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The roles of sexual selection and sexual conflict in shaping patterns of genome and transcriptome variation

Abstract

Sexual dimorphism is one of the most prevalent, and often the most extreme, examples of phenotypic variation within species, and arises primarily from genomic variation that is shared between females and males. Many sexual dimorphisms arise through sex differences in gene expression, and sex-biased expression is one way that a single, shared genome can generate multiple, distinct phenotypes. Although many sexual dimorphisms are expected to result from sexual selection, and many studies have invoked the possible role of sexual selection to explain sex-specific traits, the role of sexual selection in the evolution of sexually dimorphic gene expression remains difficult to differentiate from other forms of sex-specific selection. In this Review, we propose a holistic framework for the study of sex-specific selection and transcriptome evolution. We advocate for a comparative approach, across tissues, developmental stages and species, which incorporates an understanding of the molecular mechanisms, including genomic variation and structure, governing gene expression. Such an approach is expected to yield substantial insights into the evolution of genetic variation and have important applications in a variety of fields, including ecology, evolution and behaviour.

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Fig. 1: The relationship between intralocus sexual conflict, sex-specific selection landscapes, sexual dimorphism and some predictions for how variation in male–female gene expression might be impacted by ongoing intralocus conflict.
Fig. 2: A schematic of mechanisms that facilitate genetic variation, transcriptional variation and the ability to respond to selection.

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Acknowledgements

We acknowledge Ngāi Tūāhuriri, the Wurundjeri and Boon Wurrung peoples of the Kulin nation, and the xʷməθkʷəy̓əm (Musqueam) people, upon whose lands this work was conducted. This work was supported by the Marsden Fund Council from government funding, managed by Royal Society Te Apārangi (grant UOC1904) and the Australian Research Council (FT190100014 and DP220100245). J.E.M. gratefully acknowledges funding from the Natural Sciences and Engineering Research Council of Canada and a Canada 150 Research Chair. We thank T. Connallon, A. Wright and A. Jones for feedback on early drafts of this manuscript.

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S.P.F. conceived this work and all concepts were shaped by discussions with N.M.T., E.R.B., B.B.M.W. and J.E.M.; S.P.F., N.M.T. and E.R.B. wrote the first draft of the manuscript, and N.M.T., E.R.B., B.B.M.W., J.E.M. and S.P.F. edited subsequent drafts.

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Correspondence to Sarah P. Flanagan.

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Tosto, N.M., Beasley, E.R., Wong, B.B.M. et al. The roles of sexual selection and sexual conflict in shaping patterns of genome and transcriptome variation. Nat Ecol Evol 7, 981–993 (2023). https://doi.org/10.1038/s41559-023-02019-7

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