Spatio-temporal variation in the strength and mode of selection acting on major histocompatibility complex diversity in water vole (Arvicola terrestris) metapopulations

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Abstract

Patterns of spatio-temporal genetic variation at a class II major histocompatibility complex (MHC) locus and multiple microsatellite loci were analysed within and between three water vole metapopulations in Scotland, UK. Comparisons of MHC and microsatellite spatial genetic differentiation, based on standardised tests between two demographically asynchronous zones within a metapopulation, suggested that spatial MHC variation was affected by balancing selection, directional selection and random genetic drift, but that the relative effects of these microevolutionary forces vary temporally. At the metapopulation level, between-year differentiation for MHC loci was significantly correlated with that of microsatellites, signifying that neutral factors such as migration and drift were primarily responsible for overall temporal genetic change at the metapopulation scale. Between metapopulations, patterns of genetic differentiation implied that, at large spatial scales, MHC variation was primarily affected by directional selection and drift. Levels of MHC heterozygosity in excess of Hardy-Weinberg expectations were consistent with overdominant balancing selection operating on MHC variation within metapopulations. However, this effect was not constant among all samples, indicating temporal variation in the strength of selection relative to other factors. The results highlight the benefit of contrasting variation at MHC with neutral markers to separate the effects of stochastic and deterministic microevolutionary forces, and add to a growing body of evidence showing that the mode and relative strength of selection acting on MHC diversity varies both spatially and temporally.

Original languageEnglish
Pages (from-to)80-92
Number of pages13
JournalMolecular Ecology
Volume18
Issue number1
Early online date19 Dec 2008
DOIs
Publication statusPublished - Jan 2009

Keywords

  • drift
  • MHC
  • microsatellite
  • selection
  • SALMON ONCORHYNCHUS-TSHAWYTSCHA
  • GENETIC DIFFERENTIATION MEASURE
  • LIMITED MHC POLYMORPHISM
  • BALANCING SELECTION
  • POPULATION-STRUCTURE
  • NATURAL-SELECTION
  • MICROSATELLITE LOCI
  • MATING PREFERENCES
  • ATLANTIC SALMON
  • HETEROZYGOTE ADVANTAGE

Cite this

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title = "Spatio-temporal variation in the strength and mode of selection acting on major histocompatibility complex diversity in water vole (Arvicola terrestris) metapopulations",
abstract = "Patterns of spatio-temporal genetic variation at a class II major histocompatibility complex (MHC) locus and multiple microsatellite loci were analysed within and between three water vole metapopulations in Scotland, UK. Comparisons of MHC and microsatellite spatial genetic differentiation, based on standardised tests between two demographically asynchronous zones within a metapopulation, suggested that spatial MHC variation was affected by balancing selection, directional selection and random genetic drift, but that the relative effects of these microevolutionary forces vary temporally. At the metapopulation level, between-year differentiation for MHC loci was significantly correlated with that of microsatellites, signifying that neutral factors such as migration and drift were primarily responsible for overall temporal genetic change at the metapopulation scale. Between metapopulations, patterns of genetic differentiation implied that, at large spatial scales, MHC variation was primarily affected by directional selection and drift. Levels of MHC heterozygosity in excess of Hardy-Weinberg expectations were consistent with overdominant balancing selection operating on MHC variation within metapopulations. However, this effect was not constant among all samples, indicating temporal variation in the strength of selection relative to other factors. The results highlight the benefit of contrasting variation at MHC with neutral markers to separate the effects of stochastic and deterministic microevolutionary forces, and add to a growing body of evidence showing that the mode and relative strength of selection acting on MHC diversity varies both spatially and temporally.",
keywords = "drift, MHC, microsatellite, selection, SALMON ONCORHYNCHUS-TSHAWYTSCHA, GENETIC DIFFERENTIATION MEASURE, LIMITED MHC POLYMORPHISM, BALANCING SELECTION, POPULATION-STRUCTURE, NATURAL-SELECTION, MICROSATELLITE LOCI, MATING PREFERENCES, ATLANTIC SALMON, HETEROZYGOTE ADVANTAGE",
author = "Oliver, {Matthew Kenneth} and Xavier Lambin and Thomas Cornulier and Piertney, {Stuart Brannon}",
year = "2009",
month = "1",
doi = "10.1111/j.1365-294X.2008.04015.x",
language = "English",
volume = "18",
pages = "80--92",
journal = "Molecular Ecology",
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T1 - Spatio-temporal variation in the strength and mode of selection acting on major histocompatibility complex diversity in water vole (Arvicola terrestris) metapopulations

AU - Oliver, Matthew Kenneth

AU - Lambin, Xavier

AU - Cornulier, Thomas

AU - Piertney, Stuart Brannon

PY - 2009/1

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N2 - Patterns of spatio-temporal genetic variation at a class II major histocompatibility complex (MHC) locus and multiple microsatellite loci were analysed within and between three water vole metapopulations in Scotland, UK. Comparisons of MHC and microsatellite spatial genetic differentiation, based on standardised tests between two demographically asynchronous zones within a metapopulation, suggested that spatial MHC variation was affected by balancing selection, directional selection and random genetic drift, but that the relative effects of these microevolutionary forces vary temporally. At the metapopulation level, between-year differentiation for MHC loci was significantly correlated with that of microsatellites, signifying that neutral factors such as migration and drift were primarily responsible for overall temporal genetic change at the metapopulation scale. Between metapopulations, patterns of genetic differentiation implied that, at large spatial scales, MHC variation was primarily affected by directional selection and drift. Levels of MHC heterozygosity in excess of Hardy-Weinberg expectations were consistent with overdominant balancing selection operating on MHC variation within metapopulations. However, this effect was not constant among all samples, indicating temporal variation in the strength of selection relative to other factors. The results highlight the benefit of contrasting variation at MHC with neutral markers to separate the effects of stochastic and deterministic microevolutionary forces, and add to a growing body of evidence showing that the mode and relative strength of selection acting on MHC diversity varies both spatially and temporally.

AB - Patterns of spatio-temporal genetic variation at a class II major histocompatibility complex (MHC) locus and multiple microsatellite loci were analysed within and between three water vole metapopulations in Scotland, UK. Comparisons of MHC and microsatellite spatial genetic differentiation, based on standardised tests between two demographically asynchronous zones within a metapopulation, suggested that spatial MHC variation was affected by balancing selection, directional selection and random genetic drift, but that the relative effects of these microevolutionary forces vary temporally. At the metapopulation level, between-year differentiation for MHC loci was significantly correlated with that of microsatellites, signifying that neutral factors such as migration and drift were primarily responsible for overall temporal genetic change at the metapopulation scale. Between metapopulations, patterns of genetic differentiation implied that, at large spatial scales, MHC variation was primarily affected by directional selection and drift. Levels of MHC heterozygosity in excess of Hardy-Weinberg expectations were consistent with overdominant balancing selection operating on MHC variation within metapopulations. However, this effect was not constant among all samples, indicating temporal variation in the strength of selection relative to other factors. The results highlight the benefit of contrasting variation at MHC with neutral markers to separate the effects of stochastic and deterministic microevolutionary forces, and add to a growing body of evidence showing that the mode and relative strength of selection acting on MHC diversity varies both spatially and temporally.

KW - drift

KW - MHC

KW - microsatellite

KW - selection

KW - SALMON ONCORHYNCHUS-TSHAWYTSCHA

KW - GENETIC DIFFERENTIATION MEASURE

KW - LIMITED MHC POLYMORPHISM

KW - BALANCING SELECTION

KW - POPULATION-STRUCTURE

KW - NATURAL-SELECTION

KW - MICROSATELLITE LOCI

KW - MATING PREFERENCES

KW - ATLANTIC SALMON

KW - HETEROZYGOTE ADVANTAGE

U2 - 10.1111/j.1365-294X.2008.04015.x

DO - 10.1111/j.1365-294X.2008.04015.x

M3 - Article

VL - 18

SP - 80

EP - 92

JO - Molecular Ecology

JF - Molecular Ecology

SN - 0962-1083

IS - 1

ER -