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Curr Biol. 2016 Feb 8;26(3):344-50. doi: 10.1016/j.cub.2015.11.069. Epub 2016 Jan 21.

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

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Department of Biology and The Center for Genomic Advocacy, Indiana State University, 600 Chestnut Street, Terre Haute, IN 47809, USA. Electronic address:
Department of Biology, Stanford University, 371 Serra Mall, Stanford, CA 94305-5020, USA.
Department of Biology and The Center for Genomic Advocacy, Indiana State University, 600 Chestnut Street, Terre Haute, IN 47809, USA.
Department of Biology, East Carolina University, Howell Science Complex, Greenville, NC 27858, USA.
McDonnell Genome Institute, Washington University School of Medicine, 4444 Forest Park Avenue, Campus Box 8501, St. Louis, MO 63108, USA.
Department of Animal Biology, School of Integrative Biology, University of Illinois, Urbana-Champaign, IL 61801, USA.


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.

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