A supergene in seaweed flies modulates male traits and female perception

Abstract

Supergenes, tightly linked allelic combinations that underlie complex adaptive phenotypes represent a critical mechanism protecting intra-specific polymorphism. Supergenes represent some of the best examples of balancing selection in nature and there is increasing evidence that disassortative mating, when individuals preferentially mate with dissimilar phenotypes, is a key force stabilizing supergene polymorphisms. Yet, the underlying biological mechanisms and genetic basis of disassortative mating remain poorly known. Here, we examine a possible mechanism of disassortative mating driven by female mate choice in relation to the overdominant Cf-Inv(1) supergene in the seaweed fly Coelopa frigida by investigating chemical communication and its genomic architecture. We show that Cf-Inv(1) strongly affects chemical signaling; cuticular hydrocarbon (CHC) composition differed between genotypes in males but not females across two continents. In tandem, Cf-Inv(1) affected female perception of these compounds; females are able to sense 36 compounds from the male CHC cocktail but show differential perception between genotypes for almost half of them. This indicates that the genetic underpinnings of male traits and female perceptions are tightly linked within Cf-Inv(1) which likely facilitates disassortative mating. A differential expression approach based on candidate genes for CHC biosynthesis and odorant detection revealed differential expression for CHC biosynthesis in males alone but broad changes in odorant receptors across both sexes. Furthermore, odorant genes clustered together within Cf-Inv(1), with some of them differing between arrangements by 8.3% at the protein level, suggesting evolution via tandem duplication then divergence. We propose that the tight linkage between overdominant loci, male traits, and female perception has helped to maintain the Cf-Inv(1) polymorphism across its range in the face of supergene degeneration.

A large chromosomal inversion shapes gene expression in seaweed flies (Coelopa frigida)

“…This sexual conflict over mating rates has selected for sexual dimorphism in some of the external phenotypic traits used for mating, notably size and cuticular hydrocarbon composition (Enge et al. 2021 ). Larger males (usually αα) are more successful in obtaining copulations and resisting the rejection responses that females use to prevent male mountings.…”

“… 2020b ), and the composition of cuticular hydrocarbons (Enge et al. 2021 ). It was thus no surprise that males showed a larger gene expression difference between karyotypes compared to females.…”

Radiation and hybridization underpin the spread of the fire ant social supergene

“…The best-known example is the Batesian mimicry supergene identified in the butterfly Heliconius numata , in which various combinations of the three inversions yield different wing-color patterns ( 6 , 46 ). On the other hand, gradually formed supergene systems in which intermediate states are absent in natural populations are common, such as the supergene controlling mate choice in the seaweed fly, Coelopa frigida , which comprises three overlapping inversions ( 47 ). The supergene in the white-throated sparrow, Zonotrichia albicollis , regulates alternative mating syndromes and is composed of at least two nested pericentric inversions ( 48 ), while the social supergene in the socially polymorphic ant Formica selysi is formed by at least four successive inversions ( 49 ).…”