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 (ZAL2(m)) 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 ZAL2(m) 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 these features of the ZAL2(m) polymorphism, we generated sequence from 8 ZAL2(m) 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 ZAL2 and ZAL2(m), resulting in uniformly high levels of genetic differentiation (F(ST)=0.94), the formation of two distinct haplotype groups representing the alternate chromosome arrangements and extensive linkage disequilibrium spanning ~104 Mb within the inversion, whereas gene flow was not suppressed outside the inversion. Finally, although ZAL2(m) homozygotes are exceedingly rare in the population, occurring at a frequency of < 1%, we detected evidence of historical recombination between ZAL2(m) chromosomes inside the inversion, refuting its potential status as a non-recombining autosome.

Figure 1

ZAL2 and ZAL2^m haplotype networks. Haplotype networks were constructed using the concatenated phased haplotypes from all loci within (a) and outside (b) the inversion. For the white-striped (WS) birds the ZAL2 and ZAL2^m haplotypes are labeled as 2 or 2m. For the tan-striped (TS) birds and Junco (JHY), the haplotypes for each individual were arbitrarily labeled A and B.

Figure 2

Linkage disequilibrium between informative sites across the ZAL2/ZAL2^m chromosomes. The concatenated phased haplotypes were used to generate an LD plot across the ZAL2/2^m chromosomes. Each of the 239 informative SNPs are plotted to scale with respect to their predicted position along the ZAL2 chromosome. Black squares indicate perfect LD between pairs of SNPs (r²=1), gray squares indicate pairs of SNPs with r² between 0 and 1 and white squares show no LD. The striped segments of the line above the LD plot indicate regions outside the inversion and the solid (black) segment of the line indicates the region inside the inversion.