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.
| Original language | English |
|---|---|
| Pages (from-to) | 344-350 |
| Number of pages | 7 |
| Journal | Current Biology |
| Volume | 26 |
| Issue number | 3 |
| DOIs | |
| State | Published - Feb 8 2016 |
Funding
Funding for this work was provided by NIH NIGMS grant 1R01GM084229 (E.M.T. and R.A.G.), Indiana State University (E.M.T. and R.A.G.), and East Carolina University (C.N.B.). A.O.B. was supported by an NIH National Research Service Award (F32 GM097837) and by NIH grant R01GM100366 to Dmitri Petrov and Paul Schmidt. All experimental procedures involving live animals were approved by the Indiana State University Institutional Animal Care and Use Committee (protocols 562158-1:ET/RG and 562192-1:ET/RG). We thank the production sequencing group of the McDonnell Genome Institute at Washington University for library construction, sequencing, and data curation for the white-throated sparrow genome. The University of Alaska Museum kindly provided the Z. atricapilla and Z. querula samples. Dr. Alvaro Hernandez and the High-Throughput Sequencing and Genotyping Unit at the University of Illinois performed library preparation and genome resequencing. Marlys Houck and Oliver Ryder at the Institute for Conservation Research at the San Diego Zoo provided assistance with cell culture and karyotyping, and Michael Romanov helped with BAC identification. We thank Teri Lear and Judy Lundquist from the Gluck Equine Research Center at the University of Kentucky for fluorescence in situ hybridization. Finally, we thank the 1988–2014 white-throated sparrow field and laboratory research crews.
| Funders | Funder number |
|---|---|
| R01GM100366, F32GM097837, 1R01GM084229 | |
| Indiana State University | |
| East Carolina University |