A transcriptomic investigation of handicap models in sexual selection

Marius Alexander Wenzel, Lucy M. I. Webster, Steve Paterson, Francois Mougeot, Jesus Martinez-Padilla, Stuart B. Piertney

Research output: Contribution to journalArticle

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Abstract

Handicap models link the evolution of secondary sexual ornaments to physiological costs and thus provide a mechanistic explanation for signal honesty in sexual selection. Two commonly invoked models, the immunocompetence handicap hypothesis (ICHH) and the oxidative stress handicap hypothesis (OSHH), propose suppression of immunocompetence or increase of oxidative stress by testosterone, but empirical evidence for both models is controversial and based on morphological and physiological assays. Here, we investigated these two models on the gene transcription level using microarrays to quantify the transcriptomic response of red grouse (Lagopus lagopus scoticus) caecal, spleen and liver tissues to experimental manipulation of testosterone levels. We used a geneontology framework to identify genes related to immune function and response to reactive oxygen species and examined how transcription levels changed under experimentally increased testosterone levels in birds with parasites present or absent. Contrary to our expectations, testosterone had virtually no effect on gene transcription in spleen and liver. A small number of genes were significantly differentially regulated in caecum, and while their functions and transcription changes are consistent with the ICHH, we found little support for the OSHH. More genes responded to testosterone in the presence rather than absence of parasites, suggesting that handicap mechanisms may be context dependent and more pronounced in the presence of adverse environmental conditions. These findings illustrate the utility of transcriptomics to investigating handicap models, suggest that classic models may not underlie the handicap mechanism, and indicate that novel emerging models involving different mediators and physiological systems should be examined.

Original languageEnglish
Pages (from-to)221-234
Number of pages14
JournalBehavioral Ecology and Sociobiology
Volume67
Issue number2
Early online date8 Nov 2012
DOIs
Publication statusPublished - Feb 2013

Keywords

  • sexual selection
  • immunocompetence handicap hypothesis
  • ICHH
  • oxidative stress handicap hypothesis
  • OSHH
  • transcriptomics
  • lagopus-lagopus-scoticus
  • male red grouse
  • coloration predicts resistance
  • condition-dependent traits
  • Juncos Junco-hyemalis
  • false discovery rate
  • host immune function
  • male house sparrows
  • immunocompetence handicap
  • oxidative stress

Cite this

A transcriptomic investigation of handicap models in sexual selection. / Wenzel, Marius Alexander; Webster, Lucy M. I.; Paterson, Steve; Mougeot, Francois; Martinez-Padilla, Jesus; Piertney, Stuart B.

In: Behavioral Ecology and Sociobiology, Vol. 67, No. 2, 02.2013, p. 221-234.

Research output: Contribution to journalArticle

Wenzel, Marius Alexander ; Webster, Lucy M. I. ; Paterson, Steve ; Mougeot, Francois ; Martinez-Padilla, Jesus ; Piertney, Stuart B. / A transcriptomic investigation of handicap models in sexual selection. In: Behavioral Ecology and Sociobiology. 2013 ; Vol. 67, No. 2. pp. 221-234.
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N2 - Handicap models link the evolution of secondary sexual ornaments to physiological costs and thus provide a mechanistic explanation for signal honesty in sexual selection. Two commonly invoked models, the immunocompetence handicap hypothesis (ICHH) and the oxidative stress handicap hypothesis (OSHH), propose suppression of immunocompetence or increase of oxidative stress by testosterone, but empirical evidence for both models is controversial and based on morphological and physiological assays. Here, we investigated these two models on the gene transcription level using microarrays to quantify the transcriptomic response of red grouse (Lagopus lagopus scoticus) caecal, spleen and liver tissues to experimental manipulation of testosterone levels. We used a geneontology framework to identify genes related to immune function and response to reactive oxygen species and examined how transcription levels changed under experimentally increased testosterone levels in birds with parasites present or absent. Contrary to our expectations, testosterone had virtually no effect on gene transcription in spleen and liver. A small number of genes were significantly differentially regulated in caecum, and while their functions and transcription changes are consistent with the ICHH, we found little support for the OSHH. More genes responded to testosterone in the presence rather than absence of parasites, suggesting that handicap mechanisms may be context dependent and more pronounced in the presence of adverse environmental conditions. These findings illustrate the utility of transcriptomics to investigating handicap models, suggest that classic models may not underlie the handicap mechanism, and indicate that novel emerging models involving different mediators and physiological systems should be examined.

AB - Handicap models link the evolution of secondary sexual ornaments to physiological costs and thus provide a mechanistic explanation for signal honesty in sexual selection. Two commonly invoked models, the immunocompetence handicap hypothesis (ICHH) and the oxidative stress handicap hypothesis (OSHH), propose suppression of immunocompetence or increase of oxidative stress by testosterone, but empirical evidence for both models is controversial and based on morphological and physiological assays. Here, we investigated these two models on the gene transcription level using microarrays to quantify the transcriptomic response of red grouse (Lagopus lagopus scoticus) caecal, spleen and liver tissues to experimental manipulation of testosterone levels. We used a geneontology framework to identify genes related to immune function and response to reactive oxygen species and examined how transcription levels changed under experimentally increased testosterone levels in birds with parasites present or absent. Contrary to our expectations, testosterone had virtually no effect on gene transcription in spleen and liver. A small number of genes were significantly differentially regulated in caecum, and while their functions and transcription changes are consistent with the ICHH, we found little support for the OSHH. More genes responded to testosterone in the presence rather than absence of parasites, suggesting that handicap mechanisms may be context dependent and more pronounced in the presence of adverse environmental conditions. These findings illustrate the utility of transcriptomics to investigating handicap models, suggest that classic models may not underlie the handicap mechanism, and indicate that novel emerging models involving different mediators and physiological systems should be examined.

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KW - male red grouse

KW - coloration predicts resistance

KW - condition-dependent traits

KW - Juncos Junco-hyemalis

KW - false discovery rate

KW - host immune function

KW - male house sparrows

KW - immunocompetence handicap

KW - oxidative stress

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JO - Behavioral Ecology and Sociobiology

JF - Behavioral Ecology and Sociobiology

SN - 0340-5443

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