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Reproductive timing as an explanation for skewed parentage assignment ratio in a bisexually philopatric population

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Abstract

In mammals, reproductive success can often be directly observed for females, but not males. Early-life correlates of female reproductive success can also be easier to observe due to higher rates of philopatry. Though relatively uncommon, populations in which both sexes remain in their natal home ranges can facilitate studies of mate choice and sex-specific drivers of reproductive success. Genetic parentage assessment in these systems should be more complete due to spatial philopatry since the pool of potential mothers and fathers should be equally accessible for sampling. Nevertheless, many studies still report more maternities than paternities even when individuals are randomly sampled with respect to age and sex. This discrepancy is often attributed to unobserved outbreeding. Here, we investigate two potential drivers for biased genetic parentage assignment in a bisexually philopatric community of bottlenose dolphins in which twice as many maternities as paternities are assigned to randomly sampled adults. We examine whether this pattern can best be explained by (1) sex differences in reproductive timing or (2) high levels of extra-community mating. We use long-term data on female calving success to search for biases in our genetic data collection and to constrain simulations of male reproductive timing patterns that could generate our observed data. We find that the majority of the skew in parentage assignment could be explained by differences in reproductive timing, with a smaller putative role of extra-community mating. We discuss how explicitly considering age effects as well as outbreeding can improve our understanding of sex-specific drivers of reproductive success.

Significance statement

In most mammals, mothers are easy to identify because they provide extended parental care to their offspring, but fathers can be absent in space or time. In a resident population of Indo-Pacific bottlenose dolphins, twice as many mothers as fathers are detected with random genetic sampling. We tested whether we failed to detect paternities because fathers were outside of our main study area or if they were simply older than mothers and likely died before they could be genetically sampled. We found evidence that fathers could be much older on average than mothers. We show that comparing maternities to paternities can reveal potential sources of bias when estimating reproductive success from genetic samples, and our results can be used to target more efficient sampling in future studies.

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Data availability

Code and data to reproduce all analyses are available at https://doi.org/10.5281/zenodo.6970002.

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Acknowledgements

We thank all members of the Shark Bay Dolphin Research Project past and present. We are grateful to the West Australian Department of Biodiversity, Conservation and Attractions (DBCA), the University of Western Australia, the Monkey Mia Dolphin Resort (Royal Automobile Club), and the local Shark Bay community for logistical field support. Additional thanks to the members of the Dolphin Alliance Project for the contribution of samples. We would also like to thank Marco Festa-Bianchet and two anonymous reviewers whose comments greatly improved the manuscript. We acknowledge the Malgana peoples as traditional custodians of the lands and waters of Guthaaguda on which this work was conducted.

Funding

The study was funded by grants from NSF #0847922, 0820722, 9753044, 0316800, 0918308, 0941487, 1755229, 2106909, 2139712, 2146995, 2128134, 1515197, 0521763, 1927619 (to JM), 1559380 (to JM and CF), 2106909 (to JM and VF), ONR 10230702 (to JM), Georgetown University (to JM), Holsworth Wildlife Endowment (to AL), Australasian Society for the Study of Animal Behavior (to AL), and Genecology Research Center, USC (to AL).

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Authors and Affiliations

Authors

Contributions

VF, MM, and JM conceived the study. VF, AL, and AK collected samples for genetic analysis and AL and VF conducted lab work. JM, VF, and MM collected behavioral and demographic data. JM, CF, and AL provided funding. VF, JM, MM, and CF wrote the first draft. All authors edited and approved the final version.

Corresponding author

Correspondence to Vivienne Foroughirad.

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Ethics approval

All applicable international, national, and institutional guidelines for the use of animals were followed. Ethics approval was obtained by the University of the Sunshine Coast (AN/S/15/35) and Georgetown University IACUC (13–069, 07–041, 10–023, 2016–1235). Research was conducted under the Western Australian Department of Biodiversity, Conservation and Attractions permit (SF-009876, SF- 010347, SF-008076, SF009311, SF007457).

Competing interests

The authors declare no competing interests.

Additional information

Communicated by M. Festa-Bianchet

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This article is a contribution to the Topical Collection Measuring individual reproductive success in the wild—Guest Editors: Marco Festa-Bianchet, Janet Mann

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Foroughirad, V., McEntee, M., Kopps, A.M. et al. Reproductive timing as an explanation for skewed parentage assignment ratio in a bisexually philopatric population. Behav Ecol Sociobiol 76, 129 (2022). https://doi.org/10.1007/s00265-022-03233-2

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  • DOI: https://doi.org/10.1007/s00265-022-03233-2

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