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Female mound-building mice prefer males that invest more in building behavior, even when this behavior is not observed

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Abstract

Through behavioral correlations, mate choice could influence the evolution of traits that are not directly selected for, or even observed. We addressed whether mound building, a unique collective behavior observed in Mus spicilegus, could be favored by female mate choice, irrespective of whether females were able to observe the behavior. First, we introduced mixed sex groups of wild-born mice in large terraria with building materials and assessed male variation in building investment. Second, we presented females with a choice between males that invested the most versus the least in building. Females were either able to observe the males during building or not. Third, because overwintering juveniles rely on mound protection, we hypothesized that building could be a form of paternal care, and assessed whether males that invested more in building also invested more in direct offspring care. We showed that females were more attracted to males that invested the most in building, even when these behaviors were not observed. In addition, direct offspring care was negatively correlated with males’ investment in building, suggesting that two alternative paternal care strategies (mound building versus direct offspring care) may exist. Our study supports the hypothesis that building could be detectable by phenotypic cues that differ from building behavior per se and that mate choice may influence the evolution and maintenance of mound building that several authors describe as a common good.

Significance statement

In the mound-building mouse, individuals gather to build a common mound within which juveniles will spend the winter months. As some males invest more in building than others, we questioned whether females would prefer males that invest more in building behaviors, even though females could not observe males’ building behaviors before mate choice. We assessed male investment in building and conducted choice tests. Females were more attracted to males that invested more in building, even when building was not observed. Hence, building investment seems detectable by phenotypic cues that differ from building behavior per se. Further, the males’ investment in building was negatively correlated with their direct offspring care assessed during retrieval trials. Our findings indicate that two alternative paternal care strategies may exist in this species, and that mate choice might influence the evolution of their remarkable collective building.

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Acknowledgments

We are very grateful to D. Simeonovska-Nikolova, B. Nikolovi and C. Albinet for their help for the trapping session in Bulgaria. We also thank Z. Groó, Y. Latour, A. Orth, and M. Perriat-Sanguinet, J. Barthes, J. Bovet, M. Derex, L. Danilo, V. Durand, L. Etienne, A. Nitsch, and A. Ravel, to help provided throughout the experiment and A.J. Carter who proofread the manuscript. We also thank the reviewers for their helpful comments. We thank the Ministry of Environment and Water of Bulgaria, which permitted us to catch specimen of Mus spicilegus. Supports through the ANR - Labex IAST, the CNRS of France (www.cnrs.fr), the Région Languedoc-Roussillon ‘Chercheur(se)s d’Avenir’ (no.: DGA3/DESR/2012/Q159) and the Fondation des Treilles (www.les-treilles.com) are gratefully acknowledged. This is contribution ISEM 2018-162.

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  1. Institute for Advanced Study in Toulouse, 21 allée de Brienne, 31015, Toulouse, France

    Arnaud Tognetti

  2. Institute of Evolutionary Sciences (ISEM), University of Montpellier, CNRS, IRD, EPHE, Montpellier, France

    Arnaud Tognetti, Guila Ganem, Michel Raymond & Charlotte Faurie

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  1. Arnaud Tognetti
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Correspondence to Arnaud Tognetti.

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Ethical approval

Mouse sampling was performed with the authorization of the Bulgarian Ministry of the Environment and Water (permit no. 33-00-140). The study complied with all the relevant laws of France and mice handling and behavioral tests were authorized by the French authorities (Direction Départementale de la Protection des Populations de l’Hérault – Ministère de l’Agriculture, permit no. C34-265). This study also followed the ABS/ASAB guidelines for the ethical treatment of animals. We were particularly committed to limiting the number of mice trapped and tested, and mice were provided an enriched environment and diversified food to reduce their stress as much as possible.

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The authors declare that they have no conflict of interest.

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Tognetti, A., Ganem, G., Raymond, M. et al. Female mound-building mice prefer males that invest more in building behavior, even when this behavior is not observed. Behav Ecol Sociobiol 72, 155 (2018). https://doi.org/10.1007/s00265-018-2569-4

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