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

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 these 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 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 linkage disequilibrium spanning ∼104 Mb within the inversion, whereas gene flow was not suppressed outside the inversion. Finally, although 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 non-recombining autosome. [ABSTRACT FROM AUTHOR]