GxG epistasis in growth and condition and the maintenance of genetic polymorphism inGambusia holbrooki

Abstract

Theory on indirect genetic effects (IGEs) indicates that variation in the genetic composition of social groups can generate GxG epistasis that may promote the evolution of stable polymorphisms. Using a livebearing fish with a genetic polymorphism in coloration and associated behavioral differences, we tested whether genotypes of social partners interacted with focal individual genotypes to influence growth and condition over 16 weeks of development. We found that IGEs had a significant influence on patterns of feeding, regardless of focal fish genotype. There was no influence of social environment on juvenile length, but there was significant GxG epistasis for body condition. Each focal juvenile was in better condition when its own genotype was not present in adult social partners. These data are consistent with negative frequency-dependent selection in which each morph performs better when it is rare. Neither variation in feeding nor activity-related behaviors explained variation in body condition, suggesting that GxG epistasis for condition was caused by physiological differences between the two genotypes. These findings indicate that GxG epistasis in a given polymorphism can generate fitness landscapes that contribute to the maintenance of that polymorphism and to maintenance of genetic variation for additional fitness-related traits.

The Biology of Polymorphic Melanic Side-Spotting Patterns in Poeciliid Fishes

“…However, this trend cannot be generalized to every population, as temperature-sensitive siblings of the same genotype but different phenotype were the same size (Horth, 2003), or to every species, since X. helleri morphs did not differ in body mass (Meyer et al, 2006). Although feeding behavior does not differ between morph juveniles in G. holbrooki (Culumber et al, 2018), other correlated physiological (e.g., growth rate) or behavioral (e.g., food competition) traits could still underlie the increased size of spotted males (Martin, 1977;Culumber et al, 2018), while also explaining why this size difference is not a general trait across populations and species. Further research into morph trade-offs among life history traits is required.…”

“…For example, different frequencies of spotted and unspotted morphs alter the social environment, as the likelihood of encountering and interacting with each morph will also be different. Juvenile body condition in G. holbrooki was better when individuals were raised with a preponderance of the opposite morph, which indicates negative frequency-dependent selection (Culumber et al, 2018). Unspotted juveniles were affected to a greater degree, so morphs do seem to have underlying genetic or physiological differences that shape this trait (Culumber et al, 2018).…”

“…Xiphophorus males with heavier pigmentation often have reduced survival (Koßwig, 1927;Mac Intyre, 1961), which could reflect a fitness disadvantage that drives down the frequency of spotted morphs. In G. holbrooki, spotted males are larger than unspotted males, which could give spotted males a dominance or mating advantage that contributes to the maintenance of this polymorphism (Martin, 1977;Horth et al, 2010;Culumber et al, 2018). However, this trend cannot be generalized to every population, as temperature-sensitive siblings of the same genotype but different phenotype were the same size (Horth, 2003), or to every species, since X. helleri morphs did not differ in body mass (Meyer et al, 2006).…”

“…Juvenile body condition in G. holbrooki was better when individuals were raised with a preponderance of the opposite morph, which indicates negative frequency-dependent selection (Culumber et al, 2018). Unspotted juveniles were affected to a greater degree, so morphs do seem to have underlying genetic or physiological differences that shape this trait (Culumber et al, 2018). Survival rates also differed based on the frequency of the spotted morph in G. holbrooki (Horth and Travis, 2002).…”

“…Altered behavior in the presence of spotted males is hypothesized to drive this lower survival (Horth and Travis, 2002). For example, juvenile feeding was lower in the presence of spotted males compared to unspotted males (Culumber et al, 2018). The effect of other social environmental factors like density or sex ratio and of physical environmental factors on morph life history traits remains to be investigated across species.…”