Skip to main content
SpringerLink
Log in

Discrete genetic modules are responsible for complex burrow evolution in Peromyscus mice

  • Letter
  • Published:

From Nature

View current issue Submit your manuscript

Abstract

Relative to morphological traits, we know little about how genetics influence the evolution of complex behavioural differences in nature1. It is unclear how the environment influences natural variation in heritable behaviour2, and whether complex behavioural differences evolve through few genetic changes, each affecting many aspects of behaviour, or through the accumulation of several genetic changes that, when combined, give rise to behavioural complexity3. Here we show that in nature, oldfield mice (Peromyscus polionotus) build complex burrows with long entrance and escape tunnels, and that burrow length is consistent across populations, although burrow depth varies with soil composition. This burrow architecture is in contrast with the small, simple burrows of its sister species, deer mice (P. maniculatus). When investigated under laboratory conditions, both species recapitulate their natural burrowing behaviour. Genetic crosses between the two species reveal that the derived burrows of oldfield mice are dominant and evolved through the addition of multiple genetic changes. In burrows built by first-generation backcross mice, entrance-tunnel length and the presence of an escape tunnel can be uncoupled, suggesting that these traits are modular. Quantitative trait locus analysis also indicates that tunnel length segregates as a complex trait, affected by at least three independent genetic regions, whereas the presence of an escape tunnel is associated with only a single locus. Together, these results suggest that complex behaviours—in this case, a classic ‘extended phenotype’4—can evolve through multiple genetic changes each affecting distinct behaviour modules.

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

Figure 1: Natural variation in P. polionotus burrows.
Figure 2: Burrow variation across generations.
Figure 3: QTL analysis of burrow variation.

Similar content being viewed by others

References

  1. Boake, C. R. B. et al. Genetic tools for studying adaptation and the evolution of behavior. Am. Nat. 160, S143–S159 (2002)

    Article  PubMed  Google Scholar 

  2. West-Eberhard, M. J. Developmental Plasticity and Evolution (Oxford Univ. Press, 2003)

    Book  Google Scholar 

  3. Mackay, T. F. C. The genetic architecture of quantitative traits. Annu. Rev. Genet. 35, 303–339 (2001)

    Article  CAS  PubMed  Google Scholar 

  4. Dawkins, R. The Extended Phenotype (W. H. Freeman, 1982)

    Google Scholar 

  5. Hansell, M. H. Animal Architecture (Oxford Univ. Press, 2005)

    Book  Google Scholar 

  6. Lorenz, K. Z. The evolution of behaviour. Sci. Am. 199, 67–78 (1958)

    Article  CAS  PubMed  Google Scholar 

  7. Peichel, C. L. et al. The genetic architecture of divergence between threespine stickleback species. Nature 414, 901–905 (2001)

    Article  ADS  CAS  PubMed  Google Scholar 

  8. Steiner, C. C., Weber, J. N. & Hoekstra, H. E. Adaptive variation in beach mice caused by two interacting pigmentation genes. PLoS Biol. 5, 1880–1889 (2007)

    Article  CAS  Google Scholar 

  9. Sumner, F. B. & Karol, J. J. Notes on the burrowing habits of Peromyscus polionotus. J. Mamm. 10, 213–215 (1929)

    Article  Google Scholar 

  10. Hayne, D. W. Burrowing habits of Peromyscus polionotus. J. Mamm. 17, 420–421 (1936)

    Article  Google Scholar 

  11. Rand, A. L. & Host, P. Mammal notes from Highland County, Florida. Bull. Am. Mus. Nat. Hist. 80, 1–21 (1942)

    Google Scholar 

  12. Houtcooper, W. C. Rodent seed supply and burrows of Peromyscus in cultivated fields. Proc. Indiana Acad. Sci. 81, 348–389 (1971)

    Google Scholar 

  13. Schwartz, C. W. & Schwartz, E. R. The Wild Mammals of Missouri (Univ. Missouri Press, 1981)

    Google Scholar 

  14. Baker, R. H. in Biology of Peromyscus (Rodentia) (ed. King, J. A. ) (American Society of Mammalogists, 1968)

    Google Scholar 

  15. Wolfe, J. L. & Esher, R. J. Burrowing behaviour of old-field mice (Peromyscus polionotus): a laboratory investigation. Bio. Behav. 2, 343–351 (1977)

    Google Scholar 

  16. Dawson, W. D., Lake, C. E. & Schumpert, S. S. Inheritance of burrow building in Peromyscus. Behav. Genet. 18, 371–382 (1988)

    Article  CAS  PubMed  Google Scholar 

  17. Weber, J. N. & Hoekstra, H. E. The evolution of burrowing behavior in deer mice. Anim. Behav. 77, 603–609 (2009)

    Article  Google Scholar 

  18. Tan, K. H. Soil Sampling, Preparation, and Analysis (CRC Press, 2005)

    Book  Google Scholar 

  19. Wright, S. A mutation of the guinea pig, tending to restore the pentadactyl foot when heterozygous, producing a monstrosity when homozygous. Genetics 20, 84–107 (1935)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Peterson, B. K., Weber, J. N., Kay, E. H., Fisher, H. S. & Hoekstra, H. E. Double digest RADseq: an inexpensive method for de novo SNP discovery and genotyping in model and non-model species. PLoS ONE 7, e37135 (2012)

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  21. Beavis, W. D. in Molecular Dissection of Complex Traits (ed. Paterson, A. H. ) 431–528 (CRC Press, 1998)

    Google Scholar 

  22. Bendesky, A. & Bargmann, C. I. Genetic contributions to behaviour at the gene–environment interface. Nature Rev. Genet. 12, 809–820 (2011)

    Article  CAS  PubMed  Google Scholar 

  23. Fitzpatrick, M. J. et al. Candidate genes for behavioural ecology. Trends Ecol. Evol. 20, 96–104 (2005)

    Article  PubMed  Google Scholar 

  24. Huxley, J. S. The courtship habits of the great crested grebe (Podiceps cristatus) with an addition to the theory of sexual selection. Proc. Zool. Soc. Lond. 35, 253–291 (1914)

    Google Scholar 

  25. Mallarino, R. et al. Two developmental modules establish 3D beak shape variation in Darwin’s finches. Proc. Natl Acad. Sci. USA 108, 4057–4062 (2011)

    Article  ADS  CAS  PubMed  Google Scholar 

  26. Xu, X. et al. Modular genetic control of sexually dimorphic behaviors. Cell 148, 596–607 (2012)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Felthauser, M. & McInroy, D. Mapping pocket gopher burrow systems with expanding polyurethane foam. J. Wildl. Manage. 47, 555–558 (1983)

    Article  Google Scholar 

  28. R Development Core Team. R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2011)

  29. Broman, K. W., Wu, H., Sen, Ś. & Churchill, G. A. R/qtl: QTL mapping in experimental crosses. Bioinformatics 19, 889–890 (2003)

    Article  CAS  PubMed  Google Scholar 

  30. Lincoln, S. E. & Lander, E. S. Systematic detection of errors in genetic linkage data. Genomics 14, 604–610 (1992)

    Article  CAS  PubMed  Google Scholar 

  31. Doerge, R. W. & Rebai, A. Significance thresholds for QTL interval mapping tests. Heredity 76, 459–464 (1996)

    Article  Google Scholar 

  32. Sen, Ś., Satagopan, J., Broman, K. W. & Churchill, G. A. R/qtlDesign: Inbred Line Cross Experimental Design (UC San Francisco: Center for Bioinformatics and Molecular Biostatistics, 2006)

    Google Scholar 

  33. Cheng, R. et al. Genome-wide association studies and the problem of relatedness among advanced intercross lines and other highly recombinant populations. Genetics 185, 1033–1044 (2010)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Cheng, R., Abney, M., Palmer, A. A. & Skol, A. D. QTLRel: an R package for genome-wide association studies in which relatedness is a concern. BMC Genet. 12, 66 (2011)

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We thank D. Brimmer, A. Chiu, A. Goldberg, J. Hopwood, W. Tong, S. Wolff and the Hoekstra laboratory for assistance with behavioural assays and animal husbandry; D. Haig, B. Ölveczky, N. E. Pierce and J. Sanes for helpful discussions; and Harvard’s Office of Animal Resources, particularly J. Rocca and M. O’Donnell. We also thank R. Barrett, A. Bendesky, H. Fisher, E. Kay, H. Metz and W. Tong for comments on the manuscript. This research was funded by Chapman Funds for Vertebrate Locomotion to J.N.W., National Science Foundation grant (IOS-0910164) to J.N.W. and H.E.H., and an Arnold and Mabel Beckman Young Investigator Award to H.E.H.

Author information

Author notes

  1. Jesse N. Weber

    Present address: Present address: Section of Integrative Biology, One University Station, University of Texas Austin, Texas 78712, USA.,

Authors and Affiliations

  1. Department of Organismic & Evolutionary Biology, Museum of Comparative Zoology, 26 Oxford Street, Cambridge, Massachusetts 02138, USA,

    Jesse N. Weber, Brant K. Peterson & Hopi E. Hoekstra

  2. Department of Molecular & Cellular Biology, Center for Brain Science, 16 Divinity Avenue, Cambridge, Massachusetts 02138, USA,

    Brant K. Peterson & Hopi E. Hoekstra

Authors
  1. Jesse N. Weber
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Brant K. Peterson
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Hopi E. Hoekstra
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

J.N.W. and H.E.H. conceived and designed the experiments. B.K.P. and J.N.W. generated the ddRAD genotypes. J.N.W. performed the behaviour experiments and analysed the genetic and behavioural data. J.N.W. and H.E.H. wrote the paper.

Corresponding author

Correspondence to Hopi E. Hoekstra.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary Information

This file contains Supplementary Tables 1-2 and Supplementary Figures 1-4. (PDF 342 kb)

P. polionotus exiting through an escape tunnel and burrow casting method

P. polionotus erupt from an escape tunnel when intruders enter their burrow. We can take advantage of this behavior in the laboratory to remove mice from their burrows, while keeping the burrow architecture intact. Once empty, burrows size and shape can be quantified by constructing and measuring polyurethane casts of each burrow. (MOV 11455 kb)

PowerPoint slides

Rights and permissions

Reprints and permissions

About this article

Cite this article

Weber, J., Peterson, B. & Hoekstra, H. Discrete genetic modules are responsible for complex burrow evolution in Peromyscus mice. Nature 493, 402–405 (2013). https://doi.org/10.1038/nature11816

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature11816

  • Springer Nature Limited

This article is cited by

Search

Navigation