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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.

SUBMITTER: Tuttle EM

PROVIDER: S-EPMC4747794 | biostudies-literature | 2016 Feb

REPOSITORIES: biostudies-literature

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Divergence and Functional Degradation of a Sex Chromosome-like Supergene.

Tuttle Elaina M EM Bergland Alan O AO Korody Marisa L ML Brewer Michael S MS Newhouse Daniel J DJ Minx Patrick P Stager Maria M Betuel Adam A Cheviron Zachary A ZA Warren Wesley C WC Gonser Rusty A RA Balakrishnan Christopher N CN

Current biology : CB 20160121 3

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 ...[more]

PMID: 26804558

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Project description:BackgroundThe discovery of differentially organized sex chromosome systems suggests that heteromorphic sex chromosomes evolved from a pair of homologous chromosomes. Whereas karyotypes are highly conserved in alethinophidian snakes, the degeneration status of the W chromosomes varies among species. The Z and W chromosomes are morphologically homomorphic in henophidian species, whereas in snakes belonging to caenophidian families the W chromosomes are highly degenerated. Snakes therefore are excellent animal models in which to study sex chromosome evolution. Herein, we investigated the differentiation processes for snake sex chromosomes using both coding and repetitive sequences. We analyzed phylogenetic relationships of CTNNB1 and WAC genes, localized to the centromeric and telomeric regions, respectively, of the long arms on snake sex chromosomes, and chromosome distribution of sex chromosome-linked repetitive sequences in several henophidian and caenophidian species.ResultsPartial or full-length coding sequences of CTNNB1 and WAC were identified for Z homologs of henophidian species from Tropidophiidae, Boidae, Cylindrophiidae, Xenopeltidae, and Pythonidae, and for Z and W homologs of caenophidian species from Acrochordidae, Viperidae, Elapidae, and Colubridae. Female-specific sequences for the two genes were not found in the henophidian (boid and pythonid) species examined. Phylogenetic trees constructed using each gene showed that the Z and W homologs of the caenophidian species cluster separately. The repetitive sequence isolated from the W chromosome heterochromatin of the colubrid Elaphe quadrivirgata and a microsatellite motif (AGAT)8 were strongly hybridized with W chromosomes of the viperid and colubrid species examined.ConclusionOur phylogenetic analyses suggest that the cessation of recombination between the Z and W homologs of CTNNB1 and WAC predated the diversification of the caenophidian families. As the repetitive sequences on the W chromosomes were shared among viperid and colubrid species, heterochromatinization of the proto-W chromosome appears to have occurred before the splitting of these two groups. These results collectively suggest that differentiation of the proto-Z and proto-W chromosomes extended to wide regions on the sex chromosomes in the common ancestor of caenophidian families during a relatively short period.

Dataset Information

Divergence and Functional Degradation of a Sex Chromosome-like Supergene.

Publications

Divergence and Functional Degradation of a Sex Chromosome-like Supergene.

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