Originally published as Genetics Published Articles Ahead of Print on June 18, 2008.

Genetics, Vol. 179, 1455-1468, July 2008, Copyright © 2008
doi:10.1534/genetics.108.088229

The Chromosomal Polymorphism Linked to Variation in Social Behavior in the White-Throated Sparrow (Zonotrichia albicollis) Is a Complex Rearrangement and Suppressor of Recombination

James W. Thomas*,1, Mario Cáceres{dagger}, Joshua J. Lowman*, Caroline B. Morehouse*, Meghan E. Short*, Erin L. Baldwin*, Donna L. Maney{ddagger} and Christa L. Martin*

* Department of Human Genetics, Emory University School of Medicine, Atlanta, Georgia 30322, {dagger} Genes and Disease Program, Center for Genomic Regulation (CRG-UPF), 08003 Barcelona, Spain and {ddagger} Department of Psychology, Emory University, Atlanta, Georgia 30322

1 Corresponding author: Department of Human Genetics, Emory University School of Medicine, 615 Michael St., Suite 301, Atlanta, GA 30322.
E-mail: jthomas{at}genetics.emory.edu

Variation in social behavior and plumage in the white-throated sparrow (Zonotrichia albicollis) is linked to an inversion polymorphism on chromosome 2. Here we report the results of our comparative cytogenetic mapping efforts and population genetics studies focused on the genomic characterization of this balanced chromosomal polymorphism. Comparative chromosome painting and cytogenetic mapping of 15 zebra finch BAC clones to the standard (ZAL2) and alternative (ZAL2m) arrangements revealed that this chromosome is orthologous to chicken chromosome 3, and that at a minimum, ZAL2 and ZAL2m differ by a pair of included pericentric inversions that we estimate span at least 98 Mb. Population-based sequencing and genotyping of multiple loci demonstrated that ZAL2m suppresses recombination in the heterokaryotype and is evolving as a rare nonrecombining autosomal segment of the genome. In addition, we estimate that the first inversion within the ZAL2m arrangement originated 2.2 ± 0.3 million years ago. Finally, while previously recognized as a genetic model for the evolution of social behavior, we found that the ZAL2/ZAL2m polymorphism also shares genetic and phenotypic features with the mouse t complex and we further suggest that the ZAL2/ZAL2m polymorphism is a heretofore unrecognized model for the early stages of sex chromosome evolution.