Extensive hybridization reveals multiple coloration genes underlying a complex plumage phenotype

Coloration is an important target of both natural and sexual selection. Discovering the genetic basis of colour differences can help us to understand how this visually striking phenotype evolves. Hybridizing taxa with both clear colour differences and shallow genomic divergences are unusually tractable for associating coloration phenotypes with their causal genotypes. Here, we leverage the extensive admixture between two common North American woodpeckers—yellow-shafted and red-shafted flickers—to identify the genomic bases of six distinct plumage patches involving both melanin and carotenoid pigments. Comparisons between flickers across approximately 7.25 million genome-wide SNPs show that these two forms differ at only a small proportion of the genome (mean F ST = 0.008). Within the few highly differentiated genomic regions, we identify 368 SNPs significantly associated with four of the six plumage patches. These SNPs are linked to multiple genes known to be involved in melanin and carotenoid pigmentation. For example, a gene ( CYP2J19 ) known to cause yellow to red colour transitions in other birds is strongly associated with the yellow versus red differences in the wing and tail feathers of these flickers. Additionally, our analyses suggest novel links between known melanin genes and carotenoid coloration. Our finding of patch-specific control of plumage coloration adds to the growing body of literature suggesting colour diversity in animals could be created through selection acting on novel combinations of coloration genes.

Extensive hybridization reveals multiple coloration genes underlying a complex plumage phenotype

ABSTRACTColoration is an important target of both natural and sexual selection. Discovering the genetic basis of color differences can help us to understand how this visually striking phenotype evolves. Hybridizing taxa with both clear color differences and shallow genomic divergences are unusually tractable for associating coloration phenotypes with their causal genotypes. Here, we leverage the extensive admixture between two common North American woodpeckers—yellow-shafted and red-shafted flickers—to identify the genomic bases of six distinct plumage patches involving both melanin and carotenoid pigments. Comparisons between flickers across ~8.5 million genome-wide SNPs show that these two forms differ at only a small proportion of the genome (mean FST = 0.007). Within the few highly differentiated genomic regions, we identify 408 SNPs significantly associated with four of the six plumage patches. These SNPs are linked to multiple genes known to be involved in melanin and carotenoid pigmentation. For example, a gene (CYP2J19) known to cause yellow to red color transitions in other birds is strongly associated with the yellow versus red differences in the wings and tail feathers of these flickers. Additionally, our analyses suggest novel links between known melanin genes and carotenoid coloration. Our finding of patch-specific control of plumage coloration adds to the growing body of literature suggesting color diversity in animals could be created through selection acting on novel combinations of coloration genes.

Genomic and plumage variation in Vermivora hybrids

Hybrids with different combinations of traits can be used to identify genomic regions that underlie phenotypic characters important to species identity and recognition. Here, we explore links between genomic and plumage variation in Blue-winged Warbler x Golden-winged Warbler (Vermivora cyanoptera x V. chrysoptera) hybrids, which have traditionally been categorized into 2 discrete types. “Lawrence’s” hybrids are yellow overall, similar to Blue-winged Warblers, but exhibit the black throat patch and face mask of Golden-winged Warblers. “Brewster’s” hybrids are similar to Golden-winged Warblers, but lack the black throat patch and face mask, and sometimes have yellow on their underparts. Previous studies hypothesized that (1) first generation hybrids are of the Brewster’s type and can be distinguished by the amount of yellow on their underparts, and that (2) the throat patch/mask phenotype is consistent with Mendelian inheritance and controlled by variation in a locus near the Agouti-signaling protein (ASIP) gene. We addressed these hypotheses using whole genome re-sequencing of parental and hybrid individuals. We found that Brewster’s hybrids had genomic hybrid index scores indicating this phenotype can arise by majority ancestry from either parental species, that their plumage varied in levels of carotenoid pigmentation, and individuals captured in multiple years grew consistently less yellow over time. Variation in carotenoid pigmentation showed little relationship with genomic hybrid index score and is thus inconsistent with previous hypotheses that first generation hybrids can be distinguished by the amount of yellow in their plumage. Our results also confirm that variation near ASIP underlies the throat patch phenotype, which we refined to an ~10–15 Kb region upstream of the coding sequence. Overall, our results support the notion that traditional categorization of hybrids as either Lawrence’s or Brewster’s oversimplifies continuous variation in carotenoid pigmentation, and its inferred underlying genetic basis, and is based primarily on one discrete trait, which is the throat patch/mask phenotype.

Short-term stress: effects on cortisol levels and carotenoid spots in Arctic char (Salvelinus alpinus)

Earlier studies have shown that the carotenoid pigmentation in Arctic char (Salvelinus alpinus (L., 1758)) is connected to stress responsiveness. These studies also suggested that the pigmentation is dynamic and can change quickly. Therefore, we wanted to investigate the effect of a short-term stressor on the number of carotenoid spots before and after certain time intervals after the stressor. Individuals were exposed to a net-restraint stressor for 1 min and then assigned a recovery time of either 0, 1, 2, 8, or 24 h. Photographs were taken before the stressor and after the recovery time to count carotenoid spots and to look at the relative changes over time. Behaviour during the stressor and cortisol levels after the assigned recovery time were evaluated. We found that the change in spottiness, measured as the ratio of spots after and before the stressor, changed with recovery time on the right side but not on the left side. Furthermore, left-side spots were correlated with struggling activity. Thus, carotenoid pigmentation seems to be lateralized, with more static spots on the left side connected to stress responsiveness, whereas spots on the right side seem to be more dynamic.