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Reproductive coordination breeds success: the importance of the partnership in avian sperm biology

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Abstract

Previous experience with a partner can improve reproductive coordination between a pair and increase offspring production. We paired inexperienced zebra finches and investigated how a pairs’ experience and their reproductive success together (i.e., whether they were successful or unsuccessful at rearing chicks) related to the number of sperm reaching the ovum, sperm motile performance, and hatching success. In contrast to unsuccessful pairs, successful pairs increased their relative hatching rates over sequential breeding attempts, with pairs hatching 100% of eggs after successfully fledging their previous clutch. Across the study, hatching failure was primarily due to early embryo death. Further, the number of sperm reaching the perivitelline layer (PVL) significantly decreased after fledging chicks in successful pairs, and overall, less sperm was found on the PVL in successful pairs compared with unsuccessful pairs. Across breeding attempts, males in successful pairs also exhibited a significant decline in sperm swimming speed, whereas it increased over breeding attempts in unsuccessful pairs. Our results support the idea of an optimal level of supernumerary sperm on the avian egg. However, our data suggest that there are likely to be interactions between the quality of a partnership and male sperm traits that may contribute to fitness in socially monogamous birds and that have been largely neglected to date.

Significance statement Breeding experience with a partner can improve physiological and behavioural coordination and the reproductive success of a pair. In the zebra finch, we assessed whether experience and reproductive success altered sperm swimming speed, the number of sperm reaching the ovum, and the number of chicks hatching. These three measures are potentially correlated, given that birds require multiple sperm to fuse with the ovum for fertilization and development to occur, and the idea that sperm swimming speed impacts a sperm’s success at fertilizing ova. However, too many or too few sperm can lead to hatching failure, so there will be an optimal number of sperm to ensure fertilization and healthy development. We found that only pairs that successfully reared chicks increased hatching success in subsequent clutches and decreased the amount of sperm reaching the ovum. Additionally, with more experience, the swimming speed of the top 10% of their sperm decreased. These findings are important because they link partnership quality to sperm biology.

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Data accessibility

The dataset supporting this study is available in the Knowledge Network for Biocomplexity repository, https://doi.org/10.5063/F1T43RFB.

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Acknowledgements

We would like to thank Peri Bolton for her art used with permission in Fig. 1, Drew Allen and Shinichi Nakagawa for guidance with the statistical analyses, and Jan Lifjeld, Lars Erik Johannessen, Steve Pruett-Jones, and three anonymous reviewers for useful comments on the manuscript.

Funding

This work was supported by Australian Research Council (grant number DP130100417 to SCG and MR). MR was supported by a Young Research Talent grant from the Research Council of Norway (grant number 230434).

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Authors and Affiliations

  1. Department of Biological Sciences, Macquarie University, Sydney, Australia

    Laura L. Hurley & Simon C. Griffith

  2. Natural History Museum, University of Oslo, 0562, Oslo, Norway

    Melissah Rowe

  3. Centre for Ecological and Evolutionary Synthesis, Department of Biosciences, University of Oslo, 0316, Oslo, Norway

    Melissah Rowe

  4. Department of Animal Ecology, Netherlands Institute of Ecology (NIOO-KNAW), 6700 AB, Wageningen, The Netherlands

    Melissah Rowe

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  1. Laura L. Hurley
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Correspondence to Laura L. Hurley.

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All procedures were conducted according to relevant national and international guidelines and were approved by the Macquarie University Animal Ethics Committee: Animal Research Authority 2013/29.

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Communicated by S. Pruett-Jones

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Hurley, L.L., Rowe, M. & Griffith, S.C. Reproductive coordination breeds success: the importance of the partnership in avian sperm biology. Behav Ecol Sociobiol 74, 3 (2020). https://doi.org/10.1007/s00265-019-2782-9

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