PgmNr P2069: Degeneration and positive selection of a non-recombining chromosomal inversion underlying behavioral polymorphism in the white-throated sparrow.

Authors:
D. Sun ¹ ; I. Huh ¹ ; D. Maney ² ; S. Yi ¹

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Institutes
1) Georgia Institute of Technology, Atlanta, GA; 2) Emory University, Atlanta, GA.

Abstract:

The white-throated sparrow is a common North American songbird with two adult plumage morphs known as white- and tan-striped. The morphs differ in behavior, with white birds exhibiting more aggression and exhibiting less parental care than tan birds during the breeding season. The phenotypic differences are associated with multiple chromosomal inversions in the second chromosome. White birds are heterozygous for the inversions (ZAL2/ZAL2^m), whereas tan birds are homozygous (ZAL2/ZAL2). Tan and white morphs are maintained in relatively equal proportions in the population via a strong disassortative mating (nearly all mating pairs consist of one white and one tan bird). To elucidate the genetic and molecular basis of these fundamental phenotypic differences between the morphs, we compared the whole genome sequences of a rare superwhite bird (ZAL2^m/ZAL2^m) to the reference tan genome (ZAL2/ZAL2). We also incorporated RNA-seq data from a sample of 22 individuals that included tan, white and superwhite birds. Utilizing such rich genomic and transcriptomic resources, we can distinguish genomic scaffolds that reside within and outside the inversions. As expected, F_ST analyses indicate little recombination between the ZAL2 and ZAL2^m chromosomes within inversion. The inverted scaffolds are on average 1% divergent at the nucleotide level. Despite such small genetic differences, ZAL2^m scaffolds exhibit signs of degeneration via accumulation of slightly deleterious nonsynonymous substitutions, as expected due to the suppression of recombination. On the other hand, we also found signatures of adaptive evolution in both protein-coding and regulatory regions. Intriguingly, regions that exhibit signs of positive selection in ZAL2 and ZAL2^m chromosomes can be assigned to distinctive functional categories. Positively selected genes in ZAL2 are related to the immune system, whereas those in ZAL2^m are enriched for muscle structure development, locomotion and neuron differentiation. Our study provides new insights into how genetic differentiation can lead to phenotypic divergence in this unique vertebrate model system.