Supergenes are not necessary to explain the maintenance of complex alternative phenotypes.

Abstract

Evolutionary biology aims to explain the diversity seen in nature. Evolutionary theory provides frameworks to understand how simple polymorphisms or continuous variation are maintained, but phenotypes inherited as discrete suites of quantitative traits are difficult to fit into this framework. Supergenes have been proposed as a solution to this problem-if causal genes are co-located, they can be inherited as if a single gene, thus bridging the gap between simple polymorphisms and continuous traits. We develop models to ask: how are critical supergenes for maintaining phenotypic diversity? In our simplest model, without explicit genetic architectures, three alternative reproductive morphs are maintained in many of the parameter combinations we evaluated. For these same parameter values, models with demographic stochasticity, recombination and mutation (but without explicit genetic architecture) maintained only two of these three morphs, with stochasticity determining which morphs persisted. With explicit genetic architectures, regardless of whether causal loci were co-located in a supergene or distributed randomly, this stochasticity in which morphs are maintained was reduced. Even when phenotypic variation was lost, genetic diversity was maintained. Altogether, categorical traits with polygenic bases exhibited similar evolutionary dynamics to those determined by supergenes. Our work suggests that supergenes are not the only answer to the puzzle of how discrete polygenic phenotypic variation is maintained.