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

Nature Ecology & Evolution volume 5, pages 1394–1402 (2021)Cite this article

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Abstract

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.

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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.

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Data availability

Data generated and analysed in this study are available in the Dryad repository (https://doi.org/10.5061/dryad.dfn2z350x).

Code availability

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

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Acknowledgements

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.

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Authors and Affiliations

  1. Evolutionary Biology, Department of Ecology and Genetics, Uppsala University, Uppsala, Sweden

    Philipp Kaufmann, Arild Husby & Elina Immonen

  2. Department of Biological Sciences, Auburn University, Auburn, AL, USA

    Matthew E. Wolak

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Contributions

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.

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Correspondence to Philipp Kaufmann or Elina Immonen.

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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).

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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). https://doi.org/10.1038/s41559-021-01530-z

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