Pleiotropy in the melanocortin system

expression levels of this system are associated with melanogenesis and pigmentation in the tawny owl (Strix aluco)

Guillaume Emaresi, Anne-Lyse Ducrest, Pierre Bize, Hannes Richter, Celine Simon, Alexandre Roulin*

*Corresponding author for this work

Research output: Contribution to journalArticle

35 Citations (Scopus)

Abstract

The adaptive function of melanin-based coloration is a long-standing debate. A recent genetic model suggested that pleiotropy could account for covariations between pigmentation, behaviour, morphology, physiology and life history traits. We explored whether the expression levels of genes belonging to the melanocortin system (MC1R, POMC, PC1/3, PC2 and the antagonist ASIP), which have many pleiotropic effects, are associated with melanogenesis (through variation in the expression of the genes MITF, SLC7A11, TYR, TYRP1) and in turn melanin-based coloration. We considered the tawny owl (Strix aluco) because individuals vary continuously from light to dark reddish, and thus, colour variation is likely to stem from differences in the levels of gene expression. We measured gene expression in feather bases collected in nestlings at the time of melanin production. As expected, the melanocortin system was associated with the expression of melanogenic genes and pigmentation. Offspring of darker reddish fathers expressed PC1/3 to lower levels but tended to express PC2 to higher levels. The convertase enzyme PC1/3 cleaves the POMC prohormone to obtain ACTH, while the convertase enzyme PC2 cleaves ACTH to produce -melanin-stimulating hormone (-MSH). ACTH regulates glucocorticoids, hormones that modulate stress responses, while -MSH induces eumelanogenesis. We therefore conclude that the melanocortin system, through the convertase enzymes PC1/3 and PC2, may account for part of the interindividual variation in melanin-based coloration in nestling tawny owls. Pleiotropy may thus account for the covariation between phenotypic traits involved in social interactions (here pigmentation) and life history, morphology, behaviour and physiology.

Original languageEnglish
Pages (from-to)4915-4930
Number of pages16
JournalMolecular Ecology
Volume22
Issue number19
Early online date21 Aug 2013
DOIs
Publication statusPublished - Oct 2013

Keywords

  • adaptation
  • birds
  • development and evolution
  • convertase
  • ecological genetics
  • PC1/3
  • PC2
  • protease

Cite this

Pleiotropy in the melanocortin system : expression levels of this system are associated with melanogenesis and pigmentation in the tawny owl (Strix aluco). / Emaresi, Guillaume; Ducrest, Anne-Lyse; Bize, Pierre; Richter, Hannes; Simon, Celine; Roulin, Alexandre.

In: Molecular Ecology, Vol. 22, No. 19, 10.2013, p. 4915-4930.

Research output: Contribution to journalArticle

Emaresi, Guillaume ; Ducrest, Anne-Lyse ; Bize, Pierre ; Richter, Hannes ; Simon, Celine ; Roulin, Alexandre. / Pleiotropy in the melanocortin system : expression levels of this system are associated with melanogenesis and pigmentation in the tawny owl (Strix aluco). In: Molecular Ecology. 2013 ; Vol. 22, No. 19. pp. 4915-4930.
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abstract = "The adaptive function of melanin-based coloration is a long-standing debate. A recent genetic model suggested that pleiotropy could account for covariations between pigmentation, behaviour, morphology, physiology and life history traits. We explored whether the expression levels of genes belonging to the melanocortin system (MC1R, POMC, PC1/3, PC2 and the antagonist ASIP), which have many pleiotropic effects, are associated with melanogenesis (through variation in the expression of the genes MITF, SLC7A11, TYR, TYRP1) and in turn melanin-based coloration. We considered the tawny owl (Strix aluco) because individuals vary continuously from light to dark reddish, and thus, colour variation is likely to stem from differences in the levels of gene expression. We measured gene expression in feather bases collected in nestlings at the time of melanin production. As expected, the melanocortin system was associated with the expression of melanogenic genes and pigmentation. Offspring of darker reddish fathers expressed PC1/3 to lower levels but tended to express PC2 to higher levels. The convertase enzyme PC1/3 cleaves the POMC prohormone to obtain ACTH, while the convertase enzyme PC2 cleaves ACTH to produce -melanin-stimulating hormone (-MSH). ACTH regulates glucocorticoids, hormones that modulate stress responses, while -MSH induces eumelanogenesis. We therefore conclude that the melanocortin system, through the convertase enzymes PC1/3 and PC2, may account for part of the interindividual variation in melanin-based coloration in nestling tawny owls. Pleiotropy may thus account for the covariation between phenotypic traits involved in social interactions (here pigmentation) and life history, morphology, behaviour and physiology.",
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author = "Guillaume Emaresi and Anne-Lyse Ducrest and Pierre Bize and Hannes Richter and Celine Simon and Alexandre Roulin",
note = "We are grateful to the Swiss National Science Foundation for financing the study and Louis Bernatchez and five anonymous reviewers for useful comments. G.E., A.-L.D., P.B. and A.R. designed the study. G.E., P.B. and A.R. contributed to field work and field data collection. G.E., A.-L.D., H.R. and C.S. performed the molecular work. A.R. and G.E. performed the statistical analyses and wrote the article. A.R., G.E., A.-L.D. and P.B. edited the manuscript.",
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AU - Bize, Pierre

AU - Richter, Hannes

AU - Simon, Celine

AU - Roulin, Alexandre

N1 - We are grateful to the Swiss National Science Foundation for financing the study and Louis Bernatchez and five anonymous reviewers for useful comments. G.E., A.-L.D., P.B. and A.R. designed the study. G.E., P.B. and A.R. contributed to field work and field data collection. G.E., A.-L.D., H.R. and C.S. performed the molecular work. A.R. and G.E. performed the statistical analyses and wrote the article. A.R., G.E., A.-L.D. and P.B. edited the manuscript.

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N2 - The adaptive function of melanin-based coloration is a long-standing debate. A recent genetic model suggested that pleiotropy could account for covariations between pigmentation, behaviour, morphology, physiology and life history traits. We explored whether the expression levels of genes belonging to the melanocortin system (MC1R, POMC, PC1/3, PC2 and the antagonist ASIP), which have many pleiotropic effects, are associated with melanogenesis (through variation in the expression of the genes MITF, SLC7A11, TYR, TYRP1) and in turn melanin-based coloration. We considered the tawny owl (Strix aluco) because individuals vary continuously from light to dark reddish, and thus, colour variation is likely to stem from differences in the levels of gene expression. We measured gene expression in feather bases collected in nestlings at the time of melanin production. As expected, the melanocortin system was associated with the expression of melanogenic genes and pigmentation. Offspring of darker reddish fathers expressed PC1/3 to lower levels but tended to express PC2 to higher levels. The convertase enzyme PC1/3 cleaves the POMC prohormone to obtain ACTH, while the convertase enzyme PC2 cleaves ACTH to produce -melanin-stimulating hormone (-MSH). ACTH regulates glucocorticoids, hormones that modulate stress responses, while -MSH induces eumelanogenesis. We therefore conclude that the melanocortin system, through the convertase enzymes PC1/3 and PC2, may account for part of the interindividual variation in melanin-based coloration in nestling tawny owls. Pleiotropy may thus account for the covariation between phenotypic traits involved in social interactions (here pigmentation) and life history, morphology, behaviour and physiology.

AB - The adaptive function of melanin-based coloration is a long-standing debate. A recent genetic model suggested that pleiotropy could account for covariations between pigmentation, behaviour, morphology, physiology and life history traits. We explored whether the expression levels of genes belonging to the melanocortin system (MC1R, POMC, PC1/3, PC2 and the antagonist ASIP), which have many pleiotropic effects, are associated with melanogenesis (through variation in the expression of the genes MITF, SLC7A11, TYR, TYRP1) and in turn melanin-based coloration. We considered the tawny owl (Strix aluco) because individuals vary continuously from light to dark reddish, and thus, colour variation is likely to stem from differences in the levels of gene expression. We measured gene expression in feather bases collected in nestlings at the time of melanin production. As expected, the melanocortin system was associated with the expression of melanogenic genes and pigmentation. Offspring of darker reddish fathers expressed PC1/3 to lower levels but tended to express PC2 to higher levels. The convertase enzyme PC1/3 cleaves the POMC prohormone to obtain ACTH, while the convertase enzyme PC2 cleaves ACTH to produce -melanin-stimulating hormone (-MSH). ACTH regulates glucocorticoids, hormones that modulate stress responses, while -MSH induces eumelanogenesis. We therefore conclude that the melanocortin system, through the convertase enzymes PC1/3 and PC2, may account for part of the interindividual variation in melanin-based coloration in nestling tawny owls. Pleiotropy may thus account for the covariation between phenotypic traits involved in social interactions (here pigmentation) and life history, morphology, behaviour and physiology.

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KW - birds

KW - development and evolution

KW - convertase

KW - ecological genetics

KW - PC1/3

KW - PC2

KW - protease

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