Gene dynamics of toll-like receptor 4 through a population bottleneck in an insular population of water voles (Arvicola amphibius)

Martha K. Gavan*, Matthew K. Oliver, Alex Douglas, Stuart B. Piertney

*Corresponding author for this work

Research output: Contribution to journalArticle

3 Citations (Scopus)
5 Downloads (Pure)

Abstract

Understanding the extent to which diversity at immunologically important genes is reduced by demographic perturbations such as population bottlenecks, and the resulting consequences this has on individual fitness, is of fundamental importance for the effective management of genetic resources in natural populations. Toll-like receptors are key immunological genes with well-established links to fitness. Here, levels of allelic diversity and heterozygosity at the toll-like receptor 4 locus (Tlr4) were characterised across 280 water voles (Arvicola amphibius) from an isolated, island population in north west Scotland that went through a severe population bottleneck between 2004 and 2006 that eroded neutral microsatellite variation. Two functional Tlr4 alleles were resolved prior to the population crash at frequencies close to parity and an excess of heterozygote genotypes relative to Hardy-Weinberg expectations. Through the population bottleneck both alleles were retained with genotype frequencies conforming to Hardy-Weinberg expectations. Tlr4 genotype was significantly associated with gamasid mite, flea (Megabothris walkeri) and sheep tick larva (Ixodes ricinus) burdens among individuals, suggesting a mechanism through which parasite mediated selection could affect Tlr4 diversity. The results are examined with recourse to the extent that they are consistent with the effects of genetic drift and balancing selection, and their significance is discussed in relation to identifying target genes that assay ecological and adaptively meaningful genetic variation in a conservation context.

Original languageEnglish
Pages (from-to)1181-1193
Number of pages13
JournalConservation Genetics
Volume16
Issue number5
Early online date24 May 2015
DOIs
Publication statusPublished - Oct 2015

Keywords

  • bottleneck
  • natural selection
  • toll-like receptors
  • host-parasite interactions
  • innate immune defence
  • pathogen recognition
  • natural-population
  • biased parasitism
  • innate immunity
  • ectoparasitic arthropods
  • conservation genetics
  • selection
  • evolution
  • MHC
  • diversity

Cite this

Gene dynamics of toll-like receptor 4 through a population bottleneck in an insular population of water voles (Arvicola amphibius). / Gavan, Martha K.; Oliver, Matthew K.; Douglas, Alex; Piertney, Stuart B.

In: Conservation Genetics, Vol. 16, No. 5, 10.2015, p. 1181-1193.

Research output: Contribution to journalArticle

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abstract = "Understanding the extent to which diversity at immunologically important genes is reduced by demographic perturbations such as population bottlenecks, and the resulting consequences this has on individual fitness, is of fundamental importance for the effective management of genetic resources in natural populations. Toll-like receptors are key immunological genes with well-established links to fitness. Here, levels of allelic diversity and heterozygosity at the toll-like receptor 4 locus (Tlr4) were characterised across 280 water voles (Arvicola amphibius) from an isolated, island population in north west Scotland that went through a severe population bottleneck between 2004 and 2006 that eroded neutral microsatellite variation. Two functional Tlr4 alleles were resolved prior to the population crash at frequencies close to parity and an excess of heterozygote genotypes relative to Hardy-Weinberg expectations. Through the population bottleneck both alleles were retained with genotype frequencies conforming to Hardy-Weinberg expectations. Tlr4 genotype was significantly associated with gamasid mite, flea (Megabothris walkeri) and sheep tick larva (Ixodes ricinus) burdens among individuals, suggesting a mechanism through which parasite mediated selection could affect Tlr4 diversity. The results are examined with recourse to the extent that they are consistent with the effects of genetic drift and balancing selection, and their significance is discussed in relation to identifying target genes that assay ecological and adaptively meaningful genetic variation in a conservation context.",
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N1 - Acknowledgments We would like to thank all colleagues who have contributed to fieldwork and sampling during this study. We would especially like to thank Marius Wenzel and Sandra Telfer for collaboration with different aspects of the study, and Dave Jones and Nat Jones for Bartonella PCR assays. This work was supported by the BBSRC studentship to MKG (BB/J01446X/1) and a NERC studentship to MKO. The research was carried out under project license PPL 40/1813.

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N2 - Understanding the extent to which diversity at immunologically important genes is reduced by demographic perturbations such as population bottlenecks, and the resulting consequences this has on individual fitness, is of fundamental importance for the effective management of genetic resources in natural populations. Toll-like receptors are key immunological genes with well-established links to fitness. Here, levels of allelic diversity and heterozygosity at the toll-like receptor 4 locus (Tlr4) were characterised across 280 water voles (Arvicola amphibius) from an isolated, island population in north west Scotland that went through a severe population bottleneck between 2004 and 2006 that eroded neutral microsatellite variation. Two functional Tlr4 alleles were resolved prior to the population crash at frequencies close to parity and an excess of heterozygote genotypes relative to Hardy-Weinberg expectations. Through the population bottleneck both alleles were retained with genotype frequencies conforming to Hardy-Weinberg expectations. Tlr4 genotype was significantly associated with gamasid mite, flea (Megabothris walkeri) and sheep tick larva (Ixodes ricinus) burdens among individuals, suggesting a mechanism through which parasite mediated selection could affect Tlr4 diversity. The results are examined with recourse to the extent that they are consistent with the effects of genetic drift and balancing selection, and their significance is discussed in relation to identifying target genes that assay ecological and adaptively meaningful genetic variation in a conservation context.

AB - Understanding the extent to which diversity at immunologically important genes is reduced by demographic perturbations such as population bottlenecks, and the resulting consequences this has on individual fitness, is of fundamental importance for the effective management of genetic resources in natural populations. Toll-like receptors are key immunological genes with well-established links to fitness. Here, levels of allelic diversity and heterozygosity at the toll-like receptor 4 locus (Tlr4) were characterised across 280 water voles (Arvicola amphibius) from an isolated, island population in north west Scotland that went through a severe population bottleneck between 2004 and 2006 that eroded neutral microsatellite variation. Two functional Tlr4 alleles were resolved prior to the population crash at frequencies close to parity and an excess of heterozygote genotypes relative to Hardy-Weinberg expectations. Through the population bottleneck both alleles were retained with genotype frequencies conforming to Hardy-Weinberg expectations. Tlr4 genotype was significantly associated with gamasid mite, flea (Megabothris walkeri) and sheep tick larva (Ixodes ricinus) burdens among individuals, suggesting a mechanism through which parasite mediated selection could affect Tlr4 diversity. The results are examined with recourse to the extent that they are consistent with the effects of genetic drift and balancing selection, and their significance is discussed in relation to identifying target genes that assay ecological and adaptively meaningful genetic variation in a conservation context.

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KW - ectoparasitic arthropods

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KW - selection

KW - evolution

KW - MHC

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