Reconciling theories of dominance with the relative rates of adaptive substitution on sex chromosomes and autosomes

Mcdonough Y, Ruzicka F, Connallon T. 2024. Reconciling theories of dominance with the relative rates of adaptive substitution on sex chromosomes and autosomes. Proceedings of the National Academy of Sciences of the United States of America. 121(44), e2406335121.

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Author
Mcdonough, Yasmine; Ruzicka, FilipISTA; Connallon, Tim
Department
Abstract
The dominance of beneficial mutations is a key evolutionary parameter affecting the rate and genetic basis of adaptation, yet it is notoriously difficult to estimate. A leading method to infer it is to compare the relative rates of adaptive substitution for X-linked and autosomal genes, which—according to a classic model by Charlesworth et al. (1987)—is a simple function of the dominance of new beneficial mutations. Recent evidence that rates of adaptive substitution are faster for X-linked genes implies, accordingly, that beneficial mutations are usually recessive. However, this conclusion is incompatible with leading theories of dominance, which predict that beneficial mutations tend to be dominant or overdominant with respect to fitness. To address this incompatibility, we use Fisher’s geometric model to predict the distribution of fitness effects of new mutations and the relative rates of positively selected substitution on the X and autosomes. Previous predictions of faster-X theory emerge as a special case of our model in which the phenotypic effects of mutations are small relative to the distance to the phenotypic optimum. But as mutational effects become large relative to the optimum, we observe an elevated tempo of positively selected substitutions on the X relative to the autosomes across a broader range of dominance conditions, including those predicted by theories of dominance. Our results imply that, contrary to previous models, dominant and overdominant beneficial mutations can plausibly generate patterns of faster-X adaptation. We discuss resulting implications for genomic studies of adaptation and inferences of dominance.
Publishing Year
Date Published
2024-10-29
Journal Title
Proceedings of the National Academy of Sciences of the United States of America
Publisher
National Academy of Sciences
Acknowledgement
This work was supported by funds from the Australian Research Council and The School of Biological Sciences at Monash University. F.R. was funded by a H2020 Marie Skłodowska-Curie COFUND Action (No. 101034413). We thank three anonymous reviewers for suggestions that substantially improved the paper and breadth of the analysis.
Volume
121
Issue
44
Article Number
e2406335121
eISSN
IST-REx-ID

Cite this

Mcdonough Y, Ruzicka F, Connallon T. Reconciling theories of dominance with the relative rates of adaptive substitution on sex chromosomes and autosomes. Proceedings of the National Academy of Sciences of the United States of America. 2024;121(44). doi:10.1073/pnas.2406335121
Mcdonough, Y., Ruzicka, F., & Connallon, T. (2024). Reconciling theories of dominance with the relative rates of adaptive substitution on sex chromosomes and autosomes. Proceedings of the National Academy of Sciences of the United States of America. National Academy of Sciences. https://doi.org/10.1073/pnas.2406335121
Mcdonough, Yasmine, Filip Ruzicka, and Tim Connallon. “Reconciling Theories of Dominance with the Relative Rates of Adaptive Substitution on Sex Chromosomes and Autosomes.” Proceedings of the National Academy of Sciences of the United States of America. National Academy of Sciences, 2024. https://doi.org/10.1073/pnas.2406335121.
Y. Mcdonough, F. Ruzicka, and T. Connallon, “Reconciling theories of dominance with the relative rates of adaptive substitution on sex chromosomes and autosomes,” Proceedings of the National Academy of Sciences of the United States of America, vol. 121, no. 44. National Academy of Sciences, 2024.
Mcdonough Y, Ruzicka F, Connallon T. 2024. Reconciling theories of dominance with the relative rates of adaptive substitution on sex chromosomes and autosomes. Proceedings of the National Academy of Sciences of the United States of America. 121(44), e2406335121.
Mcdonough, Yasmine, et al. “Reconciling Theories of Dominance with the Relative Rates of Adaptive Substitution on Sex Chromosomes and Autosomes.” Proceedings of the National Academy of Sciences of the United States of America, vol. 121, no. 44, e2406335121, National Academy of Sciences, 2024, doi:10.1073/pnas.2406335121.
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