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Gene-poor Y-chromosomes substantially impact male trait heritabilities and may help shape sexually dimorphic evolution

Heredity volume 130, pages 236–241 (2023)Cite this article

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Abstract

How natural selection facilitates sexually dimorphic evolution despite a shared genome is unclear. The patrilineal inheritance of Y-chromosomes makes them an appealing solution. However, they have largely been dismissed due to their gene-poor, heterochromatic nature and because the additive genetic variation necessary for adaptive evolution is theoretically difficult to maintain. Further, previous empirical work has revealed mostly Y-linked sign epistatic variance segregating within populations, which can often impede adaptive evolution. To assess the evolutionary impact of Y-linked variation, we established replicate populations in Drosophila simulans containing multiple Y-chromosomes (YN populations) or a single Y-chromosome variant (Y1 populations) drawn from a single population. We estimated male and female heritabilities for several traits known to be influenced by Y-chromosomes, including the number of sternopleural bristles, abdominal bristles, sex comb teeth, and tibia length. A decrease in YN heritabilities compared with Y1 would be consistent with Y-chromosome variation being sign epistatic. A decrease in Y1 heritabilities would be consistent with Y-chromosome variation being additive, though additive-by-additive epistatic variation cannot be entirely dismissed. Female heritability estimates served as controls and were not expected to differ. We found male Y1 populations exhibited lower heritabilities for all traits except tibia length; consistent with Y-linked additivity (on average YN trait heritabilities were 25% greater than Y1). Female estimates showed no difference. These data suggest Y-chromosomes should play an important role in male trait evolution and may even influence sexually dimorphic evolution by shaping traits shared by both sexes.

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Fig. 1: Graphical examples of physiological epistasis among Y-chromosomes and their genetic background.
Fig. 2: Creation of YN and Y1 populations.
Fig. 3: YN-Y1 heritability differences.
Fig. 4: YN-Y1 heritability differences for combined replicates.
Fig. 5: YN-Y1 genetic correlation differences.

Data availability

Data are available at Dryad: https://doi.org/10.5061/dryad.x69p8cznk.

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Acknowledgements

We thank Megan Danis, Kevin Cedeno, Saara Rasool, Mariam Sleem, Karishma Santadasani, Connor McDonnald, and Naiomy Gonzalez Carrero for assistance with sample processing.

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Authors and Affiliations

  1. University of Central Florida, Biological Sciences Building, 4110 Libra Dr., Orlando, FL, 32816, USA

    Tobias Møgelvang Nielsen, Jaden Baldwin & Kenneth M. Fedorka

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  1. Tobias Møgelvang Nielsen
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  2. Jaden Baldwin
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  3. Kenneth M. Fedorka
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Contributions

The study was conceived and designed by TMN and KMF, data collection was overseen by TMN and JB, data analysis was conducted by TMN and KMF, and the paper was authored by TMN and KMF.

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Correspondence to Kenneth M. Fedorka.

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Nielsen, T.M., Baldwin, J. & Fedorka, K.M. Gene-poor Y-chromosomes substantially impact male trait heritabilities and may help shape sexually dimorphic evolution. Heredity 130, 236–241 (2023). https://doi.org/10.1038/s41437-023-00596-8

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