Experimental sexual selection reveals rapid evolutionary divergence in sex-specific transcriptomes and their interactions following mating.

P Veltsos, D Porcelli, Y Fang, AR Cossins, Michael G Ritchie, Rhonda Snook

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Post copulatory interactions between the sexes in internally fertilizing species elicits both sexual conflict and sexual selection. Macroevolutionary and comparative studies have linked these processes to rapid transcriptomic evolution in sex-specific tissues and substantial transcriptomic post mating responses in females, patterns of which are altered when mating between reproductively isolated species. Here, we tested multiple predictions arising from sexual selection and conflict theory about the evolution of sex-specific and tissue-specific gene expression and the post mating response at the microevolutionary level. Following over 150 generations of experimental evolution under either reduced (enforced monogamy) or elevated (polyandry) sexual selection in Drosophila pseudoobscura, we found a substantial effect of sexual selection treatment on transcriptomic divergence in virgin male and female reproductive tissues (testes, male accessory glands, the female reproductive tract and ovaries). Sexual selection treatment also had a dominant effect on the post mating response, particularly in the female reproductive tract - the main arena for sexual conflict - compared to ovaries. This effect was asymmetric with monandry females typically showing more post mating responses than polyandry females, with enriched gene functions varying across treatments. The evolutionary history of the male partner had a larger effect on the post mating response of monandry females, but females from both sexual selection treatments showed unique patterns of gene expression and gene function when mating with males from the alternate treatment. Our microevolutionary results mostly confirm comparative macroevolutionary predictions on the role of sexual selection on transcriptomic divergence and altered gene regulation arising from divergent coevolutionary trajectories between sexual selection treatments.
Original languageEnglish
Pages (from-to)3374-3388
Number of pages15
JournalMolecular Ecology
Issue number12
Publication statusPublished - Jun 2022

Bibliographical note

Funding Information:
This work was supported by the Natural Environment Research Council (NE/I014632/1 to M.G.R., A.R.C., and R.R.S), the Natural Environment Research Council Biomolecular Analysis Facility (NBAF654 to M.G.R), and the Swedish Research Council (Vetenskapsrådet; 2018‐04598 to R.R.S). We thank the many people that have contributed to the generation and maintenance of the experimental sexual selection lines in RRS’s laboratory, R Axel W Wiberg for help with dissections, and Chris Wheat and Rachel Steward for ideas to represent GO terms. We also thank three anonymous reviewers for comments that substantially improved the manuscript.

Publisher Copyright:
© 2022 The Authors. Molecular Ecology published by John Wiley & Sons Ltd.

Copyright 2022 Elsevier B.V., All rights reserved.


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