Divergence and Functional Degradation of a Sex Chromosome-like Supergene

Abstract

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 >100-Mb 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 phylogenomic data to show that alternate supergene alleles are highly divergent at over 1,000 genes and 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/W sex 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.

Figure 1. White-throated Sparrows comprise two morphs with an ancient origin

(A) Tan (T) and white (W) morph sparrows (Note differences in plumage color in the head stripe and throat) differ in chromosome 2 (sometimes referred to as ZAL2) genotype and mate almost exclusively with the opposite morph, maintaining polymorphism in the species. (B) Tan (2) and white (2^m) chromosomes are highly divergent within the inverted portion of chromosome, suggesting an ancient origin of the chromosomes 2 and 2^m. All nodes are supported by 100% bootstrap values and the depicted topology for the inverted region is a significantly better fit to the data than trees constrained to the monophyly of 2 and 2^m (p < 0.001, see Supplementary Materials). Taxa marked with an asterisk are those for which whole genomes were sequenced. The arrows highlights the ancestral node for the Zonotrichia genus. See also Table S2.

Figure 2. Contrasting divergence, diversity and linkage disequilibrium inside (pink area) and outside the inverted region

Sliding window estimate across FISH-mapped scaffolds of (A) F_ST between white and tan birds and (B) genetic diversity along the tan allele, 2. The grey bar represents the 95% confidence band (standard deviation) of neutral expectation for genetic diversity . (C) Linkage disequilibrium decays rapidly outside of the inversion, but is high, especially in 2/2^m heterozygotes, within the inversion. Using golden-crowned or Harris’ sparrow as outgroups, (D) Fay and Wu’s H estimates do not show a strong signal of recent selective sweeps in the inverted region of chromosome 2. See also Figures S1, S3 and Table S3.

Figure 3. Functional degradation of 2^m

(A) Using two different outgroups (diamond = golden-crowned sparrow, circle = Harris’ sparrow), the direction of selection statistic is strongly negative on 2^m, indicating an increased level of non-sysnonymous polymorphism. (B) For genes within the inversion, gene expression in higher for tan birds than heterozygous (2/2^m) white-morph birds and (C) in white birds, the white (2^m) allele tends to be under-expressed relative to the tan (2) allele (**: p < 0.01; ***: p < 0.001). Error bars represent 95% confidence intervals (standard error). See also Figure S2, S4, and Table S1.