Genomic architecture of supergenes: connecting form and function

Abstract

Supergenes are tightly linked sets of loci that are inherited together and control complex phenotypes. While classical supergenes—governing traits such as wing patterns in Heliconius butterflies or heterostyly in Primula —have been studied since the Modern Synthesis, we still understand very little about how they evolve and persist in nature. The genetic architecture of supergenes is a critical factor affecting their evolutionary fate, as it can change key parameters such as recombination rate and effective population size, potentially redirecting molecular evolution of the supergene in addition to the surrounding genomic region. To understand supergene evolution, we must link genomic architecture with evolutionary patterns and processes. This is now becoming possible with recent advances in sequencing technology and powerful forward computer simulations. The present theme issue brings together theoretical and empirical papers, as well as opinion and synthesis papers, which showcase the architectural diversity of supergenes and connect this to critical processes in supergene evolution, such as polymorphism maintenance and mutation accumulation. Here, we summarize those insights to highlight new ideas and methods that illuminate the path forward for the study of supergenes in nature. This article is part of the theme issue ‘Genomic architecture of supergenes: causes and evolutionary consequences’.

Stepwise recombination suppression around the mating-type locus in the fungusSchizothecium tetrasporum(Ascomycota, Sordariales)

“…The finding that the non-recombining regions in P. anserina, N. tetrasperma and S. tetrasporum contain a number of shared orthologous genes, particularly at the two edges of the non-recombining region, and that these regions display some level of synteny, raises the possibility of a third hypothesis: the selection of recombination suppression to maintain beneficial allelic combinations (55), as observed for supergenes in plants and animals (56,57). No function known to be directly related to mating compatibility was found among these orthologous genes, except for the mating-type locus, but several genes involved in sexual development in P. anserina are located in the non-recombining regions in both P. anserina (23) and S. tetrasporum (this study): ami1 , controlling nuclear migration events (44) and PaRID , a RID-like putative cytosine methyltransferase that controls sexual development (45).…”

Ecology, the pace‐of‐life, epistatic selection and the maintenance of genetic variation in life‐history genes

“…. Such clines are often ascribed to divergent directional selection in different parts of the cline, but are also consistent with balancing selection with environmental effects on equilibrium frequencies (Berdan et al, 2022). Here, density dependency and frequency dependency may be involved.…”

“…The results of a number of laboratory cage culture experiments in several species of Drosophila are at least consistent with NFDS, as inversions return to intermediate frequencies after perturbation (Alvarez‐Castro & Alvarez, 2005; Dobzhansky, 1992; Durmaz et al, 2020; Krimbas & Powell, 1992; Nassar et al, 1973; Tobari & Kojima, 1967). We note that the fact that recent efforts to understand the maintenance of inversion polymorphism has highlighted balancing selection (Berdan et al, 2022) is interesting in this regard, as inversions could represent unusually detectable and large effect variants that are symptomatic of underlying generally applicable evolutionary processes and amenable to study. Although much recent theory on inversions focuses on the accumulation of deleterious mutations and associative overdominance (e.g.…”

Stepwise recombination suppression around the mating-type locus in an ascomycete fungus with self-fertile spores

“…A third hypothesis to explain recombination suppression near the mating-type locus could be a neutral one, as proposed earlier [8,9], in which inversions or other recombination modifiers would be neutral in an initial stage at the margin of an already non-recombining region (the mating-type locus itself) and could fix by drift. A fourth hypothesis would be a selection of recombination suppression to maintain beneficial allelic combinations [73], as observed for supergenes in plants and animals [82,83]. Despite the finding of a number of shared orthologous genes in the non-recombining regions in P. anserina, N. tetrasperma and S. tetrasporum, our data did not bring support for the supergene hypothesis, as the overall synteny was not higher than in the rest of the genome and the gene functions were not related to mating-type antagonistic functions.…”