Hybridization and postzygotic isolation promote reinforcement of male mating preferences in a diverse group of fishes with traditional sex roles

Abstract

Behavioral isolation is thought to arise early in speciation due to differential sexual and/or natural selection favoring different preferences and traits in different lineages. Instead, behavioral isolation can arise due to reinforcement favoring traits and preferences that prevent maladaptive hybridization. In darters, female preference for male coloration has been hypothesized to drive speciation, because behavioral isolation evolves before F1 inviability. However, as with many long‐lived organisms, the fitness of second‐generation hybrids has not been assessed because raising animals to adulthood in the laboratory is challenging. Of late, reinforcement of male preferences has been implicated in darters because male preference for conspecific females is high in sympatry but absent in allopatry in multiple species pairs. The hypothesis that reinforcement accounts for behavioral isolation in sympatry assumes that hybridization and postzygotic isolation are present. Here, we used genomic and morphological data to demonstrate that hybridization is ongoing between orangethroat and rainbow darters and used hybrids collected from nature to measure postzygotic barriers across two hybrid generations. We observed sex ratio distortion in adult F1s and a dramatic reduction in backcross survival. Our findings indicate that selection to avoid hybridization promotes the evolution of male‐driven behavioral isolation via reinforcement in this system.

Demographic modelling helps track the rapid and recent divergence of a conifer species pair from Central Mexico

“…For instance, our results (Table 2, Figure 5a), and those of previous theoretical and empirical studies in these and other taxa, suggest that contrasting amounts of genetic load should be expected between species (Chen et al, 2017; Cruz‐Nicolás, Giles‐Pérez, Lira‐Noriega, et al, 2020; Ohta, 1992). Such a load would be more easily exposed in recombinant hybrids (i.e., F 2 , F 3 , … F n ) and backcrosses involving the parental species with the smallest N e (i.e., A. flinckii ) than in the opposite direction, which may result in reduced hybrid fitness (i.e., “hybrid load”; Moran et al, 2020; e.g., Christe et al, 2017; Fenster & Galloway, 2000; Hamilton et al, 2013; Moran et al, 2018), and explain the observed asymmetrical introgression from A. flinckii into A. religiosa (see also Pickup et al, 2019). Selection could also be favouring reproductive isolation to alleviate competition driven by interspecific pollen–style interactions (Rahmé et al, 2009; Rieseberg & Blackman, 2010).…”

“…Therefore, if self‐tolerance has evolved at contact zones, we expected less genetic diversity and both higher inbreeding and interspecific genetic differentiation ( F ST ) in sympatric than in allopatric populations (Hopkins, 2013 ; Wright et al, 2013 ). Opposite results would be expected if reproductive barriers are absent or are inefficient for countering interspecific mating (e.g., Garner et al, 2018 ; Moran et al, 2018 ). Note that these patterns should be readily observed with genetic markers randomly distributed across an extremely large genome (∼18 Gb; Mosca et al, 2019 ), as the likelihood of hitting genes associated with reproductive traits is very low; looking for and removing such genes was thus unnecessary.…”

“…Alternatively, interspecific gene flow may be selectively interrupted when hybrid offspring have lower fitness than parental taxa (Hopkins, 2013;Rahmé et al, 2009;Servedio & Noor, 2003) Hamilton et al, 2013;Moran et al, 2018), and explain the observed asymmetrical introgression from A. flinckii into A. religiosa (see also Pickup et al, 2019). Selection could also be favouring reproductive isolation to alleviate competition driven by interspecific pollen-style interactions (Rahmé et al, 2009;Rieseberg & Blackman, 2010).…”

Reinforcement in the banded darter Etheostoma zonale: The effect of sex and sympatry on preferences

“…In this same group, female preference for conspecific males was determined to be insignificant in both sympatric and allopatric populations (Moran & Fuller, ; Moran, Zhou, Catchen, & Fuller, ). Combined with an additional study showing maladaptive effects of hybridization in sympatric species pairs in this subgenus (Moran, Zhou, Catchen, & Fuller, ), their results suggest that selection is acting on male, but not female, mate choice in sympatric populations. Our results, which taken together suggest that female preferences are more strongly reinforced in sympatric populations, are therefore more consistent with results from Drosophila than with those of a congeneric species group.…”

Lacustrine speciation associated with chromosomal inversion in a lineage of riverine fishes

“…Even recently diverged darter species such as Percina freemanorum and P. kusha (diverged approximately 300,000 years ago) are allopatric and do not actively hybridize 68 . Geographic isolation is the main driver of darter diversification 19, 69 and most darter hybridization follows long periods divergence 70 . For example, hybridization between E. caereuleum and E. spectabile is well-characterized on a phenotypic and genomic level 53 , yet these species share most recent common ancestry 22 million years ago 19 .…”