Asymmetric reinforcement inLucaniakillifish: assessing reproductive isolation when both sexes choose

Abstract

Reinforcement can occur when maladaptive hybridization in sympatry favors the evolution of conspecific preferences and target traits that promote behavioral isolation. In many systems, enhanced behavioral isolation is due to increased female preference for conspecifics. In others, behavioral isolation is driven by male preference, and in other systems both sexes exert preferences. Some of these patterns can be attributed to classic sex-specific costs and benefits of preference. Alternatively, sex differences in conspecific preference can emerge due to asymmetric post-zygotic isolation (e.g., hybrid offspring from female A × male B have lower fitness than hybrid offspring from female B × male A), which can lead to asymmetric behavioral isolation (e.g., female A and male B are less likely to mate than female B and male A). Understanding reinforcement requires understanding how conspecific preferences evolve in sympatry. Yet, estimating conspecific preferences can be difficult when both sexes are choosy. In this study, we use Lucania killifish to test the hypothesis that patterns of reinforcement are driven by asymmetric post-zygotic isolation between species. If true, we predicted that sympatric female L. goodei and sympatric male L. parva should have lower levels of behavioral isolation compared to their sympatric counterparts, as they produce hybrid offspring with the highest fitness. To address the problem of measuring behavioral isolation when both sexes are choosy, we inferred the contribution to behavioral isolation of each partner using assays where one sex in the mating pair comes from an allopatric population with potentially low preference, while the other comes from a sympatric population with high preference. For one hybrid cross direction, we found that both female L. parva and male L. goodei have high contributions to behavioral isolation in sympatry. In the other hybrid cross direction, we found that only female L. goodei contribute to behavioral isolation. Sympatric male L. parva readily engaged in hybrid spawnings with allopatric L. goodei females. These results indicate that both asymmetric post-zygotic isolation and the traditional sex-specific costs to preference likely affect the nature of selection on conspecific preferences and target traits.

Reproductive isolating mechanisms contributing to asymmetric hybridization in Killifishes (Fundulus spp.)

“…The occurrence of multiple asymmetric pre‐ and post‐zygotic asymmetries suggests that a variety of genetic mechanisms, including unidirectional Bateson–Dobzhansky–Muller incompatibilities, contribute to this bias. As well, concordance among pre‐ and post‐mating barriers is consistent with the role of reinforcement in the evolution of female preference (Yukilevich, 2012), a prediction that must be further tested (e.g., St John & Fuller, 2021). While hybridization was generally detrimental for female F. heteroclitus , female F. diaphanus offspring had a higher hatching success when sired by F. heteroclitus males at 10 ppt, which could further contribute to the relative prevalence of D♀ × H♂ F1 hybrid lineages.…”

“…Alternatively, our finding that F. diaphanus , and not F. heteroclitus , act most aggressively towards competitors when in the presence of F. diaphanus females suggests that male–male aggression does not contribute to the hybrid bias in the wild, in contrast to findings for other cyprinodontiform fishes (e.g., Berdan & Fuller, 2012; Polacik & Reichard, 2011). Studies in L. parva and L. goodei find that male–male aggression is associated with preference (e.g., Berdan & Fuller, 2012), and male mating preference is an important, and asymmetrical, behavioural isolating mechanism between other species of killifishes (e.g., L. goodei and L. parva ; Berdan & Fuller, 2012; Gregorio et al, 2012; St John & Fuller, 2021). Our finding that F. diaphanus males were more aggressive towards a competitor when in the presence of conspecific females leads us to predict that there could be male preference in this species.…”

“…A pattern of concordance among asymmetric pre‐ and post‐zygotic reproductive isolating mechanisms is consistent with the role of reinforcement (e.g., Yukilevich, 2012), a situation in which the production of low‐fitness hybrids favours the evolution of pre‐zygotic barriers in sympatry (reviewed by Servedio & Noor, 2003). Indeed, asymmetric male preferences between L. parva and L. goodei , two other Fundulids, has been found to evolve due to reinforcement (Berdan & Fuller, 2012; Fuller et al, 2007; Gregorio et al, 2012; St John & Fuller, 2021). In this study, we found concordant asymmetries in pre‐mating (female preference) and post‐mating barriers (fertilization, hatching success at 10 ppt) that match the hybridization bias found in the wild.…”

The role of ecology and geography in the evolution of habitat isolation and sexual isolation among sister species of host-plant-specific insects

“…This species-pair metric ranges from 0 to 1, with 0 indicating similar habitat preferences and no habitat isolation and 1 indicating divergent habitat preferences and complete habitat isolation between species. For the purposes of statistical analysis, we obtained 10,000 bootstrap values of this metric of habitat isolation for each of the three species pairs, B. kinseyi × B. treatae , B. kinseyi × B. fossoria , and B. treatae × B. fossoria , by randomly resampling individual host preference values from the original data and recalculating habitat isolation (John and Fuller 2021). Bootstrap values of habitat isolation for the three heterospecific species pairs were then compared via t-tests.…”

Testing the predictions of reinforcement: long-term empirical data from a damselfly mosaic hybrid zone

“…Yukilevich 2012;Zhou and Fuller 2014;Ostevik et al 2021;St. John and Fuller 2021) is an important growing field in evolutionary biology, our study opens the possibility of testing the interaction between these processes in other taxa.…”