Divergence and functional degradation of a sex chromosome-like supergene (the sparrow with four sexes)

In January 2016, when the paper was published in Current Biology, it showed unequivocally that chromosome 2 was evolving like a sex chromosome. White–white and tan–tan matings were exceedingly rare. Using the whole-genome sequences of 50 birds, the team demonstrated that the genes in the inversion were acquiring mutations much more quickly than elsewhere in the genome, a pattern that echoed the evolution of sex chromosomes in humans and birds.

Arnold, C. The sparrow with four sexes. Nature 539, 482–484 (2016). https://doi.org/10.1038/539482a

Divergence and Functional Degradation of a Sex Chromosome-like Supergene
Elaina M. Tuttle Alan O. Bergland Marisa L. Korody Wesley C. Warren Rusty A. Gonser Christopher N. Balakrishnan, Current Biology VOLUME 26, ISSUE 3, P344-350, FEBRUARY 08, 2016 https://doi.org/10.1016/j.cub.2015.11.069

^{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”) 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 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.}

Video Abstract

Graphical Abstract

References (Current Biology article)

Kunte K. Zhang W. Tenger-Trolander A. Palmer D.H. Martin A. Reed R.D. Mullen S.P. Kronforst M.R. doublesex is a mimicry supergene. Nature. 2014; 507: 229-232

Wang J. Wurm Y. Nipitwattanaphon M. Riba-Grognuz O. Huang Y.-C. Shoemaker D. Keller L. A Y-like social chromosome causes alternative colony organization in fire ants. Nature. 2013; 493: 664-668

Tuttle E.M. Alternative reproductive strategies in the white-throated sparrow: behavioral and genetic evidence. Behav. Ecol. 2003; 14: 425-432

Formica V.A. Tuttle E.M. Examining the social landscapes of alternative reproductive strategies.
J. Evol. Biol. 2009; 22: 2395-2408

Knapton R.W. Falls J.B. Differences in parental contribution among pair types in the polymorphic white-throated sparrow. Can. J. Zool. 1983; 61: 1288-1292

Thorneycroft H.B. Chromosomal polymorphism in the white-throated sparrow, Zonotrichia albicollis (Gmelin). Science. 1966; 154: 1571-1572

Thorneycroft H.B. A cytogenetic study of white-throated sparrow, Zonotrichia albicollis (Gmelin). Evolution. 1975; 29: 611-621

Lowther J.K. Polymorphism in the white-throated sparrow Zonotrichia albicollis (Gmelin). Can. J. Zool. 1961; 39: 281-292

Schwander T. Libbrecht R. Keller L. Supergenes and complex phenotypes. Curr. Biol. 2014; 24: R288-R294

Frankl-Vilches C. Kuhl H. Werber M. Klages S. Kerick M. Bakker A. de Oliveira E.H.C. Reusch C. Capuano F. Vowinckel J. et al. Using the canary genome to decipher the evolution of hormone-sensitive gene regulation in seasonal singing birds. Genome Biol. 2015; 16: 19

Thomas J.W. Cáceres M. Lowman J.J. Morehouse C.B. Short M.E. Baldwin E.L. Maney D.L. Martin C.L. The chromosomal polymorphism linked to variation in social behavior in the white-throated sparrow (Zonotrichia albicollis) is a complex rearrangement and suppressor of recombination. Genetics. 2008; 179: 1455-1468

Horton B.M. Hudson W.H. Ortlund E.A. Shirk S. Thomas J.W. Young E.R. Zinzow-Kramer W.M. Maney D.L. Estrogen receptor α polymorphism in a species with alternative behavioral phenotypes. Proc. Natl. Acad. Sci. USA. 2014; 111: 1443-1448

Goodson J.L. Territorial aggression and dawn song are modulated by septal vasotocin and vasoactive intestinal polypeptide in male field sparrows (Spizella pusilla). Horm. Behav. 1998; 34: 67-77

Goodson J.L. Adkins-Regan E. Effect of intraseptal vasotocin and vasoactive intestinal polypeptide infusions on courtship song and aggression in the male zebra finch (Taeniopygia guttata). J. Neuroendocrinol. 1999; 11: 19-25

Ashburner M. Ball C.A. Blake J.A. Botstein D. Butler H. Cherry J.M. Davis A.P. Dolinski K. Dwight S.S. Eppig J.T. et al. Gene ontology: tool for the unification of biology. Nat. Genet. 2000; 25: 25-29

Balakrishnan C.N. Mukai M. Gonser R.A. Wingfield J.C. London S.E. Tuttle E.M. Clayton D.F. Brain transcriptome sequencing and assembly of three songbird model systems for the study of social behavior. PeerJ. 2014; 2: e396

Stager M. Swanson D.L. Cheviron Z.A. Regulatory mechanisms of metabolic flexibility in the dark-eyed junco (Junco hyemalis). J. Exp. Biol. 2015; 218: 767-777

Davis J.K. Mittel L.B. Lowman J.J. Thomas P.J. Maney D.L. Martin C.L. Thomas J.W. NISC Comparative Sequencing Program Haplotype-based genomic sequencing of a chromosomal polymorphism in the white-throated sparrow (Zonotrichia albicollis). J. Hered. 2011; 102: 380-390

Huynh L.Y. Maney D.L. Thomas J.W. Chromosome-wide linkage disequilibrium caused by an inversion polymorphism in the white-throated sparrow (Zonotrichia albicollis). Heredity (Edinb). 2011; 106: 537-546

Stoletzki N. Eyre-Walker A. Estimation of the neutrality index. Mol. Biol. Evol. 2011; 28: 63-70

Bachtrog D. Expression profile of a degenerating neo-Y chromosome in Drosophila. Curr. Biol. 2006; 16: 1694-1699

Hough J. Hollister J.D. Wang W. Barrett S.C.H. Wright S.I. Genetic degeneration of old and young Y chromosomes in the flowering plant Rumex hastatulus. Proc. Natl. Acad. Sci. USA. 2014; 111: 7713-7718

Charlesworth B. The effect of life-history and mode of inheritance on neutral genetic variability. Genet. Res. 2001; 77: 153-166

Charlesworth B. Coyne J.A. Barton N.H. The relative rates of evolution of sex chromosomes and autosomes. Am. Nat. 1987; 130: 113-146

Ramachandran S. Rosenberg N.A. Feldman M.W. Wakeley J. Population differentiation and migration: coalescence times in a two-sex island model for autosomal and X-linked loci. Theor. Popul. Biol. 2008; 74: 291-301

Fay J.C. Wu C.I. Hitchhiking under positive Darwinian selection. Genetics. 2000; 155: 1405-1413

Pryke S.R. Griffith S.C. Genetic incompatibility drives sex allocation and maternal investment in a polymorphic finch. Science. 2009; 323: 1605-1607

Bonier F. Martin P.R. Wingfield J.C. Maternal corticosteroids influence primary offspring sex ratio in a free-ranging passerine bird. Behav. Ecol. 2007; 18: 1045-1050

Payne R.B. Two apparent hybrid Zonotrichia sparrows. Auk. 1979; 96: 595-599

Weckstein J.D. Zink R.M. Blackwell-Rago R.C. Nelson D.A. Anomalous variation in mitochondrial genomes of white-crowned (Zonotrichia leucophrys) and golden-crowned (Z. atricapilla) sparrows: pseudogenes, hybridization, or incomplete lineage sorting?.Auk. 2001; 118: 231-236

Bellott D.W. Hughes J.F. Skaletsky H. Brown L.G. Pyntikova T. Cho T.-J. Koutseva N. Zaghlul S.
Graves T. Rock S. et al. Mammalian Y chromosomes retain widely expressed dosage-sensitive regulators. Nature. 2014; 508: 494-499

Cortez D. Marin R. Toledo-Flores D. Froidevaux L. Liechti A. Waters P.D. Grützner F. Kaessmann H. Origins and functional evolution of Y chromosomes across mammals. Nature. 2014; 508: 488-493

Hurst L.D. Why are there only two sexes?. Proc. R. Soc. Lond. B Biol. Sci. 1996; 263: 415-422