Can balancing selection on MHC loci counteract genetic drift in small fragmented populations of black grouse?

The ability of natural populations to adapt to new environmental conditions is crucial for their survival and partly determined by the standing genetic variation in each population. Populations with higher genetic diversity are more likely to contain individuals that are better adapted to new circumstances than populations with lower genetic diversity. Here, we use both neutral and major histocompatibility complex (MHC) markers to test whether small and highly fragmented populations hold lower genetic diversity than large ones. We use black grouse as it is distributed across Europe and found in populations with varying degrees of isolation and size. We sampled 11 different populations; five continuous, three isolated, and three small and isolated. We tested patterns of genetic variation in these populations using three different types of genetic markers: nine microsatellites and 21 single nucleotide polymorphisms (SNPs) which both were found to be neutral, and two functional MHC genes that are presumably under selection. The small isolated populations displayed significantly lower neutral genetic diversity compared to continuous populations. A similar trend, but not as pronounced, was found for genotypes at MHC class II loci. Populations were less divergent at MHC genes compared to neutral markers. Measures of genetic diversity and population genetic structure were positively correlated among microsatellites and SNPs, but none of them were correlated to MHC when comparing all populations. Our results suggest that balancing selection at MHC loci does not counteract the power of genetic drift when populations get small and fragmented.

• Publication year

  2012

• Venue

  Ecology and Evolution

• Publication date

  2012-02-01

• Fields of study

  Biology, Medicine, Environmental Science

• Identifiers
  DOI 10.1002/ece3.86PMID 22423328PMCID 3298947
• External record

  Open on Semantic Scholar

• Source metadata

  Semantic Scholar, PubMed

• No claims are published for this paper.

• No concepts are published for this paper.

• Amplification success of multilocus genotypes from feathers found in the field compared with feathers obtained from shot birds

  2012cited by this paper
• GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research—an update

  2012cited by this paper
• Genotyping of black grouse MHC class II B using reference Strand-Mediated Conformational Analysis (RSCA)

  2011cited by this paper
• MHC diversity in bottlenecked populations: a simulation model

  2011cited by this paper
• Genetic structure among black grouse in Britain: implications for designing conservation units

  2011cited by this paper
• Disentangling the roles of natural selection and genetic drift in shaping variation at MHC immunity genes

  2011cited by this paper
• Multi-locus inference of population structure: a comparison between single nucleotide polymorphisms and microsatellites

  2011cited by this paper
• Rapid loss of MHC class II variation in a bottlenecked population is explained by drift and loss of copy number variation

  2011cited by this paper
• MHC‐dependent survival in a wild population: evidence for hidden genetic benefits gained through extra‐pair fertilizations

  2010cited by this paper
• Major histocompatibility complex variation and age‐specific endoparasite load in subadult European rabbits

  2010cited by this paper
• MHC class I and MHC class II DRB gene variability in wild and captive Bengal tigers (Panthera tigris tigris)

  2010cited by this paper
• Selection at the MHC class IIB locus across guppy (Poecilia reticulata) populations

  2010cited by this paper
• Genetic diversity and differentiation at MHC genes in island populations of tuatara (Sphenodon spp.)

  2010influential reference
• MHC genetic structure and divergence across populations of Chinook salmon (Oncorhynchus tshawytscha)

  2010cited by this paper
• MHC heterozygosity and survival in red junglefowl

  2010cited by this paper
• How pathogens drive genetic diversity: MHC, mechanisms and misunderstandings

  2010cited by this paper
• smogd: software for the measurement of genetic diversity

  2010influential reference
• User ’ s Guide for Program SPADE ( Species Prediction And Diversity Estimation )

  2010cited by this paper
• A new theory of MHC evolution: beyond selection on the immune genes

  2009cited by this paper
• Does reduced MHC diversity decrease viability of vertebrate populations?

  2009cited by this paper
• Highly Endangered African Wild Dogs (Lycaon pictus) Lack Variation at the Major Histocompatibility Complex

  2009cited by this paper
• Collaboration for Environmental Evidence Systematic Review No . 65 DOES REDUCED MHC DIVERSITY DECREASE VIABILITY OF VERTEBRATE POPULATIONS ?

  2009influential reference
• Genetic studies of black grouse with special reference to conservation biology : a review

  2009influential reference
• Evolutionary Conservation Genetics

  2009influential reference
• To what extent do microsatellite markers reflect genome‐wide genetic diversity in natural populations?

  2008cited by this paper
• GST and its relatives do not measure differentiation

  2008influential reference
• A Genome-Scan Method to Identify Selected Loci Appropriate for Both Dominant and Codominant Markers: A Bayesian Perspective

  2008influential reference
• A multilocus assay reveals high nucleotide diversity and limited differentiation among Scandinavian willow grouse (Lagopus lagopus)

  2008cited by this paper
• Genetic impoverishment of the last black grouse (Tetrao tetrix) population in the Netherlands: detectable only with a reference from the past

  2008influential reference
• A new theory of MHC evolution: beyond selection on the immune genes.

  2008cited by this paper
• Temporal and spatial analyses disclose consequences of habitat fragmentation on the genetic diversity in capercaillie (Tetrao urogallus)

  2008cited by this paper
• LOSITAN: A workbench to detect molecular adaptation based on a Fst-outlier method

  2008influential reference
• Prediction of Protein-protein Interactions on the Basis of Evolutionary Conservation of Protein Functions

  2007influential reference
• Transmission of a fatal clonal tumor by biting occurs due to depleted MHC diversity in a threatened carnivorous marsupial

  2007cited by this paper
• Spatial pattern of MHC class II variation in the great snipe (Gallinago media)

  2007cited by this paper
• The Mhc class II of the Black grouse (Tetrao tetrix) consists of low numbers of B and Y genes with variable diversity and expression

  2007influential reference
• Rapidly advancing laying date in a seabird and the changing advantage of early reproduction.

  2006cited by this paper
• The evolutionary ecology of the major histocompatibility complex

  2006cited by this paper
• Birds in Europe: Population Estimates, Trends and Conservation Status

  2006cited by this paper
• Major histocompatibility complex class II variation in the giant panda (Ailuropoda melanoleuca)

  2006cited by this paper
• Genetic variability in European black grouse (Tetrao tetrix)

  2006influential reference
• genalex 6: genetic analysis in Excel. Population genetic software for teaching and research

  2006cited by this paper
• Site‐specific genetic divergence in parallel hybrid zones suggests nonallopatric evolution of reproductive barriers

  2006cited by this paper
• BALANCING SELECTION, RANDOM GENETIC DRIFT, AND GENETIC VARIATION AT THE MAJOR HISTOCOMPATIBILITY COMPLEX IN TWO WILD POPULATIONS OF GUPPIES (POECILIA RETICULATA)

  2006cited by this paper
• MAJOR HISTOCOMPATIBILITY ALLELES ASSOCIATED WITH LOCAL RESISTANCE TO MALARIA IN A PASSERINE

  2006cited by this paper
• Kompendium der Vögel Mitteleuropas

  2005cited by this paper
• Streams over mountains: influence of riparian connectivity on gene flow in the Pacific jumping mouse (Zapus trinotatus)

  2005cited by this paper
• MHC diversity and the association to nematode parasitism in the yellow‐necked mouse (Apodemus flavicollis)

  2005cited by this paper
• An overlooked DNA source for non‐invasive genetic analysis in birds

  2005cited by this paper
• Das Kompendium der Vögel Mitteleuropas. Band I Nonpasseriformes

  2005cited by this paper
• Associations between malaria and MHC genes in a migratory songbird

  2005cited by this paper
• Arlequin (version 3.0): An integrated software package for population genetics data analysis

  2005cited by this paper
• Does Inbreeding and Loss of Genetic Diversity Decrease Disease Resistance?

  2004cited by this paper
• MHC class I typing in a songbird with numerous loci and high polymorphism using motif-specific PCR and DGGE

  2004cited by this paper
• Birds in Europe : population estimates, trends and conservation status

  2004cited by this paper
• Most species are not driven to extinction before genetic factors impact them.

  2004cited by this paper
• Identifying adaptive genetic divergence among populations from genome scans

  2004influential reference
• TERMINAL INVESTMENT INDUCED BY IMMUNE CHALLENGE AND FITNESS TRAITS ASSOCIATED WITH MAJOR HISTOCOMPATIBILITY COMPLEX IN THE HOUSE SPARROW

  2004cited by this paper
• Does heterozygosity estimate inbreeding in real populations?

  2004cited by this paper
• Correlation between Fitness and Genetic Diversity

  2003cited by this paper
• PERSPECTIVE: DETECTING ADAPTIVE MOLECULAR POLYMORPHISM: LESSONS FROM THE MHC

  2003cited by this paper
• Low Potential for Climatic Stress Adaptation in a Rainforest Drosophila Species

  2003cited by this paper
• Rapid evolutionary dynamics and disease threats to biodiversity

  2003influential reference
• Morris, W. F., and D. F. Doak. 2003. Quantitative Conservation Biology: Theory and Practice of Population Viability Analysis. Sinauer Associates, Sunderland, Massachusetts, USA

  2003cited by this paper
• Neutral DNA markers fail to detect genetic divergence in an ecologically important trait

  2003cited by this paper
• Sampling within the genome for measuring within‐population diversity: trade‐offs between markers

  2002cited by this paper
• Quantitative conservation biology : theory and practice of population viability analysis

  2002cited by this paper
• SNPstream UHT: ultra-high throughput SNP genotyping for pharmacogenomics and drug discovery.

  2002cited by this paper
• Estimating F-statistics.

  2002cited by this paper
• Capercaillie in the Alps: genetic evidence of metapopulation structure and population decline

  2002cited by this paper
• gimlet: a computer program for analysing genetic individual identification data

  2002cited by this paper
• HOW CLOSELY CORRELATED ARE MOLECULAR AND QUANTITATIVE MEASURES OF GENETIC VARIATION? A META‐ANALYSIS

  2001cited by this paper
• When does conservation genetics matter?

  2001cited by this paper
• Conservation genetics : where are we now ?

  2001cited by this paper
• Polymorphic microsatellite DNA markers in black grouse (Tetrao tetrix)

  2001cited by this paper
• Grouse : status survey and conservation action plan 2006-2010

  2000cited by this paper
• The effect of subdivision on variation at multi-allelic loci under balancing selection.

  2000cited by this paper
• Genetic correlates of spatial population structure in central European capercaillie Tetrao urogallus and black grouse T. tetrix: a project in progress

  2000cited by this paper
• Mutation detection and typing of polymorphic loci through double-strand conformation analysis

  1998cited by this paper
• Genetic differentiation and estimation of gene flow from F-statistics under isolation by distance.

  1997cited by this paper
• The effects of local selection, balanced polymorphism and background selection on equilibrium patterns of genetic diversity in subdivided populations.

  1997cited by this paper
• Mating structure and nestmate relatedness in a communal bee, Andrena jacobi (Hymenoptera, Andrenidae), using microsatellites

  1996cited by this paper
• GENETIX 4.05, logiciel sous Windows TM pour la génétique des populations.

  1996influential reference
• Evaluating loci for use in the genetic analysis of population structure

  1996influential reference
• FSTAT (Version 1.2): A Computer Program to Calculate F-Statistics

  1995influential reference
• GENEPOP (version 1.2): population genetic software for exact tests and ecumenicism

  1995cited by this paper
• Directions in conservation biology

  1994cited by this paper
• POPULATION GENETIC CONSEQUENCES OF SMALL POPULATION SIZE: Implications for Plant Conservation

  1993cited by this paper
• A simple genealogical structure of strongly balanced allelic lines and trans-species evolution of polymorphism.

  1990influential reference
• Genetics and demography in biological conservation.

  1988cited by this paper
• ESTIMATING F‐STATISTICS FOR THE ANALYSIS OF POPULATION STRUCTURE

  1984influential reference
• The neutral theory of molecular evolution.

  1983cited by this paper
• The Authors

  1977cited by this paper

• MHC Diversity Across Time and Space

  2025cites this paper
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  2025cites this paper
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  2023influential citation
• Selection and demography drive range-wide patterns of MHC-DRB variation in mule deer

  2022cites this paper
• Effects of hunting on genetic diversity, inbreeding and dispersal in Finnish black grouse (Lyrurus tetrix)

  2022cites this paper
• Phylogenetically under‐dispersed gut microbiomes are not correlated with host genomic heterozygosity in a genetically diverse reptile community

  2022cites this paper
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  2022cites this paper
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  2022cites this paper
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  2021cites this paper
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  2021cites this paper
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  2021cites this paper
• Urbanization processes drive divergence at the major histocompatibility complex in a common waterbird

  2021cites this paper
• Mating system is correlated with immunogenetic diversity in sympatric species of Peromyscine mice

  2020cites this paper
• Wetter climates select for higher immune gene diversity in resident, but not migratory, songbirds

  2020cites this paper
• Habitat fragmentation differentially shapes neutral and immune gene variation in a tropical bird species

  2020cites this paper
• Major histocompatibility complex variation is similar in little brown bats before and after white‐nose syndrome outbreak

  2020cites this paper
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  2019cites this paper
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  2019cites this paper
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  2019cites this paper
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  2019cites this paper
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  2019cites this paper
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  2018cites this paper
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  2018cites this paper
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  2018cites this paper
• Differentiation measures for conservation genetics

  2018cites this paper
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  2018cites this paper
• Archipelagos of the Anthropocene: rapid and extensive differentiation of native terrestrial vertebrates in a single metropolis

  2017cites this paper
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  2017cites this paper
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  2017cites this paper
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  2017cites this paper
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  2017cites this paper
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  2017cites this paper
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  2017cites this paper
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  2016cites this paper
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  2014cites this paper
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  2014cites this paper
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  2014cites this paper
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  2014cites this paper
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  2014cites this paper
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  2014influential citation
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  2013cites this paper
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  2013cites this paper
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  2012cites this paper
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  2012cites this paper