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

Abstract

Colour polymorphism is known to facilitate speciation but the genetic basis of animal pigmentation and how colour polymorphisms contribute to speciation is poorly understood. Restricted recombination may promote linkage disequilibrium between the colour locus and incompatibility genes. Genomic rearrangement and the position of relevant loci within a chromosome are important factors that influence the frequency of recombination. Therefore, it is important to know the position of the colour locus, gene order and recombination landscape of the chromosome to understand the mechanism that generates incompatibilities between morphs. Recent studies showed remarkable pre-and postzygotic incompatibilities between sympatric colour morphs of the Gouldian finch (Erythrura gouldiae), in which head feather colour is genetically determined by a single sex-linked locus, Red. We constructed a genetic map for the Z chromosome of the Gouldian finch (male-specific map distance = 131 cM), using 618 captive-bred birds and 34 microsatellite markers, to investigate the extent of inter-and intraspecific genomic rearrangements and variation in recombination rate within the Z chromosome. We refined the location of the Red locus to a~7.2-cM interval in a region with a moderate recombination rate but outside the least-recombining, putative centromeric region. There was no evidence of chromosome-wide genomic rearrangements between the chromosomes carrying the red or black alleles with the current marker resolution. This work will contribute to identifying the causal gene, which will in turn enable alternative explanations for the association between incompatibility and colouration, such as fine-scale linkage disequilibrium, genomic rearrangements and pleiotropy, to be tested.

A non-coding region near Follistatin controls head colour polymorphism in the Gouldian finch

“…Orange individuals are thus identical to red individuals at the Red locus, but express a different complement of carotenoids in their masks [19]. Recently, the Red locus was mapped to an approximately 7.2 cM interval on the Z chromosome using microsatellite markers [20]. However, the resolution of this mapping did not allow for the identification of the gene(s) and causal variants underlying this polymorphism.…”

Genetics and evidence for balancing selection of a sex-linked colour polymorphism in a songbird

“…By using high-depth / low SNP density RADSeq 20 and low-depth / high SNP density whole-genome sequencing (see Methods), we identified a region on the Z chromosome strongly associated with redblack head colouration (1,000 permutations, P < 0.05, Fig. 1a, Supplementary Figures 1 and 2) within 4 the candidate interval identified in a previous linkage analysis 21 . The genotypes of the wild birds (n male = 89, n female = 72) from an allele-specific PCR in this region showed a near-perfect association with head colour, with one exception, in a female (Fisher's exact test, male: P < 10 -15 ; female: P = 7.52 × 10 -10 , Fig.…”

“…Centromeres and genomic rearrangements, particularly chromosomal inversions, may reduce recombination rates and generate significant LD blocks between haplotypes 22 . However, our previous work showed that the Red locus is not located near the centromere or in a large genomic rearrangement between morphs 21 . We confirmed this finding with a fine-scale test for inversion breakpoints using long-range PCR: our genomic assembly across the Red locus for each genotype 5 contained contiguous homologous sequence, consistent with the absence of an inversion differentiating the Z R and Z r alleles ( Fig.…”

“…By assessing whether the observed polymorphism in the sequenced region is compatible with these simulations, we can accept or reject the null hypothesis of neutrality. We used the programs SelSim 76 21 and mbs 77…”

“…A circle around a dot indicates the only significant signal in GWAS (P < 0.05, 1,000 permutations). The region shaded in green on the Z chromosome represents the candidate region (~7.2 cM) based on a previous linkage mapping study21 , where the Red locus cosegregated perfectly with microsatellite markers. b, Genotypes of 161 birds from a wild population (male: n black = 62, n red = 27; female: n black = 64, n red = 8) based on two contiguous SNPs in the Red locus, where bar colours represent head colour.…”