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A supergene in seaweed flies modulates male traits and female perception

View ORCID ProfileSwantje Enge, View ORCID ProfileClaire Mérot, View ORCID ProfileRaimondas Mozūraitis, Violeta Apšegaitė, View ORCID ProfileLouis Bernatchez, Gerrit A. Martens, Sandra Radžiutė, View ORCID ProfileHenrik Pavia, View ORCID ProfileEmma L. Berdan
doi: https://doi.org/10.1101/2021.06.30.450538
Swantje Enge
1Department of Marine Sciences, The University of Gothenburg, Göteborg, Sweden
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Claire Mérot
2Département de biologie, Institut de Biologie Intégrative et des Systèmes (IBIS), Université Laval, Québec, Canada
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Raimondas Mozūraitis
3Department of Zoology, Stockholm University, Stockholm, Sweden
4Laboratory of Chemical and Behavioural Ecology, Institute of Ecology, Nature Research Centre, Vilnius, Lithuania
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Violeta Apšegaitė
4Laboratory of Chemical and Behavioural Ecology, Institute of Ecology, Nature Research Centre, Vilnius, Lithuania
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Louis Bernatchez
2Département de biologie, Institut de Biologie Intégrative et des Systèmes (IBIS), Université Laval, Québec, Canada
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Gerrit A. Martens
5Institute of Zoology, University of Hamburg, Hamburg, Germany
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Sandra Radžiutė
4Laboratory of Chemical and Behavioural Ecology, Institute of Ecology, Nature Research Centre, Vilnius, Lithuania
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Henrik Pavia
1Department of Marine Sciences, The University of Gothenburg, Göteborg, Sweden
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Emma L. Berdan
1Department of Marine Sciences, The University of Gothenburg, Göteborg, Sweden
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  • For correspondence: emma.berdan@gmail.com
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Summary

Supergenes, tightly linked allelic combinations that underlie complex adaptive phenotypes represent a critical mechanism protecting intra-specific polymorphism [1, 2]. Supergenes represent some of the best examples of balancing selection in nature and there is increasing evidence that disassortative mating, when individuals preferentially mate with dissimilar phenotypes, is a key force stabilizing supergene polymorphisms. Yet, the underlying biological mechanisms and genetic basis of disassortative mating remain poorly known. Here, we examine a possible mechanism of disassortative mating driven by female mate choice in relation to the overdominant Cf-Inv(1) supergene in the seaweed fly Coelopa frigida by investigating chemical communication and its genomic architecture. We show that Cf-Inv(1) strongly affects chemical signaling; cuticular hydrocarbon (CHC) composition differed between genotypes in males but not females across two continents. In tandem, Cf-Inv(1) affected female perception of these compounds; females are able to sense 36 compounds from the male CHC cocktail but show differential perception between genotypes for almost half of them. This indicates that the genetic underpinnings of male traits and female perceptions are tightly linked within Cf-Inv(1) which likely facilitates disassortative mating [3]. A differential expression approach based on candidate genes for CHC biosynthesis and odorant detection revealed differential expression for CHC biosynthesis in males alone but broad changes in odorant receptors across both sexes. Furthermore, odorant genes clustered together within Cf-Inv(1), with some of them differing between arrangements by 8.3% at the protein level, suggesting evolution via tandem duplication then divergence. We propose that the tight linkage between overdominant loci, male traits, and female perception has helped to maintain the Cf-Inv(1) polymorphism across its range in the face of supergene degeneration.

Competing Interest Statement

The authors have declared no competing interest.

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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-NC-ND 4.0 International license.
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Posted July 01, 2021.
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A supergene in seaweed flies modulates male traits and female perception
Swantje Enge, Claire Mérot, Raimondas Mozūraitis, Violeta Apšegaitė, Louis Bernatchez, Gerrit A. Martens, Sandra Radžiutė, Henrik Pavia, Emma L. Berdan
bioRxiv 2021.06.30.450538; doi: https://doi.org/10.1101/2021.06.30.450538
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A supergene in seaweed flies modulates male traits and female perception
Swantje Enge, Claire Mérot, Raimondas Mozūraitis, Violeta Apšegaitė, Louis Bernatchez, Gerrit A. Martens, Sandra Radžiutė, Henrik Pavia, Emma L. Berdan
bioRxiv 2021.06.30.450538; doi: https://doi.org/10.1101/2021.06.30.450538

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