View Program - 2022 Population, Evolutionary, and Quantitative Genetics Conference

Inversion polymorphisms are well documented across many taxa, despite the potential generation of unfit, unbalanced gametes from inversion heterozygotes. Inversions may fix as a result of linkage with beneficial alleles or due to drift, but many inversions are maintained at intermediate, in some cases clearly balanced frequencies, potentially by linking alleles that share conditional benefit. In African Drosophila melanogaster, paracentric inversions are common and many inversions are stably polymorphic throughout diverse African lowland habitats, suggesting the involvement of evolutionary forces beyond local adaptation. We hypothesize that balanced sexually antagonistic selection may be responsible for maintaining the stable polymorphism, in line with the active competition among D. melanogaster males and the potential for sexual antagonism. We used a novel forward population simulator with parameters based on D. melanogaster life history to model inversion evolution in a population under sexually antagonistic selection at infinite loci and with male reproductive skew. Simulations demonstrated (1) balanced polymorphism involving alleles with a range of antagonistic effects, (2) the persistence of such polymorphic alleles at many loci only under linkage due to competitive effects, and (3) the rise in frequency and stable persistence of inversions that establish such linkage associations between sets of sexually antagonistic alleles. We followed with an empirical exploration of the selection dynamics on inversions between a pooled Zambian paternal population and their embryo and aged adult offspring to detect correlations between the inversion status, viability and mating fitness. Results demonstrated non-neutral frequency changes, consistent with a complex fitness landscape in which only Inversion 3RK demonstrated a consistent tradeoff between male reproductive success and viability-longevity under the conditions and frequencies tested. This establishes the potential presence of this modeled dynamic in D. melanogaster inversions. This model has implications for sex chromosome evolution, as a segregating autosomal antagonistic haplotype would benefit from linkage to a sex determining locus. Further, balancing selection upon epistatic haplotypes, particularly due to sexual or ecological antagonistic selection, may contribute significantly to genetic diversity and ongoing evolution and local adaptation in natural populations.

Balanced Inversions help maintain sexually antagonistic polymorphism