<i>CYP2J19</i> mediates carotenoid colour introgression across a natural avian hybrid zone

Kirschel, Alexander N. G.; Nwankwo, Emmanuel C.; Pierce, Daniel; Lukhele, Sifiso M.; Moysi, Michaella; Ogolowa, Bridget O.; Hayes, Sophia C.; Monadjem, Ara; Brelsford, Alan

doi:10.1111/mec.15691

Cited by 30 publications

(31 citation statements)

References 77 publications

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“…CYP2J19 upregulation via an introgressed variant is causal in changing the typical yellow-feathered canary (Serinus canaria) into the 'red factor' canary [6] and the lack of a functional copy in zebra finch (Taeniopygia guttata) is implicated in the 'yellowbeak' phenotype in which the normally red beak and legs are instead yellow [43]. It is currently one of only two genes known to be involved in red coloration in birds, and evidence of its functioning in natural systems is increasing [44][45][46][47]. Our identification of CYP2J19 in the GWA for wing and tail coloration suggests that it mediates this yellow versus red trait difference in flickers and provides further support for its importance in red coloration across diverse avian lineages.…”

Section: (C) Melanin and Carotenoid Genes Both Associate With Carotenoid Plumage In Flickersmentioning

confidence: 99%

Extensive hybridization reveals multiple coloration genes underlying a complex plumage phenotype

2021

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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.

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Section: (C) Melanin and Carotenoid Genes Both Associate With Carotenoid Plumage In Flickersmentioning

confidence: 99%

Extensive hybridization reveals multiple coloration genes underlying a complex plumage phenotype

2021

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“…An intriguing finding is that historical gene flow between P. pedestris and P. carpetana was asymmetric (Figures 2-4). Unidirectional introgression might have resulted from extensive hybridization during periods of secondary contact followed by repeated backcrossing between hybrids and only one parental species (e.g., Field et al, 2011;Kirschel et al, 2020). Asymmetric gene flow could also be explained by a higher capacity of the donor species to disperse into the range of the recipient one (Jacquemyn et al, 2012;Ortego et al, 2021).…”

Section: Determinants Of Permeable Species Boundariesmentioning

confidence: 99%

Geographical isolation versus dispersal: Relictual alpine grasshoppers support a model of interglacial diversification with limited hybridization

Ortego

Knowles

2021

Molecular Ecology

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Alpine biotas are paradigmatic of the countervailing roles of geographical isolation and dispersal during diversification. In temperate regions, repeated distributional shifts driven by Pleistocene climatic oscillations produced both recurrent pulses of population fragmentation and opportunities for gene flow during range expansions. Here, we test whether a model of divergence in isolation vs. with gene flow is more likely in the diversification of flightless alpine grasshoppers of the genus Podisma from the Iberian Peninsula. The answer to this question can also provide key insights about the pace of evolution. Specifically, if the data fit a divergence in isolation model, this suggests rapid evolution of reproductive isolation. Genomic data confirm a Pleistocene origin of the species complex, and multiple analytical approaches revealed limited asymmetric historical hybridization between two taxa. Genomic‐based demographic reconstructions, spatial patterns of genetic structure and range shifts inferred from palaeodistribution modelling suggest severe range contraction accompanied by declines in effective population sizes during interglacials (i.e., contemporary populations confined to sky islands are relicts) and expansions during the coldest stages of the Pleistocene in each taxon. Although limited hybridization during secondary contact leads to phylogenetic uncertainty if gene flow is not accommodated when estimating evolutionary relationships, all species exhibit strong genetic cohesiveness. Our study lends support to the notion that the accumulation of incipient differences during periods of isolation were sufficient to lead to lineage persistence, but also that the demographic changes, dispersal constraints and spatial distribution of the sky islands themselves mediated species diversification in temperate alpine biotas.

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“…Thus, it has been hypothesized that mito-nuclear incompatibilities could also be revealed in the production of red ketocarotenoid-based ornaments, driving its evolution as individual quality signals (the mitonuclear compatibility hypothesis; Hill and Johnson 2013). Red vs. yellow plumage coloration in subspecies hybrids of tinkerbirds (Pogoniulus pusillus) seems to support this idea (Kirschel et al 2020).…”

Section: Interpreting Carotenoid Ketolase Relocation From Signaling T...mentioning

confidence: 91%

“…[107] Red versus yellow plumage coloration in subspecies hybrids of tinkerbirds (Pogoniulus pusillus) seems to support this idea. [108] However, the well-known differences in mitochondrial redox activity among different tissues [109][110][111] might, in some way, buffer mitonuclear compatibility effects to some extent. Thus, mitonuclear incompatibilities could be less detrimental in the integument if the energy demand is lower in that tissue, also favoring the ketolase relocation.…”

Section: Interpreting Carotenoid Ketolase Relocation From Signaling T...mentioning

confidence: 99%

Relocation to avoid costs: A hypothesis on red carotenoid‐based signals based on recent CYP2J19 gene expression data

et al. 2022

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Sexual and social selections promote the evolution of many conspicuous colorations in animals. These traits would act as individual quality signals when they transmit reliable information. Reliability should be assured by production costs unaffordable for lowquality trait bearers or guaranteed if trait expression is tightly linked to individual quality and cannot be falsified ("index signals"). It has been suggested that colored ornaments produced by red ketocarotenoid pigments could meet the latter. These ketocarotenoids are often obtained by enzymatic transformation of dietary yellow carotenoids. Recently, the first enzyme performing this transformation has been described: CYP2J19. This enzyme, belonging to the cytochrome p450 superfamily, is presumably located in the inner mitochondrial membrane, thus linking color expression with cell respiration efficacy. However, it remains to be clarified if the tissue where this intracellular mechanism acts could influence signal reliability and trait evolution. CYP2J19 expression data are now available for different species and tissues.Here, we review current data in birds and hypothesize that CYP2J19 activity could have evolved in some species by being relocated from the liver tissue to the ornaments (epidermis), a pattern more strongly observed in those birds where the red is expressed in non-feathered bare parts (e.g. bill, legs). One potential explanation is that bare parts, unlike feathers, require a constant carotenoid mobilization to maintain color throughout the year. We propose that tissue relocation allows for avoiding production costs derived from potential CYP2J19 interference on vital liver functions. Implications for signal reliability in ornamental evolution are discussed.

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CYP2J19 mediates carotenoid colour introgression across a natural avian hybrid zone

Cited by 30 publications

References 77 publications

Extensive hybridization reveals multiple coloration genes underlying a complex plumage phenotype

Extensive hybridization reveals multiple coloration genes underlying a complex plumage phenotype

Geographical isolation versus dispersal: Relictual alpine grasshoppers support a model of interglacial diversification with limited hybridization

Relocation to avoid costs: A hypothesis on red carotenoid‐based signals based on recent CYP2J19 gene expression data

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