The role of parasite-driven selection in shaping landscape genomic structure in red grouse (Lagopus lagopus scotica)

Marius A. Wenzel, Alex Douglas, Marianne C. James, Steve M. Redpath, Stuart B. Piertney

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Abstract

Landscape genomics promises to provide novel insights into how neutral and adaptive processes shape genome-wide variation within and among populations. However, there has been little emphasis on examining whether individual-based phenotype–genotype relationships derived from approaches such as genome-wide association (GWAS) manifest themselves as a population-level signature of selection in a landscape context. The two may prove irreconcilable as individual-level patterns become diluted by high levels of gene flow and complex phenotypic or environmental heterogeneity. We illustrate this issue with a case study that examines the role of the highly prevalent gastrointestinal nematode Trichostrongylus tenuis in shaping genomic signatures of selection in red grouse (Lagopus lagopus scotica). Individual-level GWAS involving 384 SNPs has previously identified five SNPs that explain variation in T. tenuis burden. Here, we examine whether these same SNPs display population-level relationships between T. tenuis burden and genetic structure across a small-scale landscape of 21 sites with heterogeneous parasite pressure. Moreover, we identify adaptive SNPs showing signatures of directional selection using FST outlier analysis and relate population- and individual-level patterns of multilocus neutral and adaptive genetic structure to T. tenuis burden. The five candidate SNPs for parasite-driven selection were neither associated with T. tenuis burden on a population level, nor under directional selection. Similarly, there was no evidence of parasite-driven selection in SNPs identified as candidates for directional selection. We discuss these results in the context of red grouse ecology and highlight the broader consequences for the utility of landscape genomics approaches for identifying signatures of selection.
Original languageEnglish
Pages (from-to)324-341
Number of pages18
JournalMolecular Ecology
Volume25
Issue number1
Early online date12 Dec 2015
DOIs
Publication statusPublished - Jan 2016

Fingerprint

Trichostrongylus tenuis
Lagopus lagopus
Lagopus lagopus scoticus
Single Nucleotide Polymorphism
genomics
parasite
Parasites
parasites
Population
Genetic Structures
Genome
genome
Genomics
genetic structure
Trichostrongylus
gastrointestinal nematodes
Gene Flow
Ecology
gene flow
case studies

Keywords

  • landscape genomics
  • Population genomics
  • FST outliers
  • natural selection
  • parasites

Cite this

The role of parasite-driven selection in shaping landscape genomic structure in red grouse (Lagopus lagopus scotica). / Wenzel, Marius A.; Douglas, Alex; James, Marianne C.; Redpath, Steve M.; Piertney, Stuart B.

In: Molecular Ecology, Vol. 25, No. 1, 01.2016, p. 324-341.

Research output: Contribution to journalArticle

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abstract = "Landscape genomics promises to provide novel insights into how neutral and adaptive processes shape genome-wide variation within and among populations. However, there has been little emphasis on examining whether individual-based phenotype–genotype relationships derived from approaches such as genome-wide association (GWAS) manifest themselves as a population-level signature of selection in a landscape context. The two may prove irreconcilable as individual-level patterns become diluted by high levels of gene flow and complex phenotypic or environmental heterogeneity. We illustrate this issue with a case study that examines the role of the highly prevalent gastrointestinal nematode Trichostrongylus tenuis in shaping genomic signatures of selection in red grouse (Lagopus lagopus scotica). Individual-level GWAS involving 384 SNPs has previously identified five SNPs that explain variation in T. tenuis burden. Here, we examine whether these same SNPs display population-level relationships between T. tenuis burden and genetic structure across a small-scale landscape of 21 sites with heterogeneous parasite pressure. Moreover, we identify adaptive SNPs showing signatures of directional selection using FST outlier analysis and relate population- and individual-level patterns of multilocus neutral and adaptive genetic structure to T. tenuis burden. The five candidate SNPs for parasite-driven selection were neither associated with T. tenuis burden on a population level, nor under directional selection. Similarly, there was no evidence of parasite-driven selection in SNPs identified as candidates for directional selection. We discuss these results in the context of red grouse ecology and highlight the broader consequences for the utility of landscape genomics approaches for identifying signatures of selection.",
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note = "Acknowledgements This study was funded by a BBSRC studentship (MAW) and NERC grants NE/H00775X/1 and NE/D000602/1 (SBP). The authors are grateful to Mario R{\"o}der and Keliya Bai for fieldwork assistance, 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 David Busfield (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). S.B.P. and S.M.R. conceived and designed the study. M.A.W. performed field and laboratory work. A.D. and M.C.J. developed SNP markers. M.A.W. analysed the data. M.A.W. and S.B.P. wrote the manuscript.",
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N1 - Acknowledgements This study was funded by a BBSRC studentship (MAW) and NERC grants NE/H00775X/1 and NE/D000602/1 (SBP). The authors are grateful to Mario Röder and Keliya Bai for fieldwork assistance, 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 David Busfield (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). S.B.P. and S.M.R. conceived and designed the study. M.A.W. performed field and laboratory work. A.D. and M.C.J. developed SNP markers. M.A.W. analysed the data. M.A.W. and S.B.P. wrote the manuscript.

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N2 - Landscape genomics promises to provide novel insights into how neutral and adaptive processes shape genome-wide variation within and among populations. However, there has been little emphasis on examining whether individual-based phenotype–genotype relationships derived from approaches such as genome-wide association (GWAS) manifest themselves as a population-level signature of selection in a landscape context. The two may prove irreconcilable as individual-level patterns become diluted by high levels of gene flow and complex phenotypic or environmental heterogeneity. We illustrate this issue with a case study that examines the role of the highly prevalent gastrointestinal nematode Trichostrongylus tenuis in shaping genomic signatures of selection in red grouse (Lagopus lagopus scotica). Individual-level GWAS involving 384 SNPs has previously identified five SNPs that explain variation in T. tenuis burden. Here, we examine whether these same SNPs display population-level relationships between T. tenuis burden and genetic structure across a small-scale landscape of 21 sites with heterogeneous parasite pressure. Moreover, we identify adaptive SNPs showing signatures of directional selection using FST outlier analysis and relate population- and individual-level patterns of multilocus neutral and adaptive genetic structure to T. tenuis burden. The five candidate SNPs for parasite-driven selection were neither associated with T. tenuis burden on a population level, nor under directional selection. Similarly, there was no evidence of parasite-driven selection in SNPs identified as candidates for directional selection. We discuss these results in the context of red grouse ecology and highlight the broader consequences for the utility of landscape genomics approaches for identifying signatures of selection.

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KW - landscape genomics

KW - Population genomics

KW - FST outliers

KW - natural selection

KW - parasites

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JF - Molecular Ecology

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