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Influence of rearing environment on the development of social behavior in male water voles (Arvicola amphibius)

Abstract

In litter-bearing mammals, the prenatal and postnatal environments are crucial for developing social behaviors, which help individuals survive and reproduce. Here, we hypothesized that the social behavior of adult water vole [Arvicola amphibius (Linnaeus, 1758)] males is determined by natural variations in early rearing conditions (maternal body mass, litter size, and litter sex ratio at birth), which affect the growth of offspring and degree of competition for limited maternal resources among littermates. We conducted a correlational study on laboratory-born males to test this hypothesis and identify the key parameters of the family environment that affect the development of behavioral phenotypes. Social behavior was evaluated after reaching sexual maturity during dyadic encounters in a neutral arena. The frequency of amicable contacts, threats, and direct aggression was registered. Pretest body mass and serum testosterone level were determined as potential drivers of aggressiveness. Adult body mass was not correlated with social behavior or serum testosterone level but serum testosterone level was inversely correlated with threat frequency. In our linear mixed model, the frequency of direct aggressive interactions was positively correlated with the size of litter into which the males were born and weaned. We propose that the long-lasting effect of litter size on male social behavior can be explained by the association between maternal fecundity and competition for maternal resources among littermates. At 1, 2, and 3 weeks of age, litter size at birth was negatively correlated with body mass, and this association became stronger with increasing age, suggesting the presence of a trade-off between offspring number and quality.

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The datasets analyzed during the current study are available from the corresponding author on reasonable request.

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Acknowledgements

We thank Maria Orlova for the excellent care of water voles. The authors would like to thank Frank E. Zachos, Heiko G Rödel and an anonymous reviewer for valuable comments and suggestions, which helped us to improve the quality of the article.

Funding

This study was supported by the Federal Fundamental Scientific Research Programme for 2013–2020 (VI.51.1.8 № AAAA-A16-116121410118–7).

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GN and SK conceived and planned the experiments. AU, LP and KS carried out the experiments. EY assisted with testosterone measurements. GN led analyses and wrote the manuscript with support from EY All authors discussed the results and commented on the manuscript.

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Correspondence to Galina G. Nazarova.

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All experiments were performed following the Russian national instructions for the care and use of laboratory animals (GOST 33216–2014, which corresponds to the ETS N 123 "European Convention for the protection of Vertebrate animals used for experimental and other scientific purposes", NEQ).

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Nazarova, G.G., Ulshina, A.S., Starchenko, K.I. et al. Influence of rearing environment on the development of social behavior in male water voles (Arvicola amphibius). Mamm Biol 101, 545–553 (2021). https://doi.org/10.1007/s42991-021-00170-x

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Keywords

  • Litter size
  • Pre-weaning growth
  • Trade-off
  • Testosterone
  • Male aggression