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Determinants of multiple paternity in a fluctuating population of ground squirrels

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Abstract

Multiple paternity is common in vertebrates that produce several offspring in the same reproductive bout, but the rate often varies among and within populations. Three primary explanations for this variation have been advanced: null models based on encounter rate of mates, socioecological models dependent on the ability of males to monopolize females, and age- or condition-dependent models of female choice. We used 18 years of genetic and demographic data to examine the mating system and patterns of multiple paternity in a free-living population of golden-mantled ground squirrels (Callospermophilus lateralis). The mating system was polygynandrous, but opportunity for sexual selection was lower for females than for males. Annual reproductive success of males was low for yearlings and new immigrants and increased with breeding tenure in the population. Multiple paternity was evident in 62% of litters. In accordance with the socioecological model of male monopolization, rates of multiple paternity decreased with female spatial clustering, unless male–male competition, as indicated by male density, was also high. From Bateman gradients, we found no direct fitness benefit of multiple paternity for females. Though not statistically significant, multiple paternity appeared to decrease with maternal age and peri-oestrous mass, in possible support of the female choice model. Together, our results suggest that variation in the rate of multiple paternity in golden-mantled ground squirrels was determined by density and the active strategies of males and females.

Significance statement

Since the advent of molecular parentage assignment several decades ago, we have known that females of many species produce offspring with different fathers. Several theories have been developed for why females produce multiply-sired clutches or litters, but rarely are we able to identify the environmental, social, or individual conditions under which they do so. In this study, we genotyped offspring produced in one population of ground squirrels over 18 years, and found that the frequency of multiple paternity varied considerably from year to year, that density of female kin interacted with male density to influence multiple paternity, and that older and heavier females tended to be less likely to produce multiply-sired litters. These results demonstrate how dynamic population and individual characteristics of breeding males and females contribute to mating system variation in the same population over time.

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Acknowledgments

We thank the Rocky Mountain Biological Lab for logistical support, B. Barr for weather data from Gothic, and the many research assistants, including G. Aldridge, K. Jenderseck, C. Wickham, T. Anderson, and C. Mueller, who have participated in data collection. We thank M. Finger, A. Goodbla, A. Schrier, and other members of the Genomic Variation Lab at the University of California, Davis, for advice on microsatellite methods and parentage analysis. J.M. Eadie, A.K. Townsend, and two anonymous reviewers provided valuable comments on an earlier draft of this manuscript. We thank the California Agricultural Experiment Station; the Graduate Group in Ecology, University of California, Davis; Henry A. Jastro Research Fellowship, University of California, Davis; the American Society of Mammalogists; and the American Museum of Natural History Theodore Roosevelt Memorial Grant for funding this work.

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Authors and Affiliations

  1. Department of Wildlife, Fish, and Conservation Biology, University of California, One Shields Ave, Davis, CA, 95616, USA

    C. P. Wells & D. H. Van Vuren

  2. Rocky Mountain Biological Laboratory, PO Box 519, Crested Butte, CO, 81224, USA

    C. P. Wells, C. H. Floyd & D. H. Van Vuren

  3. Department of Animal Science, University of California, One Shields Ave., Davis, CA, 95616, USA

    K. M. Tomalty & B. P. May

  4. Department of Biology, University of Wisconsin-Eau Claire, Eau Claire, WI, 54701, USA

    C. H. Floyd

  5. Department of Primatology, Max Planck Institute for Evolutionary Anthropology, Deutscher Platz 6, 04103, Leipzig, Germany

    M. B. McElreath

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  1. C. P. Wells
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Correspondence to C. P. Wells.

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Funding

This work was funded by the California Agricultural Experiment Station (DHV); the Graduate Group in Ecology, University of California, Davis (CPW); Henry A. Jastro Research Fellowship, University of California, Davis (CPW); an American Society of Mammalogists Grant-in-Aid of Research (CPW); and an American Museum of Natural History Theodore Roosevelt Memorial Grant (CPW).

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

Our trapping protocol was approved by Animal Care and Use Committees of the University of California, Davis, and the Rocky Mountain Biological Laboratory and adhered to guidelines approved by the American Society of Mammalogists (Sikes and Gannon 2011).

Informed consent

This study did not involve human subjects, so no informed consent was obtained.

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Communicated by E. Korpimäki

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Wells, C.P., Tomalty, K.M., Floyd, C.H. et al. Determinants of multiple paternity in a fluctuating population of ground squirrels. Behav Ecol Sociobiol 71, 42 (2017). https://doi.org/10.1007/s00265-017-2270-z

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  • DOI: https://doi.org/10.1007/s00265-017-2270-z

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