Environmental heterogeneity generates opposite gene-by-environment interactions for two fitness-related traits within a population

Abstract

Theory predicts that environmental heterogeneity offers a potential solution to the maintenance of genetic variation within populations, but empirical evidence remains sparse. The live-bearing fish Xiphophorus variatus exhibits polymorphism at a single locus, with different alleles resulting in up to five distinct melanistic "tailspot" patterns within populations. We investigated the effects of heterogeneity in two ubiquitous environmental variables (temperature and food availability) on two fitness-related traits (upper thermal limits and body condition) in two different tailspot types (wild-type and upper cut crescent). We found gene-by-environment (G × E) interactions between tailspot type and food level affecting upper thermal limits (UTL), as well as between tailspot type and thermal environment affecting body condition. Exploring mechanistic bases underlying these G × E patterns, we found no differences between tailspot types in hsp70 gene expression despite significant overall increases in expression under both thermal and food stress. Similarly, there was no difference in routine metabolic rates between the tailspot types. The reversal of relative performance of the two tailspot types under different environmental conditions revealed a mechanism by which environmental heterogeneity can balance polymorphism within populations through selection on different fitness-related traits.

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

“…; Fisher and Rosenthal ) or be better able to withstand bouts of food limitation (Culumber et al. ) or parasitic infection (Van Oosterhout et al. ) when they are rare in the population, which could translate to greater lifetime fitness (Ryan et al.…”

“…; Froese ; Culumber et al. ). This approach to analyzing body condition generally has been advocated over using residuals from a regression of mass and length as a dependent variable (Froese ), in part to avoid biases that can arise if other independent variables (e.g., time in experiment) are correlated with length.…”

“…; Culumber et al. ; Gulisija and Kim ; Culumber and Tobler ), there is little understanding of how variation in the social environment—and particularly the genetic composition of the social environment—can influence the maintenance of variation (Saltz and Nuzhdin ). Phenotypic differences caused by genetic variation in the social environment are generally termed "indirect genetic effects" (IGEs: Moore et al.…”

Correlated evolution of thermal niches and functional physiology in tropical freshwater fishes

“…The protocol used for quantifying thermal tolerances has been described in previous studies of Xiphophorus fishes (Culumber et al ., , , ) and followed institutionally approved procedures. A 7.5‐L aluminium chamber (22 cm diameter × 20 cm height) was filled with 4 L of aged tap water at the same temperature at which fish were maintained in the laboratory.…”

Variation in the evolutionary integration of melanism with behavioral and physiological traits in Xiphophorus variatus

“…S1). X. variatus is also polymorphic for melanistic tailspot patterns, caused by different alleles at a single locus, which are known to differ in response to environmental stressors such as temperature and resource limitation Culumber et al 2015). The tailspot polymorphism appears to be maintained in large part by heterogeneity in environmental variables Culumber and Tobler accepted) with little influence of sexual selection (Culumber and Rosenthal 2013;.…”