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How sexual selection can drive the evolution of costly sperm ornamentation


Post-copulatory sexual selection (PSS), fuelled by female promiscuity, is credited with the rapid evolution of sperm quality traits across diverse taxa1. Yet, our understanding of the adaptive significance of sperm ornaments and the cryptic female preferences driving their evolution is extremely limited1,2. Here we review the evolutionary allometry of exaggerated sexual traits (for example, antlers, horns, tail feathers, mandibles and dewlaps), show that the giant sperm of some Drosophila species are possibly the most extreme ornaments3,4 in all of nature and demonstrate how their existence challenges theories explaining the intensity of sexual selection, mating-system evolution and the fundamental nature of sex differences5,6,7,8,9. We also combine quantitative genetic analyses of interacting sex-specific traits in D. melanogaster with comparative analyses of the condition dependence of male and female reproductive potential across species with varying ornament size to reveal complex dynamics that may underlie sperm-length evolution. Our results suggest that producing few gigantic sperm evolved by (1) Fisherian runaway selection mediated by genetic correlations between sperm length, the female preference for long sperm and female mating frequency, and (2) longer sperm increasing the indirect benefits to females. Our results also suggest that the developmental integration of sperm quality and quantity renders post-copulatory sexual selection on ejaculates unlikely to treat male–male competition and female choice as discrete processes.

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Figure 1: Allometry of sperm length and egg volume.
Figure 2: Evolutionary allometry of Drosophila sperm length in comparison with other, classic examples of sexually selected traits.
Figure 3: Comparison of intraspecific condition dependence of sperm length and egg volume across seven Drosophila species.

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The authors thank B. Reil for technical assistance and S. Dorus for helpful comments on the manuscript. Financial support for this research was provided by the National Science Foundation (grants DEB-9806649 to S.P. and DEB-1145965 to S.P., S.L., M.K.M. and J.M.B.), the Swiss National Science Foundation (Fellowships PA00P3_134191 and PZ00P3_154767 to S.L.), the National University of Singapore (Overseas Postdoctoral Fellowship to N.P.) and a generous gift from Mike and Jane Weeden to Syracuse University.

Author information

Authors and Affiliations



S.P. and S.L. conceived the research. S.P. and C.S. performed the reproductive potential experiments. S.P., C.S. and W.T.S. collected data for sperm and egg production allometry. S.L., S.P., M.K.M. and J.M.B. performed the male–female trait genetic covariance experiments. S.P., S.L., N.P. and S.H.B.L. performed the sperm length condition dependence experiment. S.L. and W.T.S. performed all statistical analyses. S.P. and S.L. wrote the paper.

Corresponding author

Correspondence to Scott Pitnick.

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Competing interests

The authors declare no competing financial interests.

Extended data figures and tables

Extended Data Figure 1 Phylogeny for the Drosophila comparative analyses of gamete allometry.

Molecular phylogeny of the 46 species based on ref. 40, with species added based on refs. 29 and 41. Owing to a lack of information on branch lengths, equal branch lengths were used.

Extended Data Figure 2 Phylogeny of the Phasianinae.

Tree topology of the Phasianinae in Supplementary Table 1 based on the molecular phylogeny of ref. 52. Owing to a lack of information on branch lengths, equal branch lengths were used.

Extended Data Figure 3 Phylogeny of the Bovidae.

Tree topology of the Bovidae in Supplementary Table 2 based on the molecular phylogenies of the 10kTrees Project60 and ref. 59. Equal branch lengths were used because of combining different trees.

Extended Data Figure 4 Lacking condition dependence of sperm length.

a, b, Comparison of sperm length (a) and male thorax length (b) between flies reared under benign and moderately stressful conditions. Each line connects the means of a nuclear genotype (n = 45), based on measurements of the same five males in a and b, and the box plots reflect the between-genotype variation for each treatment. On average, sperm length did not differ between the benign (mean ± s.d. = 1.853 ± 0.019 mm) and moderately stressful treatments (1.851 ± 0.021 mm; linear mixed-effects model controlling for genetic background: t = −0.57, P = 0.58), thereby reflecting no condition dependence. By contrast, all males reared under stressful conditions were smaller (thorax length: 0.816 ± 0.019 mm versus 0.892 ± 0.026 mm; t = −17.08, P < 0.0001), thus being strongly condition-dependent and highlighting the relatively higher cost of sperm length for low-quality males.

Extended Data Figure 5 Variation in investment per sperm and in spermatogenesis.

ad, Intact male fly above his reproductive tract (a, b) and a single spermatozoon (c, d) for Drosophila arizonae (a, c) and D. bifurca (b, d). Top panels and bottom panels depict equal magnification, respectively. All photos by S.P.

Extended Data Figure 6 Condition dependence of male and female reproductive potential in seven Drosophila species.

an, Intraspecific relationships between reproductive potential and body size as a proxy of condition for males (ag) and females (hn) of seven Drosophila species. Species are ordered from shortest (top) to longest (bottom) sperm. Dotted lines represent ordinary least-squares slopes and, where these regressions were statistically significant, solid lines indicate RMA slopes. For detailed statistics see Extended Data Table 3.

Extended Data Figure 7 Comparison of intraspecific variation in female thorax length.

Box plot reflecting the greater intraspecific standard deviation in female thorax length in D. hydei compared to the remaining species (Bartlett’s test of homogeneity of variances: K2 = 12.67, P = 0.05).

Extended Data Table 1 Statistics of evolutionary allometries in different taxa
Extended Data Table 2 Comparative data set of Drosophila gamete and body size
Extended Data Table 3 Intraspecific analyses of condition dependence of reproductive potential

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Lüpold, S., Manier, M., Puniamoorthy, N. et al. How sexual selection can drive the evolution of costly sperm ornamentation. Nature 533, 535–538 (2016).

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