Drosophila pseudoobscura third chromosome inversion arrangements have temperature-dependent and sex-specific effects on life history traits

Abstract

Chromosomal inversions can create polymorphic "supergenes" consisting of many alleles in linkage disequilibrium that affect constellations of traits. The coadaptation hypothesis supposes that many alleles within an inversion haplotype have synergistic epistatic interactions, which are maintained by suppressed recombination in inversion heterozygotes, heterozygote advantage, and context-dependent fitness effects. The fitness benefits of chromosomal inversions frequently arise from effects on life history syndromes, including ecotypes and reproductive strategies. Life history syndromes can also be caused by individual pleiotropic alleles in ways that resemble the effects of chromosomal inversions. It is therefore possible that the fitness effects of chromosomal inversions arise because of pleiotropic alleles and not coadaptation. These two hypotheses can be distinguished because pleiotropy predicts greater genetic correlations of traits than coadaptation. To test the coadaptation and pleiotropy hypotheses, we measured three life history traits (lifespan, development time, and body size) in Drosophila pseudoobscura with six different chromosomal inversion genotypes. We assayed males and females raised at multiple temperatures in order to expose phenotype variation. Temperature affected lifespan and development more than any other factor, but we also observed differences in mortality rates and development times that depended on chromosomal inversions and sex. Despite these context-dependent effects on life history traits, we failed to identify genetic correlations that would be evidence for pleiotropic alleles. Our results therefore suggest that the coadaptation hypothesis is better supported.