A genetic mechanism for sexual dichromatism in birds

Gazda, Małgorzata Anna; Araújo, Pedro M.; Lopes, Ricardo J.; Toomey, Matthew B.; Andrade, Pedro; Afonso, Sandra; Marques, C; Nunes, Luís; Pereira, Paulo; Trigo, Sandra; Hill, Geoffrey E.; Corbo, Joseph C.; Carneiro, Miguel

doi:10.1126/science.aba0803

Cited by 79 publications

(59 citation statements)

References 61 publications

(19 reference statements)

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“…Birds with low levels of background divergence have served as particularly powerful non-model systems for discovering the genetic bases of melanin and carotenoid coloration6, 8,11,12,14,18,20,[26][27][28], as they often exhibit discrete feather patches that differ in color and pigment type across the body19. Yet, despite the substantial variation in pigmentation across birds, the genetic bases of melanin and carotenoid coloration have only rarely been studied together in the same system (but see 11,14,16), though the genes involved are not currently known to overlap in function or co-localize in the genome3,5.…”

Section: Introductionmentioning

confidence: 99%

Extensive hybridization reveals multiple coloration genes underlying a complex plumage phenotype

Aguillon

Walsh²,

Lovette³

2020

Preprint

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Coloration 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.

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Section: Introductionmentioning

confidence: 99%

Extensive hybridization reveals multiple coloration genes underlying a complex plumage phenotype

Aguillon

Walsh²,

Lovette³

2020

Preprint

View full text Add to dashboard Cite

show abstract

“…Sex hormones such as androgen may indirectly influence the expression of androgen-regulated genes, through binding to transcription factors that interact with regulatory elements such as enhancer and cause sex-biased gene expression, which leads to sex-specific phenotypes ( Coyne et al 2008 ; Mank 2009 ). Whereas male plumage appears to be testosterone-dependent in passerines ( Kimball 2006 ), the molecular mechanisms controlling sex-biased gene expression and development of sexually dimorphic traits in birds is largely unknown ( Kraaijeveld 2019 ; Gazda et al 2020a ). In this study, we identified potential TFs that may regulate the expression of the red plumage color gene CYP2J19 .…”

Section: Resultsmentioning

confidence: 99%

De NovoAssembly of the Northern Cardinal (Cardinalis cardinalis) Genome Reveals Candidate Regulatory Regions for Sexually Dichromatic Red Plumage Coloration

Sin

Edwards

2020

G3 Genes|Genomes|Genetics

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Northern cardinals (Cardinalis cardinalis) are common, mid-sized passerines widely distributed in North America. As an iconic species with strong sexual dichromatism, it has been the focus of extensive ecological and evolutionary research, yet genomic studies investigating the evolution of genotype-phenotype association of plumage coloration and dichromatism are lacking. Here we present a new, highly-contiguous assembly for C. cardinalis. We generated a 1.1 Gb assembly comprised of 4,762 scaffolds, with a scaffold N50 of 3.6 Mb, a contig N50 of 114.4 kb and a longest scaffold of 19.7 Mb. We identified 93.5% complete and single-copy orthologs from an Aves dataset using BUSCO, demonstrating high completeness of the genome assembly. We annotated the genomic region comprising the CYP2J19 gene, which plays a pivotal role in the red coloration in birds. Comparative analyses demonstrated non-exonic regions unique to the CYP2J19 gene in passerines and a long insertion upstream of the gene in C. cardinalis. Transcription factor binding motifs discovered in the unique insertion region in C. cardinalis suggest potential androgen-regulated mechanisms underlying sexual dichromatism. Pairwise Sequential Markovian Coalescent (PSMC) analysis of the genome reveals fluctuations in historic effective population size between 100,000-250,000 in the last 2 millions years, with declines concordant with the beginning of the Pleistocene epoch and Last Glacial Period. This draft genome of C. cardinalis provides an important resource for future studies of ecological, evolutionary, and functional genomics in cardinals and other birds.

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“…Nonetheless, even in the face of apparent strong constraint, sexual dimorphism can evolve rapidly (Stewart and Rice 2018) and differ strongly between closely related species (Owens and Hartley 1998). In at least some cases, dichromatism may evolve by a simple molecular mechanism at a single locus (Gazda et al 2020). Although it is clear that the majority of the color evolution in European butterflies is shared between the sexes, it remains an open question whether this reflects substantial unresolved antagonistic selection.…”

Section: Discussionmentioning

confidence: 99%

Butterfly dichromatism primarily evolved via Darwin's, not Wallace's, model

et al. 2020

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Sexual dimorphism is typically thought to result from sexual selection for elaborated male traits, as proposed by Darwin. However, natural selection could reduce expression of elaborated traits in females, as proposed by Wallace. Darwin and Wallace debated the origins of dichromatism in birds and butterflies, and although evidence in birds is roughly equal, if not in favor of Wallace's model, butterflies lack a similar scale of study. Here, we present a large-scale comparative phylogenetic analysis of the evolution of butterfly coloration, using all European non-hesperiid butterfly species (n = 369). We modeled evolutionary changes in coloration for each species and sex along their phylogeny, thereby estimating the rate and direction of evolution in three-dimensional color space using a novel implementation of phylogenetic ridge regression. We show that male coloration evolved faster than female coloration, especially in strongly dichromatic clades, with male contribution to changes in dichromatism roughly twice that of females. These patterns are consistent with a classic Darwinian model of dichromatism via sexual selection on male coloration, suggesting this model was the dominant driver of dichromatism in European butterflies.

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A genetic mechanism for sexual dichromatism in birds

Cited by 79 publications

References 61 publications

Extensive hybridization reveals multiple coloration genes underlying a complex plumage phenotype

Extensive hybridization reveals multiple coloration genes underlying a complex plumage phenotype

De NovoAssembly of the Northern Cardinal (Cardinalis cardinalis) Genome Reveals Candidate Regulatory Regions for Sexually Dichromatic Red Plumage Coloration

Butterfly dichromatism primarily evolved via Darwin's, not Wallace's, model

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