Admixture can readily lead to the formation of supergenes

Abstract

Supergenes are genetic architectures allowing the segregation of alternative combinations of alleles underlying complex phenotypes. The co-segregation of sets of alleles at linked loci is determined by polymorphic chromosomal rearrangements suppressing recombination locally. Supergenes are involved in many complex polymorphisms, including sexual, color or behavioral polymorphisms in numerous plants, fungi, mammals, fish, and insects. Despite a long history of empirical and theoretical research, the genetic origin of supergenes remains poorly understood. Here, using a population genetic two-island model, we explore how the evolution of overdominant chromosomal inversions may lead to the formation of supergenes. We show that the evolution of inversions in differentiated populations connected by gene flow leads to an increase in frequency of poorly adapted, immigrant haplotypes. When inversions are associated with recessive fitness cost hampering their fixation (such as a mutational load), this results in the formation of supergenes. These results provide a realistic scenario for the evolution of supergenes and inversion polymorphisms in general, and bring new light into the importance of admixture in the formation of new genetic architectures.