Digging for gold nuggets

uncovering novel candidate genes for variation in gastrointestinal nematode burden in a wild bird species

M. A. Wenzel*, S. B. Piertney

*Corresponding author for this work

Research output: Contribution to journalArticle

4 Citations (Scopus)
3 Downloads (Pure)

Abstract

The extent to which genotypic variation at a priori identified candidate genes can explain variation in complex phenotypes is a major debate in evolutionary biology. Whereas some high-profile genes such as the MHC or MC1R clearly do account for variation in ecologically relevant characters, many complex phenotypes such as response to parasite infection may well be underpinned by a large number of genes, each of small and effectively undetectable effect. Here, we characterize a suite of novel candidate genes for variation in gastrointestinal nematode (Trichostrongylus tenuis) burden among red grouse (Lagopus lagopus scotica) individuals across a network of moors in north-east Scotland. We test for associations between parasite load and genotypic variation in twelve genes previously identified to be differentially expressed in experimentally infected red grouse or genetically differentiated among red grouse populations with overall different parasite loads. These genes are associated with a broad physiological response including immune system processes. Based on individual-level generalized linear models, genotypic variants in nine genes were significantly associated with parasite load, with effect sizes accounting for differences of 514-666 worms per bird. All but one of these variants were synonymous or untranslated, suggesting that these may be linked to protein-coding variants or affect regulatory processes. In contrast, population-level analyses revealed few and inconsistent associations with parasite load, and little evidence of signatures of natural selection. We discuss the broader significance of these contrasting results in the context of the utility of population genomics and landscape genomics approaches in detecting adaptive genomic signatures.

Original languageEnglish
Pages (from-to)807-825
Number of pages19
JournalJournal of Evolutionary Biology
Volume28
Issue number4
Early online date20 Mar 2015
DOIs
Publication statusPublished - Apr 2015

Keywords

  • candidate genes
  • complex phenotypes
  • genetic architecture
  • infinitesimal theory
  • large-effect polymorphisms
  • parasite susceptibility
  • lagopus-lagopus-scoticus
  • male red grouse
  • major histocompatibility complex
  • generalized estimating equations
  • waterflea daphnia-magna
  • expressed sequence tags
  • Columbia river-basin
  • trichostrongylus-tenuis
  • linkage disequilibrium
  • phenotypic plasticity

Cite this

@article{1df9436a3e774a3ca6c4c5d582e82c38,
title = "Digging for gold nuggets: uncovering novel candidate genes for variation in gastrointestinal nematode burden in a wild bird species",
abstract = "The extent to which genotypic variation at a priori identified candidate genes can explain variation in complex phenotypes is a major debate in evolutionary biology. Whereas some high-profile genes such as the MHC or MC1R clearly do account for variation in ecologically relevant characters, many complex phenotypes such as response to parasite infection may well be underpinned by a large number of genes, each of small and effectively undetectable effect. Here, we characterize a suite of novel candidate genes for variation in gastrointestinal nematode (Trichostrongylus tenuis) burden among red grouse (Lagopus lagopus scotica) individuals across a network of moors in north-east Scotland. We test for associations between parasite load and genotypic variation in twelve genes previously identified to be differentially expressed in experimentally infected red grouse or genetically differentiated among red grouse populations with overall different parasite loads. These genes are associated with a broad physiological response including immune system processes. Based on individual-level generalized linear models, genotypic variants in nine genes were significantly associated with parasite load, with effect sizes accounting for differences of 514-666 worms per bird. All but one of these variants were synonymous or untranslated, suggesting that these may be linked to protein-coding variants or affect regulatory processes. In contrast, population-level analyses revealed few and inconsistent associations with parasite load, and little evidence of signatures of natural selection. We discuss the broader significance of these contrasting results in the context of the utility of population genomics and landscape genomics approaches in detecting adaptive genomic signatures.",
keywords = "candidate genes, complex phenotypes, genetic architecture, infinitesimal theory, large-effect polymorphisms, parasite susceptibility, lagopus-lagopus-scoticus, male red grouse, major histocompatibility complex, generalized estimating equations, waterflea daphnia-magna, expressed sequence tags, Columbia river-basin, trichostrongylus-tenuis, linkage disequilibrium, phenotypic plasticity",
author = "Wenzel, {M. A.} and Piertney, {S. B.}",
note = "Acknowledgements This study was funded by a BBSRC studentship (MAWenzel) and NERC grants NE/H00775X/1 and NE/D000602/1 (SB Piertney). The authors are grateful to Marianne James, Mario Roder and Keliya Bai for field-work assistance, Lucy M.I. Webster and Steve Paterson for help during prior development of genetic markers,Heather Ritchie for helpful comments on manuscript drafts and all estate owners, factors and keepers for access to field sites, most particularly MJ Taylor and Mike Nisbet (Airlie), Neil Brown (Allargue), RR Gledson and David Scrimgeour (Delnadamph), Andrew Salvesen and John Hay (Dinnet), Stuart Young and Derek Calder (Edinglassie), Kirsty Donald and DavidBusfield (Glen Dye), Neil Hogbin and Ab Taylor (Glen Muick), Alistair Mitchell (Glenlivet), Simon Blackett, Jim Davidson and Liam Donald (Invercauld), Richard Cooke and Fred Taylor (Invermark), Shaila Rao and Christopher Murphy (Mar Lodge), and Ralph Peters and Philip Astor (Tillypronie)",
year = "2015",
month = "4",
doi = "10.1111/jeb.12614",
language = "English",
volume = "28",
pages = "807--825",
journal = "Journal of Evolutionary Biology",
issn = "1010-061X",
publisher = "Wiley-Blackwell",
number = "4",

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T1 - Digging for gold nuggets

T2 - uncovering novel candidate genes for variation in gastrointestinal nematode burden in a wild bird species

AU - Wenzel, M. A.

AU - Piertney, S. B.

N1 - Acknowledgements This study was funded by a BBSRC studentship (MAWenzel) and NERC grants NE/H00775X/1 and NE/D000602/1 (SB Piertney). The authors are grateful to Marianne James, Mario Roder and Keliya Bai for field-work assistance, Lucy M.I. Webster and Steve Paterson for help during prior development of genetic markers,Heather Ritchie for helpful comments on manuscript drafts and all estate owners, factors and keepers for access to field sites, most particularly MJ Taylor and Mike Nisbet (Airlie), Neil Brown (Allargue), RR Gledson and David Scrimgeour (Delnadamph), Andrew Salvesen and John Hay (Dinnet), Stuart Young and Derek Calder (Edinglassie), Kirsty Donald and DavidBusfield (Glen Dye), Neil Hogbin and Ab Taylor (Glen Muick), Alistair Mitchell (Glenlivet), Simon Blackett, Jim Davidson and Liam Donald (Invercauld), Richard Cooke and Fred Taylor (Invermark), Shaila Rao and Christopher Murphy (Mar Lodge), and Ralph Peters and Philip Astor (Tillypronie)

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N2 - The extent to which genotypic variation at a priori identified candidate genes can explain variation in complex phenotypes is a major debate in evolutionary biology. Whereas some high-profile genes such as the MHC or MC1R clearly do account for variation in ecologically relevant characters, many complex phenotypes such as response to parasite infection may well be underpinned by a large number of genes, each of small and effectively undetectable effect. Here, we characterize a suite of novel candidate genes for variation in gastrointestinal nematode (Trichostrongylus tenuis) burden among red grouse (Lagopus lagopus scotica) individuals across a network of moors in north-east Scotland. We test for associations between parasite load and genotypic variation in twelve genes previously identified to be differentially expressed in experimentally infected red grouse or genetically differentiated among red grouse populations with overall different parasite loads. These genes are associated with a broad physiological response including immune system processes. Based on individual-level generalized linear models, genotypic variants in nine genes were significantly associated with parasite load, with effect sizes accounting for differences of 514-666 worms per bird. All but one of these variants were synonymous or untranslated, suggesting that these may be linked to protein-coding variants or affect regulatory processes. In contrast, population-level analyses revealed few and inconsistent associations with parasite load, and little evidence of signatures of natural selection. We discuss the broader significance of these contrasting results in the context of the utility of population genomics and landscape genomics approaches in detecting adaptive genomic signatures.

AB - The extent to which genotypic variation at a priori identified candidate genes can explain variation in complex phenotypes is a major debate in evolutionary biology. Whereas some high-profile genes such as the MHC or MC1R clearly do account for variation in ecologically relevant characters, many complex phenotypes such as response to parasite infection may well be underpinned by a large number of genes, each of small and effectively undetectable effect. Here, we characterize a suite of novel candidate genes for variation in gastrointestinal nematode (Trichostrongylus tenuis) burden among red grouse (Lagopus lagopus scotica) individuals across a network of moors in north-east Scotland. We test for associations between parasite load and genotypic variation in twelve genes previously identified to be differentially expressed in experimentally infected red grouse or genetically differentiated among red grouse populations with overall different parasite loads. These genes are associated with a broad physiological response including immune system processes. Based on individual-level generalized linear models, genotypic variants in nine genes were significantly associated with parasite load, with effect sizes accounting for differences of 514-666 worms per bird. All but one of these variants were synonymous or untranslated, suggesting that these may be linked to protein-coding variants or affect regulatory processes. In contrast, population-level analyses revealed few and inconsistent associations with parasite load, and little evidence of signatures of natural selection. We discuss the broader significance of these contrasting results in the context of the utility of population genomics and landscape genomics approaches in detecting adaptive genomic signatures.

KW - candidate genes

KW - complex phenotypes

KW - genetic architecture

KW - infinitesimal theory

KW - large-effect polymorphisms

KW - parasite susceptibility

KW - lagopus-lagopus-scoticus

KW - male red grouse

KW - major histocompatibility complex

KW - generalized estimating equations

KW - waterflea daphnia-magna

KW - expressed sequence tags

KW - Columbia river-basin

KW - trichostrongylus-tenuis

KW - linkage disequilibrium

KW - phenotypic plasticity

U2 - 10.1111/jeb.12614

DO - 10.1111/jeb.12614

M3 - Article

VL - 28

SP - 807

EP - 825

JO - Journal of Evolutionary Biology

JF - Journal of Evolutionary Biology

SN - 1010-061X

IS - 4

ER -