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Sexual conflict drives micro- and macroevolution of sexual dimorphism in immunity

Basabi Bagchi, Quentin Corbel, Imroze Khan, Ellen Payne, Devshuvam Banerji, Johanna Liljestrand-Rönn, Ivain Martinossi-Allibert, Julian Baur, Ahmed Sayadi, Elina Immonen, Göran Arnqvist, Irene Söderhäll, David Berger
doi: https://doi.org/10.1101/2020.12.20.423717
Basabi Bagchi
1Department of Biological Sciences, Ashoka University
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Quentin Corbel
2Department of Ecology and Genetics, Program of Animal Ecology. Evolutionary Biology Centre, Uppsala University
3Cavanilles Institute of Biodiversity and Evolutionary Biology, University of Valencia
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Imroze Khan
1Department of Biological Sciences, Ashoka University
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Ellen Payne
2Department of Ecology and Genetics, Program of Animal Ecology. Evolutionary Biology Centre, Uppsala University
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Devshuvam Banerji
1Department of Biological Sciences, Ashoka University
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Johanna Liljestrand-Rönn
2Department of Ecology and Genetics, Program of Animal Ecology. Evolutionary Biology Centre, Uppsala University
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Ivain Martinossi-Allibert
2Department of Ecology and Genetics, Program of Animal Ecology. Evolutionary Biology Centre, Uppsala University
5Department of Organismal Biology, Evolutionary Biology Centre, Uppsala University
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Julian Baur
2Department of Ecology and Genetics, Program of Animal Ecology. Evolutionary Biology Centre, Uppsala University
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Ahmed Sayadi
2Department of Ecology and Genetics, Program of Animal Ecology. Evolutionary Biology Centre, Uppsala University
6Department of Chemistry, Biochemistry, Uppsala University
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Elina Immonen
4Department of Ecology and Genetics, Program of Evolutionary Biology. Evolutionary Biology Centre, Uppsala University
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Göran Arnqvist
2Department of Ecology and Genetics, Program of Animal Ecology. Evolutionary Biology Centre, Uppsala University
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Irene Söderhäll
7Department of Organismal Biology, Program of Comparative Physiology. Uppsala University
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David Berger
2Department of Ecology and Genetics, Program of Animal Ecology. Evolutionary Biology Centre, Uppsala University
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  • For correspondence: david.berger@ebc.uu.se
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Abstract

Background Sexual selection can have major effects on mating rates and sex-specific costs of mating and may thereby influence sex-differences in immunity as well as associated host-pathogen dynamics. Yet, experimental evidence linking the mating system to evolved sexual dimorphism in immunity are scarce and the direct effects of mating rate on immunity are not well established. Here, we use transcriptomic analyses, experimental evolution and phylogenetic comparative methods to study the association between the mating system and sexual dimorphism in immunity in seed beetles, where mating causes internal injuries in females.

Results We demonstrate that female phenoloxidase (PO) activity, involved in wound healing and defence against parasitic infections, is elevated relative to males. This difference is accompanied by concomitant sex-differences in the expression of genes in the pro-phenoloxidase activating cascade. We document substantial phenotypic plasticity in female PO activity in response to mating and show that experimental evolution under enforced monogamy (resulting in low remating rates and sexual conflict relative to natural polygamy) rapidly decreases female (but not male) PO activity. Moreover, monogamous females have evolved increased tolerance to bacterial infection unrelated to mating, implying that female responses to costly mating may trade off with other aspects of immune defence, an hypothesis which broadly accords with the documented sex differences in gene expression. Finally, female (but not male) PO activity shows correlated evolution with the perceived harmfulness of male genitalia across 12 species of seed beetles, suggesting that sexual conflict has a significant influence on sexual dimorphisms in immunity in this group of insects.

Conclusions Our study provides insights into the links between sexual conflict and sexual dimorphism in immunity at the molecular and phenotypic level and suggests that selection pressures moulded by mating interactions can lead to a sex-specific mosaic of immune responses with important implications for host-pathogen dynamics in sexually reproducing organisms.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • ↵* Equal contribution and presented in alphabetical order

  • Revisions made to main text, figures and new Supplementary Information 6 included.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-ND 4.0 International license.
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Posted April 07, 2021.
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Sexual conflict drives micro- and macroevolution of sexual dimorphism in immunity
Basabi Bagchi, Quentin Corbel, Imroze Khan, Ellen Payne, Devshuvam Banerji, Johanna Liljestrand-Rönn, Ivain Martinossi-Allibert, Julian Baur, Ahmed Sayadi, Elina Immonen, Göran Arnqvist, Irene Söderhäll, David Berger
bioRxiv 2020.12.20.423717; doi: https://doi.org/10.1101/2020.12.20.423717
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Sexual conflict drives micro- and macroevolution of sexual dimorphism in immunity
Basabi Bagchi, Quentin Corbel, Imroze Khan, Ellen Payne, Devshuvam Banerji, Johanna Liljestrand-Rönn, Ivain Martinossi-Allibert, Julian Baur, Ahmed Sayadi, Elina Immonen, Göran Arnqvist, Irene Söderhäll, David Berger
bioRxiv 2020.12.20.423717; doi: https://doi.org/10.1101/2020.12.20.423717

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