in producing the observed patterns.

Extreme environments and the origins of biodiversity: Adaptation and speciation in sulphide spring fishes

“…“Magic trait” mechanisms, where mating preferences evolve as a by‐product of divergent selection on ecological traits that serve as cues, have recently garnered much attention (Servedio, van Doorn, Kopp, Frame, & Nosil, ). Consistent with magic trait mechanisms, assortative mating in P. mexicana appears to be linked to adaptive population differences in body shape, which serve as cues to distinguish potential mating partners from different habitats (Greenway, Drexler, Arias‐Rodriguez, & Tobler, ). However, neither sulphide spring fish (which are unlikely to encounter migrants from nonsulphidic habitats due to H 2 S toxicity) nor allopatric P. mexicana from nonsulphidic waters (which have never experienced migrants from sulphide spring populations) exhibit a preference for mating partners from their own ecotype, suggesting that assortative mating in this system is a product of reinforcement (i.e., direct selection for assortative mating; Greenway et al., ).…”

Correlated divergence of female and male genitalia in replicated lineages with ongoing ecological speciation

“…), which are linked to adaptive differences in body shape that serve as cues (Greenway et al. ). Importantly, neither sulfidic females nor females from nonsulfidic 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.…”

“…Importantly, neither sulfidic females nor females from nonsulfidic 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. ). 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.…”

“…Reproductive isolation between populations in different habitat types is in part facilitated by natural selection against migrants, as reciprocal translocation experiments revealed strong selection against migrants from nonsulfidic habitats into sulfide springs, as well as varying levels of selection against sulfidic individuals moving into nonsulfidic habitats . Additionally, mate choice experiments have revealed significant association preferences for individuals of the same ecotype in nonsulfidic females from populations adjacent to sulfide springs , which are linked to adaptive differences in body shape that serve as cues (Greenway et al 2016). Importantly, neither sulfidic females nor females from nonsulfidic 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).…”

“…Additionally, mate choice experiments have revealed significant association preferences for individuals of the same ecotype in nonsulfidic females from populations adjacent to sulfide springs , which are linked to adaptive differences in body shape that serve as cues (Greenway et al 2016). Importantly, neither sulfidic females nor females from nonsulfidic 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 , indicating that other reproductive isolating barriers, such as genital incompatibilities, likely contribute to the strong reproductive isolation observed between populations (Bierbach et al 2017).…”