Skip to main content
SpringerLink
Log in

The Sex Specific Genetic Variation of Energetics in Bank Voles, Consequences of Introgression?

  • Research Article
  • Published:
Evolutionary Biology Aims and scope Submit manuscript

Abstract

Interaction between mitochondrial and nuclear genomes is expected to affect energetic phenotypes of traits linked to mitochondrial physiology, further influencing the fitness. A rodent, the bank vole (Myodes glareolus), has a population structure completely or partially introgressed with mitochondria from its relative, the red vole (M. r utilus). Females that carried either bank vole mitochondria or mitochondria from the introgressed species were repeatedly mated with males of both mtDNA types. We found that in males, but not in females, morpho-physiological phenotypes are affected by sire type, causing decreases in body mass (BM) and basal metabolic rate (BMR; including BM corrected, rBMR) in individuals sired by fathers carrying introgressed mitochondria. Higher effect sizes for the proportion of additive genetic variation (and 5.6, 1.9 and 3.6 times higher narrow sense heritability for BM, BMR and rBMR, respectively), and lower for proportion of environmental variation were detected in progeny of non-introgressed males. Our data indicate that co-adapted and possibly co-introgressed nuclear genes related to energetic physiology have an important role in adaptation to the northern conditions in bank voles, and that sex linked nuclear genes are a potential source for variation in basal metabolic rate.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Arnold, M. L., Ballerini, E. S., & Brothers, A. N. (2012). Hybrid fitness, adaptation and evolutionary diversification: Lessons learned from Louisiana Irises. Heredity (Edinb), 108, 159–166.

    Article  CAS  Google Scholar 

  • Arnqvist, G., Dowling, D. K., Eady, P., Gay, L., Tregenza, T., Tuda, M., et al. (2010). Genetic architecture of metabolic rate: Environment specific epistasis between mitochondrial and nuclear genes in an insect. Evolution, 64, 3354–3363.

    Article  CAS  PubMed  Google Scholar 

  • Barnett, A. G., Koper, N., Dobson, A. J., Schmiegelow, F., & Manseau, M. (2010). Using information criteria to select the correct variance-covariance structure for longitudinal data in ecology. Methods in Ecology and Evolution, 1, 15–24.

    Article  Google Scholar 

  • Boratyński, Z., Alves, P., Berto, S., Koskela, E., Mappes, T., & Melo-Ferreira, J. (2011). Introgression of mitochondrial DNA among Myodes voles: Consequences for energetics? BMC Evolutionary Biology, 11, 355.

    Article  PubMed Central  PubMed  Google Scholar 

  • Boratyński, Z., Koskela, E., Mappes, T., & Schroderus, E. (2013). Quantitative genetics and fitness effects of basal metabolism. Evolutionary Ecology, 27, 301–314.

    Article  Google Scholar 

  • Boratyński, Z., & Koteja, P. (2010). Sexual and natural selection on body mass and metabolic rates in free-living bank voles. Functional Ecology, 24, 1252–1261.

    Article  Google Scholar 

  • Boratyński, Z., & Koteja, P. (2009). The association between body mass, metabolic rates and survival of bank voles. Functional Ecology, 23, 330–339.

    Article  Google Scholar 

  • Boratyński, Z., Melo-Ferreira, J., Alves, P. C., Berto, S., Koskela, E., Pentikäinen, O. T., et al. (2014). Molecular and ecological signs of mitochondrial adaptation: Consequences for introgression? Heredity (Edinb), 113, 277–286.

    Article  Google Scholar 

  • Burton, T., Killen, S. S., Armstrong, J. D., & Metcalfe, N. B. (2011). What causes intraspecific variation in resting metabolic rate and what are its ecological consequences? Proceedings of the Royal Society of London B: Biological Sciences, 278, 3465–3473.

    Article  CAS  Google Scholar 

  • Einum, S. (2014). Ecological modeling of metabolic rates predicts diverging optima across food abundances. The American Naturalist, 183, 410–417.

    Article  PubMed  Google Scholar 

  • Field, D., Tiwari, B., Booth, T., Houten, S., Swan, D., Bertrand, N., et al. (2006). Open software for biologists: From famine to feast. Nature Biotechnology, 24, 801–803.

    Article  CAS  PubMed  Google Scholar 

  • Filipi, K., Marková, S., Searle, J. B., & Kotlík, P. (2015). Mitogenomic phylogenetics of the bank vole Clethrionomys glareolus, a model system for studying end-glacial colonization of Europe. Molecular Phylogenetics and Evolution, 82, 245–257.

    Article  PubMed  Google Scholar 

  • Gaitán-Espitia, J. D., Belén Arias, M., Lardies, M. A., & Nespolo, R. F. (2013). Variation in thermal sensitivity and thermal tolerances in an invasive species across a climatic gradient: Lessons from the land snail Cornu aspersum. PLoS One, 8, e70662.

    Article  PubMed Central  PubMed  Google Scholar 

  • Hadfield, J. D. (2010). MCMC methods for multi-response generalized linear mixed models: The MCMCglmm R package. Journal of Statistical Software, 33, 1–22.

    Article  Google Scholar 

  • Hadjivasiliou, Z., Pomiankowski, A., Seymour, R. M., & Lane, N. (2012). Selection for mitonuclear co-adaptation could favour the evolution of two sexes. Proceedings of the Royal Society of London B: Biological Sciences, 279, 1865–1872.

    Article  Google Scholar 

  • Hill, G. E., & Johnson, J. D. (2013). Proceedings of the Royal Society of London B: Biological Sciences. Proc. R. Soc. B Biol. Sci., 280, 20131314.

    Article  Google Scholar 

  • Ketola, T., & Kotiaho, J. S. (2009). Inbreeding, energy use and condition. Journal of Evolutionary Biology, 22, 770–781.

    Article  CAS  PubMed  Google Scholar 

  • Kohli, B. A., Fedorov, V. B., Waltari, E., & Cook, J. A. (2015). Phylogeography of a Holarctic rodent (Myodes rutilus): Testing high-latitude biogeographical hypotheses and the dynamics of range shifts. Journal of Biogeography, 42(2), 377–389.

    Article  Google Scholar 

  • Koteja, P. (1996). Measuring energy metabolism with open-flow respirometric systems: Which design to choose? Functional Ecology, 10, 675–677.

    Article  Google Scholar 

  • Kotlík, P., Deffontaine, V., Mascheretti, S., Zima, J., Michaux, J. R., & Searle, J. B. (2006). A northern glacial refugium for bank voles (Clethrionomys glareolus). Proceedings of the National Academy of Sciences, 103, 14860–14864.

    Article  Google Scholar 

  • Labocha, M. K., Sadowska, E. T., Baliga, K., Semer, A. K., & Koteja, P. (2004). Individual variation and repeatability of basal metabolism in the bank vole, Clethrionomys glareolus. Proceedings of the Royal Society of London B: Biological Sciences, 271, 367–372.

    Article  Google Scholar 

  • Lane, N. (2011). Mitonuclear match: Optimizing fitness and fertility over generations drives ageing within generations. BioEssays, 33, 860–869.

    Article  CAS  PubMed  Google Scholar 

  • Mariette, M. M., Buchanan, K. L., Buttemer, A. W., & Careau, V. (2015). Tough decisions: Reproductive timing and output vary with individuals’ physiology, behavior and past success in a social opportunistic breeder. Hormones and behavior,. doi:10.1016/j.yhbeh.2015.03.011.

    PubMed  Google Scholar 

  • Naya, D. E., Spangenberg, L., Naya, H., & Bozinovic, F. (2013). How does evolutionary variation in Basal metabolic rates arise? A statistical assessment and a mechanistic model. Evolution, 67, 1463–1476.

    PubMed  Google Scholar 

  • Nespolo, R. F., Bartheld, J. L., González, A., Bruning, A., Roff, D. A., Bacigalupe, L. D., et al. (2014). The quantitative genetics of physiological and morphological traits in an invasive terrestrial snail: Additive vs. non-additive genetic variation. Functional Ecology, 28, 682–692.

    Article  Google Scholar 

  • Puurtinen, M., Ketola, T., & Kotiaho, J. S. (2009). The good-genes and compatible-genes benefits of mate choice. The American Naturalist, 174, 741–752.

    Article  PubMed  Google Scholar 

  • Sadowska, E. T., Baliga-Klimczyk, K., Labocha, M. K., & Koteja, P. (2009). Genetic correlations in a wild rodent: Grass-eaters and fast-growers evolve high basal metabolic rates. Evolution, 63, 1530–1539.

    Article  PubMed  Google Scholar 

  • Sadowska, E. T., Stawski, C., Rudolf, A., Dheyongera, G., Chrząścik, K. M., Baliga-Klimczyk, K., & Koteja, P. (2015). Evolution of basal metabolic rate in bank voles from a multidirectional selection experiment. Proceedings of the Royal Society of London B: Biological Sciences, 282, 20150025.

    Article  Google Scholar 

  • Šíchová, K., Koskela, E., Mappes, T., Lantová, P., & Boratyński, Z. (2014). On personality, energy metabolism and mtDNA introgression in bankvoles. Animal Behaviour, 92, 229–237.

    Article  Google Scholar 

  • Tegelström, H. (1987). Transfer of mitochondrial DNA from the northern red-backed vole (Clethrionomys rutilus) to the bank vole (C. g lareolus). Journal of Molecular Evolution, 24, 218–227.

    Article  PubMed  Google Scholar 

  • White, C. R., & Kearney, M. R. (2013). Determinants of inter-specific variation in basal metabolic rate. Journal of Comparative Physiology B, 183, 1–26.

    Article  CAS  Google Scholar 

  • Williams, C. M., Henry, H. A. L., & Sinclair, B. J. (2015). Cold truths: How winter drives responses of terrestrial organisms to climate change. Biological Reviews, 90, 214–235.

    Article  PubMed  Google Scholar 

  • Wilson, A. J., Réale, D., Clements, M. N., Morrissey, M. M., Postma, E., Walling, C. A., et al. (2010). An ecologist’s guide to the animal model. Journal of Animal Ecology, 79, 13–26.

    Article  PubMed  Google Scholar 

  • Wolff, J. N., Ladoukakis, E. D., Enríquez, J. A., & Dowling, D. K. (2014). Mitonuclear interactions: Evolutionary consequences over multiple biological scales. Philosophical Transactions of the Royal Society B: Biological Sciences, 369(1646), 20130443.

    Article  Google Scholar 

  • Zub, K., Borowski, Z., Szafrańska, P. A., Wieczorek, M., & Konarzewski, M. (2014). Lower body mass and higher metabolic rate enhance winter survival in root voles, Microtus oeconomus. Biological Journal of the Linnean Society, 113, 297–309.

    Article  Google Scholar 

Download references

Acknowledgments

We acknowledge Paulina A. Szafranska, Mikael Mökkönen and one anonymous reviewer for comments and corrections of the manuscript. This work was supported by Finnish Academy of Science (Grants Numbers: 257340 to EK, 278751 to TK and 132190 to TM). ZB is post-doctoral grantee of the Foundation for Science and Technology, Portugal (SFRH/BPD/84822/2012).

Author information

Authors and Affiliations

  1. CIBIO/InBio, Research Center in Biodiversity and Genetic Resources, University of Porto, Campus Agrário de Vairão, R. Padre Armando Quintas, 4485-661, Vairão, Portugal

    Zbyszek Boratyński

  2. Division of Ecology and Evolutionary Biology, Department of Biological and Environmental Science, University of Jyväskylä, Jyväskylä, Finland

    Zbyszek Boratyński, Tarmo Ketola, Esa Koskela & Tapio Mappes

Authors
  1. Zbyszek Boratyński
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Tarmo Ketola
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Esa Koskela
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Tapio Mappes
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Zbyszek Boratyński.

Ethics declarations

Conflict of interest

The authors declare that there are no conflicts of interest.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Boratyński, Z., Ketola, T., Koskela, E. et al. The Sex Specific Genetic Variation of Energetics in Bank Voles, Consequences of Introgression?. Evol Biol 43, 37–47 (2016). https://doi.org/10.1007/s11692-015-9347-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11692-015-9347-2

Keywords

Search

Navigation