Chromosome-wide linkage disequilibrium caused by an inversion polymorphism in the white-throated sparrow (Zonotrichia albicollis)

Abstract

Chromosomal inversions have been of long standing interest to geneticists because they are capable of suppressing recombination and facilitating the formation of adaptive gene complexes. An exceptional inversion polymorphism (ZAL2m) in the white-throated sparrow (Zonotrichia albicollis) is linked to variation in plumage, social behavior and mate choice and is maintained in the population by negative assortative mating. The ZAL2m polymorphism is a complex inversion spanning >100 Mb and has been proposed to be a strong suppressor of recombination, as well as a potential model for studying neo-sex chromosome evolution. To quantify and evaluate those features of the ZAL2m polymorphism, we generated sequence from 8 ZAL2m and 16 ZAL2 chromosomes at 58 loci inside and 4 loci outside the inversion. Inside the inversion we found that recombination was completely suppressed between the ZAL2 and ZAL2m resulting in uniformly high levels of genetic differentiation (FST = 0.94), the formation of two distinct haplotype groups representing the alternate chromosome arrangements, and extensive LD spanning ~104 Mb within the inversion, whereas gene flow was not suppressed outside of the inversion. Finally, while ZAL2m homozygotes are exceedingly rare in the population, occurring at a frequency of < 1%, we detected evidence of historical recombination between ZAL2m chromosomes inside the inversion, refuting its potential status as a completely non-recombining autosome.

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?…”

“…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.…”

“…In the current issue, Huynh et al (2011) report an extensive study of genetic variation and recombination along the polymorphic chromosomes, shedding light on the population processes shaping these chromosomal forms and evaluating their merit as models for the initial stages of sex chromosome evolution. Huynh et al sequenced 62 loci (totalling 36.7 kb) distributed across the entire chromosome, thoroughly sampling across the inversions and the small flanking nonrearranged terminal portions.…”

Supergenes and their role in evolution

“…There are two morphs, 'tan-stripe' and 'white-stripe,' that show divergent plumage, behaviour and mate preference. 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.…”

Linkage mapping of a polymorphic plumage locus associated with intermorph incompatibility in the Gouldian finch (Erythrura gouldiae)

“…For example, chromosome-wide LD caused by complex rearrangements and reduced recombination in the second chromosome of white-throated sparrows (Zonotrichia albicollis) generates the association between plumage polymorphism and social behaviour (Thorneycroft, 1966;Tuttle, 2003;Huynh et al, 2011). Similarly, the three alternative, phenotypically complex and distinctly plumaged morphs of the ruff Philomachus pugnax are determined by a large inversion and the multiple genes combined within such an inversion may act together as alleles of a supergene (Küpper et al, 2016;Lamichhaney et al, 2016).…”