Replicated analysis of the genetic architecture of quantitative traits in two wild great tit populations

Anna W. Santure*, Jocelyn Poissant, Isabelle De Cauwer, Kees van Oers, Matthew R. Robinson, John L. Quinn, M.A.M. Groenen, M.E. Visser, Ben C. Sheldon, Jon Slate

*Corresponding author for this work

Research output: Contribution to journalArticleAcademicpeer-review

26 Citations (Scopus)

Abstract

Currently, there is much debate on the genetic architecture of quantitative traits in wild populations. Is trait variation influenced by many genes of small effect or by a few genes of major effect? Where is additive genetic variation located in the genome? Do the same loci cause similar phenotypic variation in different populations? Great tits (Parus major) have been studied extensively in long-term studies across Europe and consequently are considered an ecological 'model organism'. Recently, genomic resources have been developed for the great tit, including a custom SNP chip and genetic linkage map. In this study, we used a suite of approaches to investigate the genetic architecture of eight quantitative traits in two long-term study populations of great tits - one in the Netherlands and the other in the United Kingdom. Overall, we found little evidence for the presence of genes of large effects in either population. Instead, traits appeared to be influenced by many genes of small effect, with conservative estimates of the number of contributing loci ranging from 31 to 310. Despite concordance between population-specific heritabilities, we found no evidence for the presence of loci having similar effects in both populations. While population-specific genetic architectures are possible, an undetected shared architecture cannot be rejected because of limited power to map loci of small and moderate effects. This study is one of few examples of genetic architecture analysis in replicated wild populations and highlights some of the challenges and limitations researchers will face when attempting similar molecular quantitative genetic studies in free-living populations.

Original languageEnglish
Pages (from-to)6148-6162
JournalMolecular Ecology
Volume24
Issue number24
DOIs
Publication statusPublished - 2015

Fingerprint

quantitative traits
genetic techniques and protocols
Population
gene
wild population
loci
Genes
heritability
Genetic Linkage
analysis
effect
genetic variation
genomics
Population Genetics
genes
Parus major
genome
quantitative genetics
Netherlands
major genes

Keywords

  • chromosome partitioning
  • genome-wide association
  • genomics
  • GWAS
  • QTL mapping
  • quantitative genetics

Cite this

Santure, A. W., Poissant, J., De Cauwer, I., van Oers, K., Robinson, M. R., Quinn, J. L., ... Slate, J. (2015). Replicated analysis of the genetic architecture of quantitative traits in two wild great tit populations. Molecular Ecology, 24(24), 6148-6162. https://doi.org/10.1111/mec.13452
Santure, Anna W. ; Poissant, Jocelyn ; De Cauwer, Isabelle ; van Oers, Kees ; Robinson, Matthew R. ; Quinn, John L. ; Groenen, M.A.M. ; Visser, M.E. ; Sheldon, Ben C. ; Slate, Jon. / Replicated analysis of the genetic architecture of quantitative traits in two wild great tit populations. In: Molecular Ecology. 2015 ; Vol. 24, No. 24. pp. 6148-6162.
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Santure, AW, Poissant, J, De Cauwer, I, van Oers, K, Robinson, MR, Quinn, JL, Groenen, MAM, Visser, ME, Sheldon, BC & Slate, J 2015, 'Replicated analysis of the genetic architecture of quantitative traits in two wild great tit populations', Molecular Ecology, vol. 24, no. 24, pp. 6148-6162. https://doi.org/10.1111/mec.13452

Replicated analysis of the genetic architecture of quantitative traits in two wild great tit populations. / Santure, Anna W.; Poissant, Jocelyn; De Cauwer, Isabelle; van Oers, Kees; Robinson, Matthew R.; Quinn, John L.; Groenen, M.A.M.; Visser, M.E.; Sheldon, Ben C.; Slate, Jon.

In: Molecular Ecology, Vol. 24, No. 24, 2015, p. 6148-6162.

Research output: Contribution to journalArticleAcademicpeer-review

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AU - Santure, Anna W.

AU - Poissant, Jocelyn

AU - De Cauwer, Isabelle

AU - van Oers, Kees

AU - Robinson, Matthew R.

AU - Quinn, John L.

AU - Groenen, M.A.M.

AU - Visser, M.E.

AU - Sheldon, Ben C.

AU - Slate, Jon

PY - 2015

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N2 - Currently, there is much debate on the genetic architecture of quantitative traits in wild populations. Is trait variation influenced by many genes of small effect or by a few genes of major effect? Where is additive genetic variation located in the genome? Do the same loci cause similar phenotypic variation in different populations? Great tits (Parus major) have been studied extensively in long-term studies across Europe and consequently are considered an ecological 'model organism'. Recently, genomic resources have been developed for the great tit, including a custom SNP chip and genetic linkage map. In this study, we used a suite of approaches to investigate the genetic architecture of eight quantitative traits in two long-term study populations of great tits - one in the Netherlands and the other in the United Kingdom. Overall, we found little evidence for the presence of genes of large effects in either population. Instead, traits appeared to be influenced by many genes of small effect, with conservative estimates of the number of contributing loci ranging from 31 to 310. Despite concordance between population-specific heritabilities, we found no evidence for the presence of loci having similar effects in both populations. While population-specific genetic architectures are possible, an undetected shared architecture cannot be rejected because of limited power to map loci of small and moderate effects. This study is one of few examples of genetic architecture analysis in replicated wild populations and highlights some of the challenges and limitations researchers will face when attempting similar molecular quantitative genetic studies in free-living populations.

AB - Currently, there is much debate on the genetic architecture of quantitative traits in wild populations. Is trait variation influenced by many genes of small effect or by a few genes of major effect? Where is additive genetic variation located in the genome? Do the same loci cause similar phenotypic variation in different populations? Great tits (Parus major) have been studied extensively in long-term studies across Europe and consequently are considered an ecological 'model organism'. Recently, genomic resources have been developed for the great tit, including a custom SNP chip and genetic linkage map. In this study, we used a suite of approaches to investigate the genetic architecture of eight quantitative traits in two long-term study populations of great tits - one in the Netherlands and the other in the United Kingdom. Overall, we found little evidence for the presence of genes of large effects in either population. Instead, traits appeared to be influenced by many genes of small effect, with conservative estimates of the number of contributing loci ranging from 31 to 310. Despite concordance between population-specific heritabilities, we found no evidence for the presence of loci having similar effects in both populations. While population-specific genetic architectures are possible, an undetected shared architecture cannot be rejected because of limited power to map loci of small and moderate effects. This study is one of few examples of genetic architecture analysis in replicated wild populations and highlights some of the challenges and limitations researchers will face when attempting similar molecular quantitative genetic studies in free-living populations.

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KW - genome-wide association

KW - genomics

KW - GWAS

KW - QTL mapping

KW - quantitative genetics

U2 - 10.1111/mec.13452

DO - 10.1111/mec.13452

M3 - Article

VL - 24

SP - 6148

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JO - Molecular Ecology

JF - Molecular Ecology

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IS - 24

ER -