Evolutionary Ecology

, Volume 28, Issue 5, pp 957–975 | Cite as

Wild cyclic voles maintain high neutral and MHC diversity without strong evidence for parasite-mediated selection

  • J. C. Winternitz
  • J. P. Wares
  • M. J. Yabsley
  • S. Altizer
Original Paper


The major histocompatibility complex (MHC) is an important component of vertebrate immune defense involved with self/nonself recognition and disease susceptibility. The high variability of genes of the MHC is thought to arise from both parasite-mediated and sexual selection. An outstanding question involves the degree to which balancing selection can oppose genetic drift to maintain high MHC diversity in the face of population bottlenecks. To address this question we examined genetic diversity and population structure at neutral (microsatellite) and MHC genes in montane voles [Microtus montanus (Peale, 1848)] subject to high amplitude population fluctuations, and compared these to measures of infection by common gastrointestinal parasites. We found high neutral and MHC allelic variability, indicating low impacts of genetic drift despite large fluctuations in population size. Greater MHC diversity did not predict lower parasite richness or infection by the two most common endoparasites (cestodes and coccidian protozoa), as might be expected if genotypic composition confers resistance to infection. One specific MHC allele predicted lower cestode intensity, but we found no other associations between MHC and infection measures. Neutral heterozygosity was positively associated with total parasite richness, possibly owing to greater parasite tolerance among heterozygous relative to more inbred hosts. Overall, these results suggest that factors beyond the parasites examined here, such as high inter-patch migration, mate choice, gene conversion or other infectious agents, are likely maintaining the high levels of MHC diversity observed in wild montane voles.


Major histocompatibility complex Host-parasite relationship Balancing selection Microtus montanus Cestodes Eimeria Microsatellites 



We thank the Rocky Mountain Biological Laboratory for field site coordination and J. Brancale, L. Bryant, M. Eisel, P. Howell, J. Lieb, and J. Parmer for trapping assistance. T. Glenn provided advice and resources for molecular genetic work, and J. Carroll, J. Moore, and the Altizer and Ezenwa lab groups at UGA, and two anonymous reviewers provided useful discussion and comments on previous manuscript drafts. We thank the Odum School of Ecology, National Geographic Society, Animal Behavior Society, Association for Women in Science, Philosophical Society, and the Rocky Mountain Biological Laboratory for funding of field and lab work. JCW was supported by a Graduate School Assistantship from the University of Georgia and a T-32 Training Grant from the National Institutes of Health. SA was supported by funding from the National Science Foundation (DEB-0643831 and DEB-1020966). JPW was supported by funding from the National Science Foundation (NSF-OCE-1029526).

Supplementary material

10682_2014_9709_MOESM1_ESM.docx (57 kb)
Supplementary material 1 (DOCX 58 kb)


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Copyright information

© Springer International Publishing Switzerland 2014

Authors and Affiliations

  • J. C. Winternitz
    • 1
    • 4
  • J. P. Wares
    • 2
  • M. J. Yabsley
    • 3
  • S. Altizer
    • 1
  1. 1.Odum School of EcologyUniversity of GeorgiaAthensUSA
  2. 2.Department of GeneticsUniversity of GeorgiaAthensUSA
  3. 3.College of Veterinary MedicineUniversity of GeorgiaAthensUSA
  4. 4.Institute of Vertebrate BiologyAcademy of Sciences of the Czech Republic, v.v.i.BrnoCzech Republic

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