Skip to main content

Thank you for visiting You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Rapid evolution of sexual size dimorphism facilitated by Y-linked genetic variance


Sexual dimorphism is ubiquitous in nature but its evolution is puzzling given that the mostly shared genome constrains independent evolution in the sexes. Sex differences should result from asymmetries between the sexes in selection or genetic variation but studies investigating both simultaneously are lacking. Here, we combine a quantitative genetic analysis of body size variation, partitioned into autosomal and sex chromosome contributions and ten generations of experimental evolution to dissect the evolution of sexual body size dimorphism in seed beetles (Callosobruchus maculatus) subjected to sexually antagonistic or sex-limited selection. Female additive genetic variance (VA) was primarily linked to autosomes, exhibiting a strong intersexual genetic correlation with males (\(r_{\mathrm{{m,f}}}^{\mathrm{a}}\) = 0.926), while X- and Y-linked genes further contributed to the male VA and X-linked genes contributed to female dominance variance. Consistent with these estimates, sexual body size dimorphism did not evolve in response to female-limited selection but evolved by 30–50% under male-limited and sexually antagonistic selection. Remarkably, Y-linked variance alone could change dimorphism by 30%, despite the C. maculatus Y chromosome being small and heterochromatic. Our results demonstrate how the potential for sexual dimorphism to evolve depends on both its underlying genetic basis and the nature of sex-specific selection.

This is a preview of subscription content, access via your institution

Access options

Rent or buy this article

Prices vary by article type



Prices may be subject to local taxes which are calculated during checkout

Fig. 1: Overview of the posterior estimates for genetic variances.
Fig. 2: Change in sexual dimorphism (SD) over the course of ten generations of artificial family-level selection.
Fig. 3: Trajectory of male (left) and female (right) body size evolution under the five different selection regimes.
Fig. 4: Effect of Y chromosome on body size after introgression into an isogenic background.

Similar content being viewed by others

Data availability

Data generated and analysed in this study are available in the Dryad repository (

Code availability

R code for the MCMCglmm and ASReml-R 4.0 is provided in the Supplementary Information.


  1. Darwin, C. The Descent of Man, and Selection in Relation of Sex (John Murray, 1871).

  2. Andersson, M. Sexual Selection (Princeton Univ. Press, 1994).

  3. Fairbairn, D. J. Odd Couples: Extraordinary Differences between the Sexes in the Animal Kingdom (Princeton Univ. Press, 2013).

  4. Cox, R. M. & Calsbeek, R. Sexually antagonistic selection, sexual dimorphism, and the resolution of intralocus sexual conflict. Am. Nat. 173, 176–187 (2009).

    Article  PubMed  Google Scholar 

  5. Lande, R. Sexual dimorphism, sexual selection, and adaptation in polygenic characters. Evolution 34, 292–305 (1980).

    Article  PubMed  Google Scholar 

  6. Mezey, J. G. & Houle, D. The dimensionality of genetic variation for wing shape in Drosophila melanogaster. Evolution 59, 1027–1038 (2005).

    PubMed  Google Scholar 

  7. Gomulkiewicz, R. & Houle, D. Demographic and genetic constraints on evolution. Am. Nat. 174, 218–229 (2009).

    Article  Google Scholar 

  8. Rice, W. R. & Chippindale, A. K. Intersexual ontogenetic conflict. J. Evol. Biol. 14, 685–693 (2001).

    Article  Google Scholar 

  9. Bonduriansky, R. & Chenoweth, S. F. Intralocus sexual conflict. Trends Ecol. Evol. 24, 280–288 (2009).

    Article  PubMed  Google Scholar 

  10. Poissant, J., Wilson, A. J. & Coltman, D. W. Sex-specific genetic variance and the evolution of sexual dimorphism: a systematic review of cross-sex genetic correlations. Evolution 64, 97–107 (2010).

    Article  PubMed  Google Scholar 

  11. Delph, L. F., Gehring, J. L., Frey, F. M., Arntz, A. M. & Levri, M. Genetic constraints on floral evolution in a sexually dimorphic plant revealed by artificial selection. Evolution 58, 1936–1946 (2004).

    PubMed  Google Scholar 

  12. Tigreros, N. & Lewis, S. M. Direct and correlated responses to artificial selection on sexual size dimorphism in the flour beetle, Tribolium castaneum. J. Evol. Biol. 24, 835–842 (2011).

    Article  CAS  PubMed  Google Scholar 

  13. Reeve, J. P. & Fairbairn, D. J. Sexual size dimorphism as a correlated response to selection on body size: an empirical test of the quantitative genetic model. Evolution 50, 1927–1938 (1996).

    Article  PubMed  Google Scholar 

  14. Stewart, A. D. & Rice, W. R. Arrest of sex-specific adaptation during the evolution of sexual dimorphism in Drosophila. Nat. Ecol. Evol. 2, 1507–1513 (2018).

    Article  PubMed  Google Scholar 

  15. Delph, L. F., Steven, J. C., Anderson, I. A., Herlihy, C. R. & Brodie, E. D. Elimination of a genetic correlation between the sexes via artificial correlational selection. Evolution 65, 2872–2880 (2011).

    Article  PubMed  Google Scholar 

  16. Rice, W. R. Sex chromosomes and the evolution of sexual dimorphism. Evolution 38, 735–742 (1984).

    Article  PubMed  Google Scholar 

  17. Rice, W. R. Evolution of the Y sex chromosome in animals. Bioscience 46, 331–343 (1996).

    Article  Google Scholar 

  18. Charlesworth, B. & Charlesworth, D. The degeneration of Y chromosomes. Philos. Trans. R. Soc. Lond. B 355, 1563–1572 (2000).

    Article  CAS  Google Scholar 

  19. Delph, L. F., Arntz, A. M., Scotti-Saintagne, C. & Scotti, I. The genomic architecture of sexual dimorphism in the dioecious plant Silene latifolia. Evolution 64, 2873–2886 (2010).

    PubMed  Google Scholar 

  20. Griffin, R. M., Le Gall, D., Schielzeth, H. & Friberg, U. Within-population Y-linked genetic variation for lifespan in Drosophila melanogaster. J. Evol. Biol. 28, 1940–1947 (2015).

    Article  CAS  PubMed  Google Scholar 

  21. Charlesworth, D. The guppy sex chromosome system and the sexually antagonistic polymorphism hypothesis for Y chromosome recombination suppression. Genes 9, 264 (2018).

    Article  PubMed Central  CAS  Google Scholar 

  22. Evans, S. R., Schielzeth, H., Forstmeier, W., Sheldon, B. C. & Husby, A. Nonautosomal genetic variation in carotenoid coloration. Am. Nat. 184, 374–383 (2014).

    Article  PubMed  Google Scholar 

  23. Chippindale, A. K. & Rice, W. R. Y chromosome polymorphism is a strong determinant of male fitness in Drosophila melanogaster. Proc. Natl Acad. Sci. USA 98, 5677–5682 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Skaletsky, H. et al. The male-specific region of the human Y chromosome is a mosaic of discrete sequence classes. Nature 423, 825–837 (2003).

    Article  CAS  PubMed  Google Scholar 

  25. Maan, A. A. et al. The Y chromosome: a blueprint for men’s health? Eur. J. Hum. Genet. 25, 1181–1188 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Prokop, J. W. & Deschepper, C. F. Chromosome Y genetic variants: impact in animal models and on human disease. Physiol. Genomics 47, 525–537 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Ruzicka, F. & Connallon, T. Is the X chromosome a hot spot for sexually antagonistic polymorphisms? Biases in current empirical tests of classical theory. Proc. R. Soc. Lond. B 287, 20201869 (2020).

    Google Scholar 

  28. Husby, A., Schielzeth, H., Forstmeier, W., Gustafsson, L. & Qvarnström, A. Sex chromosome linked genetic variance and the evolution of sexual dimorphism of quantitative traits. Evolution 67, 609–619 (2013).

    Article  CAS  PubMed  Google Scholar 

  29. Dean, R. & Mank, J. E. The role of sex chromosomes in sexual dimorphism: discordance between molecular and phenotypic data. J. Evol. Biol. 27, 1443–1453 (2014).

    Article  CAS  PubMed  Google Scholar 

  30. Fry, J. D. The genomic location of sexually antagonistic variation: some cautionary comments. Evolution 64, 1510–1516 (2010).

    PubMed  Google Scholar 

  31. Spencer, H. G. & Priest, N. K. The evolution of sex-specific dominance in response to sexually antagonistic selection. Am. Nat. 187, 658–666 (2016).

    Article  PubMed  Google Scholar 

  32. Barson, N. J. et al. Sex-dependent dominance at a single locus maintains variation in age at maturity in salmon. Nature 528, 405–408 (2015).

    Article  CAS  PubMed  Google Scholar 

  33. Pearse, D. E. et al. Sex-dependent dominance maintains migration supergene in rainbow trout. Nat. Ecol. Evol. 3, 1731–1742 (2019).

    Article  PubMed  Google Scholar 

  34. Grieshop, K. & Arnqvist, G. Sex-specific dominance reversal of genetic variation for fitness. PLoS Biol. 16, e2006810 (2018).

  35. Reinhold, K. & Engqvist, L. The variability is in the sex chromosomes. Evolution 67, 3662–3668 (2013).

    Article  PubMed  Google Scholar 

  36. Mank, J. E. & Ellegren, H. Sex-linkage of sexually antagonistic genes is predicted by female, but not male, effects in birds. Evolution 63, 1464–1472 (2009).

    Article  CAS  PubMed  Google Scholar 

  37. Sayadi, A. et al. The genomic footprint of sexual conflict. Nat. Ecol. Evol. 3, 1725–1730 (2019).

    Article  PubMed  Google Scholar 

  38. Angus, R. B., Dellow, J., Winder, C. & Credland, P. F. Karyotype differences among four species of Callosobruchus Pic (Coleoptera: Bruchidae). J. Stored Prod. Res. 47, 76–81 (2011).

    Article  Google Scholar 

  39. Van Hooft, P. et al. Rainfall-driven sex-ratio genes in African buffalo suggested by correlations between Y-chromosomal haplotype frequencies and foetal sex ratio. BMC Evol. Biol. 10, 106 (2010).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  40. Postma, E., Spyrou, N., Rollins, L. A. & Brooks, R. C. Sex-dependent selection differentially shapes genetic variation on and off the guppy Y chromosome. Evolution 65, 2145–2156 (2011).

    Article  PubMed  Google Scholar 

  41. Clark, A. G. Natural selection and Y-linked polymorphism. Genetics 115, 569–577 (1987).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Jiang, P. P., Hartl, D. L. & Lemos, B. Y not a dead end: epistatic interactions between Y-linked regulatory polymorphisms and genetic background affect global gene expression in Drosophila melanogaster. Genetics 186, 109–118 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Lemos, B., Araripe, L. O. & Hartl, D. L. Polymorphic Y chromosomes harbor cryptic variation with manifold functional consequences. Science 319, 91–93 (2008).

    Article  CAS  PubMed  Google Scholar 

  44. Lund-Hansen, K. K., Olito, C., Morrow, E. H. & Abbott, J. K. Sexually antagonistic coevolution between the sex chromosomes of Drosophila melanogaster. Proc. Natl Acad. Sci. USA 118, e2003359 (2021).

    Article  CAS  Google Scholar 

  45. Sayres, M. A. W. Genetic diversity on the sex chromosomes. Genome Biol. Evol. 10, 1064–1078 (2018).

    Article  Google Scholar 

  46. Connallon, T. & Clark, A. G. Balancing selection in species with separate sexes: insights from Fisher’s geometric model. Genetics 197, 991–1006 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  47. McGlothlin, J. W., Cox, R. M. & Brodie, E. D. Sex-specific selection and the evolution of between-sex genetic covariance. J. Hered. 110, 422–432 (2019).

    Article  PubMed  Google Scholar 

  48. Arnqvist, G. & Tuda, M. Sexual conflict and the gender load: correlated evolution between population fitness and sexual dimorphism in seed beetles. Proc. R. Soc. B 277, 1345–1352 (2010).

    Article  PubMed  Google Scholar 

  49. Berger, D., Berg, E. C., Widegren, W., Arnqvist, G. & Maklakov, A. A. Multivariate intralocus sexual conflict in seed beetles. Evolution 68, 3457–3469 (2014).

    Article  PubMed  Google Scholar 

  50. Berger, D. et al. Intralocus sexual conflict and the tragedy of the commons in seed beetles. Am. Nat. 188, 98–112 (2016).

    Article  Google Scholar 

  51. Fairbairn, D. J. & Roff, D. A. The quantitative genetics of sexual dimorphism: assessing the importance of sex-linkage. Heredity 97, 319–328 (2006).

    Article  CAS  PubMed  Google Scholar 

  52. R Core Team. R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2020).

  53. Hadfield, J. D. MCMC methods for multi-response generalized linear mixed models: the MCMCglmm R package. J. Stat. Softw. 33, 1–22 (2010).

    Article  Google Scholar 

  54. Wolak, M. E. Nadiv: an R package to create relatedness matrices for estimating non-additive genetic variances in animal models. Methods Ecol. Evol. 3, 792–796 (2012).

    Article  Google Scholar 

  55. Lynch, M. & Walsh, B. Genetics and Analysis of Quantitative Traits (Sinauer, 1998).

Download references


We thank J. Liljestrand-Rönn for help in the laboratory and D. Scofield for computational support. We also thank the beetle research group at Uppsala University for valuable discussions and G. Arnqvist and S. Karrenberg for comments on the earlier draft of the manuscript. The computations were enabled by resources in project SNIC 2019/8-55 provided by the Swedish National Infrastructure for Computing at UPPMAX, partially founded by the Swedish Research Council. This work was funded by the grants from the Swedish Research Council (grant no. 2019-05038) and Carl Trygger Foundation (grant no. CTS-18:163) to E.I.

Author information

Authors and Affiliations



The study idea and the general experimental design were conceived by E.I., while P.K. developed further the details of the experimental design, carried out the experiments and collected the data with assistance from E.I. Data analysis and preparation of results were done by P.K. with input and assistance from E.I., M.E.W. and A.H. The initial manuscript was written by P.K. and E.I. with substantial contributions from all the authors on later versions.

Corresponding authors

Correspondence to Philipp Kaufmann or Elina Immonen.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Peer review information Nature Ecology & Evolution thanks the anonymous reviewers for their contribution to the peer review of this work. Peer reviewer reports are available.

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Extended data

Extended Data Fig. 1 Genetic (co)variance estimates.

Marginal posterior distribution of the genetic (co)variances in females and males as a histogram and density curve (black solid line), with the 95% credible intervals (purple dashed line), mean (red dotted line) and the prior distribution (blue solid line). Additionally, we also show the restricted likelihood-based mean (yellow vertical line) for a comparison. a & b, Autosomal additive genetic variance is larger in females than in males. c, Genetic covariance between males and females d, Y-linked additive genetic variance. e & f, X-linked additive genetic variance in females and males. g & h, Dominance variance in females and males. i & j, Residual variance in females and males.

Extended Data Fig. 2 Genetic (co)variance estimates of a model with X-linked dominance variance partitioning.

Marginal posterior distribution of the genetic (co)variances as a histogram and density (black solid line), 95% credible interval (purple dashed line), mean (red dotted line) and the prior distribution (blue solid line). Additionally, we also show the restricted likelihood-based mean (yellow vertical line). a & b, Autosomal additive genetic variance is larger in females than in males. c, Genetic covariance between males and females. d, Y-linked additive genetic variance. (e & f, X-linked additive genetic variance in females and males. g & h, Dominance variance in females and males. i, X-linked dominance variance in females. j & k, Residual variance in females and males.

Extended Data Fig. 3 Y-lineage effect in the pedigree analysis.

Estimated mean Y-lineage effect and their 95% credible interval (grey bar) in the pedigree analysis. Positive values make males on average larger while negative values make males on average smaller. a, There is a significant positive correlation between Y-lineage effect and body size of males that carry this Y lineage (t value = 16.61, p value = <0.0001). b, We see no correlation between the Y-lineage effect and the body size of related females (t value = 0.014, p value = <0.989). c, Overall, there is a significant positive correlation between male and female body size within patrilines.

Extended Data Fig. 4 Y-lineage frequency changes in response to artificial selection.

a, Y-lineage frequency changes over the course of 10 generations of artificial selection in 5 different selection regimes (C = drift control, SA = sexually antagonistic selection, SL = sex-limited selection for; m↓ small males, m↑ large males, f↑ large females), each selection regime has 2 replicate lines. All selection lines started from the same ancestral population (G0), shown with the big circle. b, The Y lineages are colour coded according to their estimated effect on male body size. Note that Y-lineage ≠ Y haplotype. The Y lineage represent each founder male (GGP) in our 4-generation pedigree, and most of these Y lineages are likely the same haplotype (for example all Y lineages in dark blue have a very similar effect on male body size).

Extended Data Fig. 5 Phenotypic body size variance in the pedigree population.

Body size is normally distributed in both sexes, indicating that size is a polygenic trait. Males are on average lighter than females (\(\bar z_m\) = 4.43, \(\bar z_f\) = 6.39) and body size is less variable in males than in females (\(\sigma _{z,m}^2\) = 0.410, \(\sigma _{z,f}^2\) = 0.478, F = 0.857, dfnum = 3702, dfdenum = 3642, p < 0.001).

Supplementary information

Supplementary Information

Supplementary Tables 1–4, Fig. 1 and R code.

Reporting Summary

Peer Review Information

Rights and permissions

Reprints and Permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kaufmann, P., Wolak, M.E., Husby, A. et al. Rapid evolution of sexual size dimorphism facilitated by Y-linked genetic variance. Nat Ecol Evol 5, 1394–1402 (2021).

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI:

This article is cited by


Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing