Abstract
In animals with multiple-partner mating systems, the gametes of two or more males must compete to fertilize a given set of ova1,2,3,4,5. Here we show that the volume of the midpiece in individual sperm is significantly greater in primate species in which the females mate with multiple partners, and in which males have larger testes in relation to their body weight, than in those species that mate with only one partner and have relatively small testes. Our results indicate that sexual selection by sperm competition has influenced the evolution of a specific component of male-gamete morphology, the volume of the sperm midpiece.
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We classified different primate species as having either a single- or multiple-partner mating system on the basis of published descriptions of primary mating systems and behavioural information6,7. We measured the lengths (in µm) and volumes (in µm3) of sperm head, midpiece and flagellum in 31 species, representing 21 primate genera. We compared differences in sperm morphology between single- and multiple-partner mating systems at both the genus and species levels, using comparative analysis of independent contrasts (CAIC)8. Critical α-levels were adjusted for multiple comparisons of sperm traits using the sequential Bonferroni technique.
Sperm lengths did not differ statistically between single- and multiple-partner mating systems. By contrast, sperm midpiece volumes differed significantly at both the genus (F = 20.86, P < 0.01) and species (F = 3.46, P < 0.05) levels (Fig. 1a). When sperm-head volumes associated with single- and multiple-partner mating systems were compared, there was no significant difference between genera or species (44.01 ± 2.71 µm3 versus 41.82 ± 2.40 µm3, and 46.20 ± 3.2 µm3 versus 44.56 ± 2.89 µm3, respectively). The same was true for flagellum volumes (9.74 ± 0.82 µm3 versus 9.73 ± 1.21 µm3, and 8.01 ± 0.81 µm3 versus 9.69 ± 0.88 µm3, respectively).
Because there is disagreement over the classification of primate mating systems, we also used relative testis weight as an indirect measure of likely sperm competition. We calculated residual values of testis weight from a regression plot of combined testes weight against body weight. We compared genera with relatively small testes (negative residuals) with those with relatively large testes (positive residuals). Midpiece volumes were significantly greater in sperm from primate genera with relatively large testes (mean ± s.e.m.: 9.758 ± 0.558 µm3 for genera with large testes; 5.360 ± 0.609 µm3 for genera with small testes; t = − 4.57, P < 0.001). No significant difference was found when the analysis was repeated for sperm-head volume and flagellum volume.
We also tested for a possible correlation between relative testis weight and sperm midpiece volume, and found a strong effect (r2 = 0.49, P < 0.0001; Fig.1b), although none of the other variables examined was correlated with relative testis weight. We conclude that sexual selection has probably influenced midpiece volume as well as testicular size.
Certain features of midpiece anatomy are highly heritable9. The volume of the midpiece is a more informative measure than its length, as this section contains a densely packed, helical array of mitochondria which provides energy for motility in the absence of glycolytic support10,11. The volume is therefore a likely indicator of the degree of mitochondrial loading.
Mitochondrial loading also has a bearing on flagellar hydrodynamics10,11, and the ATP content of the sperm of domestic fowl is positively correlated with its motility12. The greater midpiece volumes we have observed in primates with multiple-partner mating systems, in which sperm competition is most prevalent, may therefore result from selection for increased mitochondrial loading and greater motility. This would mirror the situation in domestic fowl, in which high sperm motility is correlated with successful sperm competition13.
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Anderson, M., Dixson, A. Motility and the midpiece in primates. Nature 416, 496 (2002). https://doi.org/10.1038/416496a
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DOI: https://doi.org/10.1038/416496a
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