A masculinizing supergene underlies an exaggerated male reproductive morph in a spider

In many species, individuals can develop into strikingly different morphs, which are determined by a simple Mendelian locus. How selection shapes loci that control complex phenotypic differences remains poorly understood. In the spider Oedothorax gibbosus, males develop either into a ‘hunched’ morph with conspicuous head structures or as a fast-developing ‘flat’ morph with a female-like appearance. We show that the hunched-determining allele contains a unique genomic fragment of approximately 3 megabases that is absent in the flat-determining allele. This fragment comprises dozens of genes that duplicated from genes found at the same as well as different chromosomes. All functional duplicates, including a duplicate of the key sexual differentiation regulatory gene doublesex, show male-specific expression, which illustrates their integrated role as a masculinizing supergene. Our findings demonstrate how extensive indel polymorphisms and duplications of regulatory genes may contribute to the evolution of co-adapted gene clusters, sex-limited reproductive morphs and the enigmatic evolution of exaggerated sexual traits in general.