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

Abstract

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 (ZAL2 m ) arrangements revealed that this chromosome is orthologous to chicken chromosome 3, and that at a minimum, ZAL2 and ZAL2 m 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 ZAL2 m 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 ZAL2 m arrangement originated 2.2 6 0.3 million years ago. Finally, while previously recognized as a genetic model for the evolution of social behavior, we found that the ZAL2/ZAL2 m polymorphism also shares genetic and phenotypic features with the mouse t complex and we further suggest that the ZAL2/ZAL2 m polymorphism is a heretofore unrecognized model for the early stages of sex chromosome evolution.

Supergenes and their role in evolution

“…The morphs show strong negative assortative mating with 96% of all pairings being between individuals of opposite morphs, and are associated with two alternative forms of chromosome 2, characterised by an extremely large (c. 104 Mb out of c. 110 Mb of chromosome 2) region of linkage disequilibrium and high levels of genetic divergence compared with collinear regions (Huynh et al, 2010a), associated with one or more inversions (Thomas et al, 2008;Huynh et al, 2010b;Davis et al, 2011). The existence of a partially non-recombining chromosome containing on the order of 1000 genes (Thomas et al, 2008) and maintained in a balanced state by assortative mating offers a striking parallel to a sex chromosome and effectively represents a second and separate set of sex chromosomes. The genetic determination of reproductive morphs in Z. albicollis fulfils many of the criteria necessary for designation of a supergene: there is a mechanism to reduce recombination and a balanced polymorphism of a complex, polygenic and co-adapted phenotype.…”

Estrogen receptor α polymorphism in a species with alternative behavioral phenotypes

“…1) that segregate absolutely with a rearranged chromosome 2 called ZAL2 m (2). ZAL2 m consists of at least two pericentric inversions (3) and is present in all white-striped (WS) individuals but never in tan-striped (TS) individuals. The rearrangement occurs equally in males and females, and almost all breeding pairs consist of one individual with and one without it (4).…”

Stripes, sex and sparrows: what processes underlie heteromorphic chromosome evolution?

“…Similarly, a chromosomal inversion and fusion event in the black muntjac within the past 0.5 million years also bears an imprint of accumulated mutation on the neo-Y chromosome (Zhou et al, 2008). In marked contrast to these studies, the ZAL2 m chromosome, which is estimated to have split from ZAL2 two million years ago, does not show significant signs of genetic degeneration (Thomas et al, 2008;Romanov et al, 2009;Huynh et al, 2011). What might underlie the differences between these cases?…”

“…ZAL2 m /ZAL2 m homozygotes are vanishingly rare (only a few birds have ever been recorded), so ZAL2 m chromosomes occur almost exclusively in the heterozygous state with the ZAL2 chromosome. The karyotype frequencies appear to be balanced by strong negative assortative mating, in which almost all breeding pairs are between birds with different plumage colours (and their associated different chromosome complements) (Thomas et al, 2008). The chromosome dimorphism, nearly obligate cross-mating and the rarity of ZAL2 m homozgyotes, coupled with the complex inversion patterns and a suggested absence of recombination, are reminiscent of balancing selection associated with heterogametic sex chromosomes (Thomas et al, 2008).…”

“…Several lines of evidence also suggest that the divergence between the chromosome forms occurred before the radiation of the Zonotrichia clade (Thomas et al, 2008;Romanov et al, 2009;Huynh et al, 2011), which raises the question of the processes favouring long-term maintenance of the haplotypes in the clade, and the possibility of similar cryptic behavioural polymorphisms occurring in other species in the absence of plumage dimorphism. It is then tempting to speculate that the stripe pattern might represent a male signalling display (Tuttle, 2003) more recently recruited onto the polymorphic chromosome, with optimal effects in combination with the other male behaviours correlated with the ZAL2 m haplotype.…”