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

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.

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

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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.

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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.

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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)

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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

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