A mechanism for red coloration in vertebrates

Toomey, Matthew B.; Marques, C; Araújo, Pedro; Huang, Delai; Zhong, Siqiong; Liu, Yu; Schreiner, Gretchen D; Myers, Connie A.; Pereira, Paulo; Afonso, Sandra; Andrade, Pedro; Gazda, Małgorzata Anna; Lopes, Ricardo; Viegas, Iván; Koch, Rebecca E.; Haynes, Maureen E.; Smith, Dustin J.; Ogawa, Yohsuke; Murphy, Daniel P.; Kopec, Rachel; Parichy, David M.; Carneiro, Miguel; Corbo, Joseph C.

doi:10.1016/j.cub.2022.08.013

Cited by 39 publications

(38 citation statements)

References 88 publications

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“…In any case, as mentioned above, a more comprehensive sampling effort across different taxa is now needed to test more conclusively the relative relevance of costly or cost‐free mechanisms. The use of comparative analyses on tissue‐specific expression data of CYP2J19 or any other candidate enzyme [see 117 ] should contribute to clarifying this point. The phylogeny‐based approach would also clarify where the carotenoid conversion for coloration occurred first, providing new grounds for inferring the selective pressures favoring color evolution.…”

Section: Discussionmentioning

confidence: 99%

“…In fact, the dehydrogenase BDH1L has recently been proposed as a missing step in the ketolation process, at least in bird species showing red ketocarotenoid‐based plumages [i.e. 117 ] , with both CYP2J19 and BDH1L being necessary to convert dietary carotenoids into ketocarotenoids. The same study [ 117 ] reported two homologues of BDH1L and CYP2J19 in the pearl danio ( Danio albolineatus ) which are also sufficient to perform the same pigment conversion in this fish.…”

Section: Introductionmentioning

confidence: 99%

“… 117 ] , with both CYP2J19 and BDH1L being necessary to convert dietary carotenoids into ketocarotenoids. The same study [ 117 ] reported two homologues of BDH1L and CYP2J19 in the pearl danio ( Danio albolineatus ) which are also sufficient to perform the same pigment conversion in this fish. This hints at the existence of a general ketolation mechanism in vertebrates.…”

Section: Introductionmentioning

confidence: 99%

“…Additionally, a third gene ( TTC39B ) was shown to act as an enhancer of carotenoid conversion in the same metabolic pathway. [ 117 ] All these findings highlight how interactions between CYP2J19 and other components of carotenoid metabolism may impact the evolutionary trajectory of colorful ornaments. A better understanding of the exact roles of these genes in carotenoid metabolism across different tissues and taxa is now needed to obtain a more comprehensive scenario.…”

Section: Introductionmentioning

confidence: 99%

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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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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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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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“…More recently, studies in non-model organisms have identified new genetic mechanisms that underpin colour variation, independent of the need for a candidate gene approach. This is exemplified by the identification of recently-described enzymes Cyp2J19 and BDH1L in the carotenoid biosynthesis pathway, where a combination of genome wide association studies (GWAS), quantitative trait locus (QTL) mapping, and functional validation illustrated that these enzymes convert dietary carotenoids into red ketocarotenoids in birds (Toomey et al, 2022), and have likely acquired their role in body pigmentation through regulatory co-option from their function in eyes (Twyman et al, 2016). Continuing broad surveys of colour diversity are likely to uncover additional novel mechanisms for pigmentation across the tree of life.…”

Section: Introductionmentioning

confidence: 99%

Genetics of continuous colour variation in a pair of sympatric sulphur butterflies

Hanly

Francescutti

Loh

et al. 2023

Preprint

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Continuous colour polymorphisms can serve as a tractable model for the genetic and developmental architecture of traits, but identification of the causative genetic loci is complex due to the number of individuals needed, and the challenges of scoring continuously varying traits. Here we investigated continuous colour variation in Colias eurytheme and C. philodice, two sister species of sulphur butterflies that hybridise in sympatry. Using Quantitative Trait Locus (QTL) analysis of 483 individuals from interspecific crosses and an high-throughput method of colour quantification, we found that two interacting large effect loci explain around 70% of the heritable variation in orange-to-yellow chromaticity. Knockouts of red Malphighian tubules (red), a candidate gene at the primary QTL likely involved in endosomal maturation, resulted in depigmented wing scales showing disorganised pterin granules. The Z sex chromosome contains a large secondary colour QTL that includes the transcription factor bric-a-brac (bab), which we show can act as a modulator of orange pigmentation in addition to its previously-described role in specifying UV-iridescence. We also describe the QTL architecture of other continuously varying traits, and that wing size maps to the Z chromosome, supporting a Large-X effect model where the genetic control of species-defining traits is enriched on sex chromosomes. This study sheds light on the genetic architecture of a continuously varying trait, and illustrates the power of using automated measurement to score phenotypes that are not always conspicuous to the human eye.

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Canary domestication as a model for genomics research and avian evolution

Lopes,

Carneiro

2024

The Canary

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A mechanism for red coloration in vertebrates

Cited by 39 publications

References 88 publications

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

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

Genetics of continuous colour variation in a pair of sympatric sulphur butterflies

Canary domestication as a model for genomics research and avian evolution

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