Divergence and Functional Degradation of a Sex Chromosome-like Supergene

Abstract

SUMMARY A major challenge in biology is to understand the genetic basis of adaptation. One compelling idea is that groups of tightly linked genes (i.e. ‘supergenes’ [1, 2]) facilitate adaptation in suites of traits that determine fitness. Despite their likely importance, little is known about how alternate supergene alleles arise and become differentiated, nor their ultimate fate within species. Herein we address these questions by investigating the evolutionary history of a supergene in white-throated sparrows, Zonotrichia albicollis. This species comprises two morphs, tan and white, that differ in pigmentation and components of social behavior [3–5]. Morph is determined by alternative alleles at a balanced >100Mb inversion-based supergene, providing a unique system for studying gene-behavior relationships. Using over two decades of field data we document near-perfect disassortative mating among morphs, as well as the fitness consequences of rare assortative mating. We use de novo whole genome sequencing coupled with population- and phylo-genomic data, to show that alternate supergene alleles are highly divergent at over 1,000 genes, that these alleles originated prior to the split of Z. albicollis from its sister species, and may be polymorphic in Z. albicollis due to a past hybridization event. We provide evidence that the ‘white' allele may be degrading, similar to neo-Y/Wsex chromosomes. We further show that the ‘tan’ allele has surprisingly low levels of genetic diversity, yet does not show several canonical signatures of recurrent positive selection. We discuss these results in the context of the origin, molecular evolution, and possible fate of this remarkable polymorphism.

Polymorphism at a mimicry supergene maintained by opposing frequency-dependent selection pressures

“…Mimicry polymorphism in H. numata is controlled by a supergene characterized by distinct chromosomal inversions maintaining the different haplotypes underlying the various wing patterns (14). As documented in an increasing number of cases, inversions may be associated with deleterious effects, either through the disruption of gene regulation by the breakpoints or due to deleterious mutations present within the segment at the time of the inversion, causing reduced fitness in homozygotes (27,(38)(39)(40). By minimizing the frequency of homozygotes for the inversion in offspring, disassortative mating protects from the deleterious effects associated with the inversions.…”

“…Mate preference generally causes positive assortative mating between individuals with the same phenotype and may reinforce local monomorphism in the warning signal. However, sexual preferences may maintain color polymorphism through a preference for rare phenotypes (24) or from disassortative mating [i.e., between individuals of different phenotypes (25)(26)(27)], generating negative FDS (3). Indeed, under disassortative mating, individuals with a rarer phenotype enjoy increased reproductive success because a larger proportion of the population will prefer them.…”

Supergene evolution triggered by the introgression of a chromosomal inversion

“…Examples include floral heteromorphy determining alternative pollination strategies 10 , butterfly mimicry of alternative wing-pattern and behaviours of toxic models 3,11,12 , contrasting mating tactics in several birds 13,14 , and alternative social organization in ant colonies 4 . In most documented cases, the maintenance of character associations is mediated by polymorphic rearrangements, such as inversions, which suppress local recombination and allow the differentiated supergene alleles to persist 2,4,5,10,13 . However, the build-up of differentiated haplotypes from initially recombining loci is poorly understood 1,6 .…”

Gene Regulatory Evolution During Speciation in a Songbird

“…We also predicted that under strong drift, deleterious mutations would accumulate and impair normal levels of gene expression. Such patterns have been observed in situations where recombination is suppressed (e.g., neo sex chromosomes: Bachtrog 2006; "supergenes": Tuttle et al 2016). In this case, Timor zebra finch alleles would show a tendency to be underexpressed relative to the Australian allele in heterozygous hybrids.…”