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Competition drives cooperation among closely related sperm of deer mice

Abstract

Among the extraordinary adaptations driven by sperm competition is the cooperative behaviour of spermatozoa1. By forming cooperative groups, sperm can increase their swimming velocity and thereby gain an advantage in intermale sperm competition1,2. Accordingly, selection should favour cooperation of the most closely related sperm to maximize fitness3. Here we show that sperm of deer mice (genus Peromyscus) form motile aggregations, then we use this system to test predictions of sperm cooperation. We find that sperm aggregate more often with conspecific than heterospecific sperm, suggesting that individual sperm can discriminate on the basis of genetic relatedness. Next, we provide evidence that the cooperative behaviour of closely related sperm is driven by sperm competition. In a monogamous species lacking sperm competition, Peromyscus polionotus, sperm indiscriminately group with unrelated conspecific sperm. In contrast, in the highly promiscuous deer mouse, Peromyscus maniculatus, sperm are significantly more likely to aggregate with those obtained from the same male than with sperm from an unrelated conspecific donor. Even when we test sperm from sibling males, we continue to see preferential aggregations of related sperm in P. maniculatus. These results suggest that sperm from promiscuous deer mice discriminate among relatives and thereby cooperate with the most closely related sperm, an adaptation likely to have been driven by sperm competition.

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Figure 1: Images of Peromyscus sperm in BWW medium.
Figure 2: Preferential sperm aggregations.

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Acknowledgements

We thank M. Manceau and J. Gros for technical assistance and R. Lewontin for statistical advice. S. Immler, K. Foster and D. Haig provided comments and discussion on the manuscript. H.S.F. is supported by an NIH Ruth Kirschstein National Research Service Award. Research was funded by an Arnold and Mabel Beckman Foundation Young Investigator Award to H.E.H.

Author Contributions H.S.F proposed the idea for the study, collected and analysed the data. H.S.F. and H.E.H designed the study and wrote the paper. H.E.H. acquired funding for the project.

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Correspondence to Heidi S. Fisher.

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Supplementary information

Supplementary Movie 1

This movie shows live sperm as both single cells and in multi-cellular aggregations. Sperm were harvested from a Peromyscus maniculatus male, incubated for 10 min in BWW media at 37°C, then viewed on a plastic slide with a raised plastic cover to prevent sperm from adhering to the slide surface. (MOV 35869 kb)

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Fisher, H., Hoekstra, H. Competition drives cooperation among closely related sperm of deer mice. Nature 463, 801–803 (2010). https://doi.org/10.1038/nature08736

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