Multiple forms of balancing selection maintain inversion polymorphism

Abstract

Despite many examples of balanced inversion polymorphisms, little is known about how they affect fitness-related traits. This knowledge gap hampers our understanding of how they are selectively maintained as protected polymorphisms. Here, we study the effects of a cosmopolitan balanced inversion polymorphism in D. melanogaster, In(3R)Payne, on fitness components, including traits related to development, growth, reproduction, stress resistance, and adult survival. We find that the non-inverted standard (STD) chromosomal arrangement and the inverted (INV) arrangement behave like Mendelian alleles of a supergene, which affect a suite of complex fitness-related phenotypes. While the STD arrangement tends to have positive, mostly dominant effects on size-related traits, fecundity, fertility, stress resistance, and lifespan, the INV arrangement exhibits mostly recessive effects that are indicative of fitness costs. Yet, in favor of the balanced polymorphism, we observe overdominance for egg hatchability, egg-to-adult survival, pupal survival at 18 °C, developmental time, and male desiccation resistance. The most parsimonious explanation for these heterotic effects is that they are due to some form of multi-locus heterokaryotype advantage. We also find several instances of trait-, sex-, and temperature-dependent changes in the degree of dominance, suggesting a possible role of antagonistic selection with context-specific dominance reversals in maintaining the polymorphism. Moreover, genotype-by-environment interactions and parental effects appear to contribute as well. Together, our results suggest that multiple phenotypic modes of balancing selection are involved in maintaining the inversion polymorphism.