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Genetic, Morphological and Ecological Variation Across a Sharp Hybrid Zone Between Two Alpine Butterflies Species Thibaut Capblancq, Laurence Despres, Jesus Mavarez

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Genetic, Morphological and Ecological Variation Across a Sharp Hybrid Zone Between Two Alpine Butterflies Species Thibaut Capblancq, Laurence Despres, Jesus Mavarez Genetic, morphological and ecological variation across a sharp hybrid zone between two alpine butterflies species Thibaut Capblancq, Laurence Despres, Jesus Mavarez To cite this version: Thibaut Capblancq, Laurence Despres, Jesus Mavarez. Genetic, morphological and ecological vari- ation across a sharp hybrid zone between two alpine butterflies species. Evolutionary Applications, Blackwell, 2020, 13, pp.1435 - 1450. 10.1111/eva.12925. hal-02405698 HAL Id: hal-02405698 https://hal.archives-ouvertes.fr/hal-02405698 Submitted on 28 Nov 2020 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. Received: 27 June 2019 | Revised: 2 December 2019 | Accepted: 9 December 2019 DOI: 10.1111/eva.12925 SPECIAL ISSUE ORIGINAL ARTICLE Genetic, morphological and ecological variation across a sharp hybrid zone between two alpine butterfly species Thibaut Capblancq1,2 | Laurence Després1 | Jesús Mavárez1,3 1Laboratoire d’Écologie Alpine, UMR UGA- USMB-CNRS 5553, Université Grenoble Abstract Alpes, Grenoble, France Identifying the mechanisms involved in the formation and maintenance of species 2 Department of Plant Biology, University of is a central question in evolutionary biology, and distinguishing the selective drivers Vermont, Burlington, VT, USA 3Departamento de Ciencias Biológicas of populations’ divergence from demographic processes is of particular interest to y Ambientales, Universidad Jorge Tadeo better understand the speciation process. Hybrid zones are recognized to provide Lozano, Bogotá, Colombia ideal places to investigate the genetic architecture of speciation and to identify the Correspondence mechanisms allowing diverging species to maintain their integrity in the face of gene Thibaut Capblancq, Laboratoire d’Écologie Alpine, UMR UGA-USMB-CNRS 5553, flow. Here, we studied two alpine butterfly species, Coenonympha macromma and Université Grenoble Alpes, Grenoble 38000, C. gardetta, which can be found flying together and hybridizing in narrow contact France. Email: [email protected] zones in the southern French Alps. We characterized the genomic composition of individuals, their morphology and their local habitat requirements, within and around Funding information CNRS INEE, Grant/Award Number: APEGE; a hybrid zone. Genetic diversity analysis at 794 SNPs revealed that all individuals Conseil Général de l'Isère within the hybrid zone were highly admixed, which was not the case outside the hybrid zone. Cline analysis showed that, despite ongoing hybridization, 56 out of 122 loci differentially fixed or nearly so between the two species were impermeable to introgression across the sharp hybrid zone (9 km wide). We also found concordance in cline position and width among genetic, morphological and environmental varia- tion, suggesting a coupling of different reproductive barriers. Habitat characteristics such as the presence of trees and shrubs and the start of the growing season were strongly associated with the genetic variation, and we found evidence of divergence at genetic markers associated with morphology and physiology, putatively involved in visual or environmental reproductive isolation. We discuss the various behavioural and ecological factors that might interplay to maintain current levels of divergence and gene flow between this species pair. KEYWORDS Alps, Coenonympha, genetic cline, hybrid zone, morphometrics, speciation 1 | INTRODUCTION by a balance between divergent selection, promoting species differ- entiation, and gene flow, acting as a homogenizing force between Hybrid zones are geographic regions where genetically divergent taxa genetic pools (Barton, 2001; Barton & Hewitt, 1985; Endler, 1977; meet and hybridize (Barton & Hewitt, 1985). They are maintained Haldane, 1948; Jiggins & Mallet, 2000). In such zones, genes can This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. © 2020 The Authors. Evolutionary Applications published by John Wiley & Sons Ltd Evolutionary Applications. 2020;13:1435–1450. wileyonlinelibrary.com/journal/eva | 1435 1436 | CAPBLANCQ ET al. potentially be exchanged between populations through segregation gardetta (Prunner 1798) and the Darwin Heath C. macromma (Turati and recombination in hybrids, at rates that, depending on the inten- & Verity 1910). Coenonympha gardetta is a typical alpine species, sity of selection, can go from virtually zero for the genomic regions largely distributed at elevations above 1,500 m along the Alps, the highly involved in species isolation and differentiation, to almost French Massif Central and the Balkans, whereas C. macromma is re- free circulation for the “neutral” or not divergently selected parts stricted to the south part of the French Alps, where it replaces C. of the genome (Barton, 1979; Harrison, 1986, 1993; Payseur, 2010; gardetta. The two species are found flying together in narrow zones Rieseberg, Whitton, & Gardner, 1999). Hybrid zones thus provide where their distribution ranges abut. Hybrids are relatively common natural segregation experiments that allow both the study of factors in these contact zones, which highlights incomplete reproductive that shape gene flow between divergent lineages and the identifi- isolation between species, even if they remain highly differentiated cation of genetic loci and traits that contribute to species isolation genetically at a large geographic scale (Capblancq, Mavárez, Rioux, (Payseur, 2010). The analysis of hybrid zones has therefore played & Després, 2019). Identifying the mechanisms involved in repro- an important role in the understanding of the genomic regions under ductive isolation between these species would provide a better selection and/or responsible for isolation in species that are difficult understanding of the speciation process for C. macromma, which to breed in the laboratory (e.g. insects with a diapause) or long-lived has been suggested to be the product of homoploid hybridization organisms (e.g. trees) (Derryberry, Derryberry, Maley, & Brumfield, between C. gardetta and a third species, the Pearly Heath C. arca- 2014; Lindtke et al., 2012). nia (Linné 1761). Indeed, in a previous study (Capblancq, Després, The estimation of cline width and slope for a genetic locus along Rioux, & Mavárez, 2015), we showed that C. macromma is composed the hybrid zone provides important information about its introgres- of a genetic mixture between C. gardetta and C. arcania (30% and sion rate. When performed over many loci distributed throughout 70%, respectively) and that it exhibits intermediate wing morphol- the genome, this analysis not only gives genome-wide introgression ogy and ecological preferences (climatic niche). Statistical modelling rates, but also allows for the identification of genomic regions ex- of different past evolutionary scenarios allowed us to confirm the hibiting significantly higher-than-average or lower-than-average hybrid origin of C. macromma and estimate its emergence at around introgression between species (Abbott et al., 2013; De La Torre, 12,000–20,000 years ago. Investigating the patterns of species di- Ingvarsson, & Aitken, 2015; Gay, Crochet, Bell, & Lenormand, 2008). vergence and its drivers in this clade would further provide more The study of such patterns of heterogeneity in genetic exchange general insights into the process of homoploid hybrid speciation along the genome can help identify barrier loci, and when analysed (Mavárez & Linares, 2008; Schumer, Rosenthal, & Andolfatto, 2014). together with morphological and behavioural traits, or with environ- We used genomic, morphological and environmental data to in- mental variables, may shed light on the forces underlying species vestigate the fine-scale divergence between C. gardetta and C. mac- isolation and differentiation (Lexer, Buerkle, Joseph, Heinze, & Fay, romma. After identifying an active and narrow hybrid zone between 2007; Lindtke et al., 2012). Nonetheless, untangling the drivers of these two species, we performed a geographic cline analysis to char- species differentiation and their genomic consequences can be dif- acterize the genetic architecture of the hybrid zone and to investi- ficult. The main reason is that hybrid zones tend to be positioned gate the genomic heterogeneity of introgression between the two in areas of low population density and/or environmental ecotones species. We also looked for patterns of morphological and ecological (Endler, 1977; Leaché, Grummer, Harris, & Breckheimer, 2017; Taylor divergence between species. Our goal was to evaluate the degree of et al., 2014; Wielstra et al., 2017), even when environmental factors concordance between ecological, morphological and genetic clines are not the main drivers of species isolation (Bierne, Welch, Loire, in the hybrid zone and to identify loci and traits potentially involved Bonhomme, & David, 2011). Besides, a hybrid zone associated with in species divergence and isolation. intrinsic
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