Admixture Can Readily Lead to the Formation of Supergenes Paul Jay, Thomas Aubier, Mathieu Joron

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Admixture Can Readily Lead to the Formation of Supergenes Paul Jay, Thomas Aubier, Mathieu Joron Admixture can readily lead to the formation of supergenes Paul Jay, Thomas Aubier, Mathieu Joron To cite this version: Paul Jay, Thomas Aubier, Mathieu Joron. Admixture can readily lead to the formation of supergenes. 2021. hal-03101072 HAL Id: hal-03101072 https://hal.archives-ouvertes.fr/hal-03101072 Preprint submitted on 6 Jan 2021 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. bioRxiv preprint doi: https://doi.org/10.1101/2020.11.19.389577; this version posted November 19, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. Admixture can readily lead to the formation of supergenes Paul Jay1 *, Thomas G. Aubier1,2 *, and Mathieu Joron1 1CEFE, CNRS, Université de Montpellier, Université Paul Valery, Montpellier 3, EPHE, IRD, Montpellier, France 2Department of Evolutionary Biology and Environmental Studies, University of Zurich, Zurich, Switzerland *These authors contributed equally. Supergenes are genetic architectures allowing the segregation of populations (6,8, 10, 17, 18). Inversions suppress recombi- alternative combinations of alleles underlying complex pheno- nation in heterozygotes, and are therefore prone to capture types. The co-segregation of sets of alleles at linked loci is deter- and accumulate deleterious mutations (18–20). This reces- mined by polymorphic chromosomal rearrangements suppress- sive mutational load may generate balancing selection and ing recombination locally. Supergenes are involved in many contribute to polymorphism at supergenes (18). Neverthe- complex polymorphisms, including sexual, color or behavioral less, while the maintenance of supergene alleles is theoret- polymorphisms in numerous plants, fungi, mammals, fish, and ically well understood, how these differentiated functional insects. Despite a long history of empirical and theoretical re- search, the genetic origin of supergenes remains poorly under- haplotypes arise remains a challenging question (21–24) stood. Here, using a population genetic two-island model, we The difficulty of solving the origin of supergenes can be ap- explore how the evolution of overdominant chromosomal inver- preciated using the metaphor of the fitness landscape intro- sions may lead to the formation of supergenes. We show that the duced by Wright (25). A population harbouring a supergene evolution of inversions in differentiated populations connected can be seen as a population with several non-recombining by gene flow leads to an increase in frequency of poorly adapted, haplotypes underlying distinct phenotypes corresponding to immigrant haplotypes. When inversions are associated with re- alternative fitness peaks. The separation of fitness peaks cessive fitness cost hampering their fixation (such as a muta- in this model implies the existence of epistatic interac- tional load), this results in the formation of supergenes. These tions; supergene haplotypes link together co-adapted alle- results provide a realistic scenario for the evolution of super- les, and recombinant haplotypes thus display poor fitness genes and inversion polymorphisms in general, and bring new (16, 22, 23, 26). To reach this situation, a polymorphic pop- light into the importance of admixture in the formation of new genetic architectures. ulation may have evolved from a monomorphic populations. This implies a peak shift, across a fitness valley, forming dif- Polymorphism | Genome evolution | Inversion | Load | Overdominance | Pop- ferentiated haplotypes which do not reach fixation and thus ulation genetic model segregate under balancing selection with an ancestral form. Correspondence: [email protected] Peak shifts may occur via genetic drift (‘shifting balance the- Discrete polymorphisms are widespread in nature. Besides ory’ (25)), via varying selective conditions (27), via major the ubiquitous polymorphism of sexual and mating types effect mutations (23), or when mutation rate and population (1,2), classic examples of discrete polymorphisms involving size are high (28). Nevertheless, the processes underlying multiple functional loci include polymorphic immune sys- peak shifts do not explain the maintenance of ancestral and tems in vertebrates (3–5), and color polymorphisms in several derived adaptive strategies in a polymorphism. birds (6–8), insects (9–11), snails (12, 13) and lizards (14). The puzzle of the origin and the maintenance of polymor- Supergenes are genetic architectures which are often found to phisms at supergenes rests on the antagonistic effects of re- underlie discrete polymorphisms by preventing the formation combination on the evolution of new combination of co- of intermediate maladapted phenotypes. Supergenes are gen- adapted alleles. On the one hand, recombination can promote erally formed by polymorphic chromosomal rearrangements peak shifts by bringing into linkage beneficial mutations that that suppress recombination among linked loci. Suppressed arose on different chromatids. On the other hand, recom- recombination is thought to facilitate the evolution of alterna- bination can mix up alternative combinations of alleles and tive combinations of co-adapted alleles (15). Such combina- thus hamper the formation of new differentiated haplotypes tions are assumed to evolve as a result of selection favoring (29). Therefore, recombination can promote the evolution of alternative evolutionary strategies (16). new adaptive strategies, but is also a homogenizing force that The maintenance of polymorphism is a key feature of su- inhibits their maintenance in a polymorphism (23, 30). As pergenes. Yet one would expect that the best evolutionary a corollary, reduced recombination, caused by chromosomal strategy, determined by a combination of alleles (i.e. a hap- rearrangements or by tight linkage between adaptive loci, can lotype), should eventually fix in populations via selection. In allow the maintenance of alternative haplotypes, but may also nature, supergene alleles have been shown to be maintained prevent peak shift and the formation of differentiated haplo- by balancing selection, in particular by negative frequency- types. dependent selection taking the form of disassortative mate Because of this dual effect of recombination, polymorphism choice (17) or heterozygote advantage (7,8, 18). Indeed, su- is unlikely to be maintained during the process of peak shift pergene alleles are often associated with chromosomal inver- (28). Nonetheless, the evolution of supergene haplotypes sions that seem to harbour recessive deleterious mutations, as may occur in situations where rearrangements reducing re- suggested by the lack of inversions homozygotes in natural combination occur after peak shifts. Indeed, a solution to bioRxiv preprint doi: https://doi.org/10.1101/2020.11.19.389577; this version posted November 19, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. this paradox may involve the evolution of alternative super- between population is likely to lead to the formation of a su- gene haplotypes in either (i) different genomic regions or (ii) pergene, suggesting that admixture may play an important different taxa (15, 31, 32). In this later case, haplotypes be- role in the formation of new genetic architectures. In par- longing to the same population recombine normally, but not ticular, we show that the formation of a supergene strongly with haplotypes from the other population. Alternative strate- depends on the interaction between frequency-dependent ef- gies encoded by differentiated haplotypes can readily evolve fects of recombination and of overdominance. in separated populations if they experience variation in selec- tive pressure, and the same rationale applies for alternative Methods haplotypes evolving in distinct genomic regions, for instance following a duplication. By the way of genomic transloca- Purpose. We investigate the conditions under which chro- tion or migration between population (admixture), the differ- mosomal inversions spread in neighboring populations under ent haplotypes may be grouped respectively (i) in the same disruptive selection, and how it associates with the forma- genomic region or (ii) in the same population. If these haplo- tion of supergenes underlying the maintenance of discrete types are not recombining, for instance because one of them polymorphisms. We define a supergene as a genetic archi- has experienced a chromosomal inversion, and if some form tecture maintaining under balancing selection multiple non- of balancing selection maintains them in coexistence, they recombining haplotypes encoding alternative discrete pheno- may form a supergene. types. Polymorphisms at supergene is thus maintained over the long term by evolutionary forces balancing
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