The Genomic Architecture and Evolutionary Fates of Supergenes

Abstract

Supergenes are genomic regions containing sets of tightly linked loci that control multi-trait phenotypic polymorphisms under balancing selection. Recent advances in genomics have uncovered significant variation in both the genomic architecture as well as the mode of origin of supergenes across diverse organismal systems. Although the role of genomic architecture for the origin of supergenes has been much discussed, differences in the genomic architecture also subsequently affect the evolutionary trajectory of supergenes and the rate of degeneration of supergene haplotypes. In this review, we synthesize recent genomic work and historical models of supergene evolution, highlighting how the genomic architecture of supergenes affects their evolutionary fate. We discuss how recent findings on classic supergenes involved in governing ant colony social form, mimicry in butterflies, and heterostyly in flowering plants relate to theoretical expectations. Furthermore, we use forward simulations to demonstrate that differences in genomic architecture affect the degeneration of supergenes. Finally, we discuss implications of the evolution of supergene haplotypes for the long-term fate of balanced polymorphisms governed by supergenes.

A supergene in seaweed flies modulates male traits and female perception

“…genomic regions harboring linked combinations of alleles from recombination [2, 4, 5]. Yet the persistence of supergene polymorphism over long time scales is puzzling especially given that supergene haplotypes often degrade [e.g., accumulate deleterious mutations; 6, 7–9]. While several mechanisms of balancing selection have been identified in classic supergene polymorphisms one form, disassortative mating (when individuals preferentially mate with dissimilar phenotypes) appears to be quite prevalent [7].…”

“…Yet the persistence of supergene polymorphism over long time scales is puzzling especially given that supergene haplotypes often degrade [e.g., accumulate deleterious mutations; 6, 7–9]. While several mechanisms of balancing selection have been identified in classic supergene polymorphisms one form, disassortative mating (when individuals preferentially mate with dissimilar phenotypes) appears to be quite prevalent [7]. Disassortative mating, occurs in many classic supergene systems [10–14] and is adaptive in degraded supergenes because deleterious mutations are generally private to their supergene haplotype, generating a heterozygote advantage [3, 6, 15, 16].…”

Tempo of degeneration across independently evolved non-recombining regions

“…Despite these long-term advantages of recombination, local recombination suppression can be selected for, maintaining beneficial allelic combinations, and leading to a genetic structure known as a supergene, where multiple genes are linked together and are transmitted as a single locus [7,8]. Examples of complex phenotypes controlled by supergenes include wing patterns in the Heliconius butterflies [9,10], social systems in ants [11] and mating compatibility systems, such as sex chromosomes or mating-type loci [12][13][14][15].…”

“…Examples of complex phenotypes controlled by supergenes include wing patterns in the Heliconius butterflies [9,10], social systems in ants [11] and mating compatibility systems, such as sex chromosomes or mating-type loci [12][13][14][15]. The suppression of recombination can thus arise and be maintained by selection, but the corresponding genomic regions then accumulate deleterious mutations through interferences between loci and Muller's ratchet [7,[16][17][18][19]. Typical deleterious mutations include non-synonymous substitutions [20][21][22][23][24][25] which alters the amino-acid sequences of a protein and may result in protein dysfunction.…”

Highlight: The Evolutionary Fates of Supergenes Unmasked

“…Now, however, thanks to advances in genomic sequencing and computational biology, scientists can put those theories to the test with real-world data. In a recent review published in Genome Biology and Evolution titled “ The genomic architecture and evolutionary fates of supergenes, ” Associate Professor Tanja Slotte and her colleagues at Stockholm University in Sweden discuss new findings in the field of supergene evolution and reveal how the genomic architecture of a supergene is inextricably tied to its evolutionary fate ( Gutiérrez-Valencia et al 2021 ).…”