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Souissi, Ecol. Evol., 2017. In Introgressive hybridization and morphological transgression in the contact zone between two Mediterranean Solea species Ahmed Souissi, Pierre-Alexandre Gagnaire, François Bonhomme, Lilia Bahri-Sfar To cite this version: Ahmed Souissi, Pierre-Alexandre Gagnaire, François Bonhomme, Lilia Bahri-Sfar. Introgressive hy- bridization and morphological transgression in the contact zone between two Mediterranean Solea species. Ecology and Evolution, Wiley Open Access, 2017, 7 (5), pp.1394-1402. 10.1002/ece3.2533. hal-02395842 HAL Id: hal-02395842 https://hal.archives-ouvertes.fr/hal-02395842 Submitted on 5 Dec 2019 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: 18 June 2016 | Revised: 4 September 2016 | Accepted: 13 September 2016 DOI: 10.1002/ece3.2533 ORIGINAL RESEARCH Introgressive hybridization and morphological transgression in the contact zone between two Mediterranean Solea species Ahmed Souissi1,2,3 | Pierre-Alexandre Gagnaire2,3 | François Bonhomme2,3 | Lilia Bahri-Sfar1 1Université de Tunis El Manar, Faculté des Sciences de Tunis, UR 11ES08 Biologie Abstract integrative et écologie évolutive et Hybrid zones provide natural experiments where new combinations of genotypes and fonctionnelle des milieu aquatiques, 2092, Tunis, Tunisie phenotypes are produced. Studying the reshuffling of genotypes and remodeling of 2Université de Montpellier, Montpellier, phenotypes in these zones is of particular interest to document the building of repro- France ductive isolation and the possible emergence of transgressive phenotypes that can be 3CNRS – Institut des Sciences de a source of evolutionary novelties. Here, we specifically investigate the morphological l’Evolution, UMR 5554 UM-CNRS-IRD- EPHE, Station Méditerranéenne de variation patterns associated with introgressive hybridization between two species of l’Environnement Littoral, Sète, France sole, Solea senegalensis and Solea aegyptiaca. The relationship between genetic compo- Correspondence sition at nuclear loci and individual body shape variation was studied in four popula- Lilia Bahri-Sfar, Université de Tunis El Manar, tions sampled across the hybrid zone located in northern Tunisia. A strong correlation Faculté des Sciences de Tunis, UR 11ES08 Biologie integrative et écologie évolutive et between genetic and phenotypic variation was observed among all individuals but not fonctionnelle des milieu aquatiques, within populations, including the two most admixed ones. Morphological convergence 2092, Tunis, Tunisie Email: [email protected] between parental species was observed close to the contact zone. Nevertheless, the samples taken closest to the hybrid zone also displayed deviant segregation of geno- Funding information PHC Maghreb, Grant/Award Number: types and phenotypes, as well as transgressive phenotypes. In these samples, deviant XE27961 body shape variation could be partly attributed to a reduced condition index, and the distorted genetic composition was most likely due to missing allelic combinations. These results were interpreted as an indication of hybrid breakdown, which likely con- tributes to postmating reproductive isolation between the two species. KEYWORDS body shape, genetic–phenotypic correlation, introgressive hybridization, Solea aegyptiaca, Solea senegalensis, transgressive phenotypes 1 | INTRODUCTION isolation to be exchanged among species (Barton & Gale, 1993; Barton & Hewitt, 1985; Harrison, 1993; Harrison & Larson, 2014). Secondary contacts between closely related species, resulting from ei- Depending on the traits considered, introgressive hybridization ther natural processes or anthropogenic activity, often lead to the for- may lead to morphological convergence of parental populations if the mation of hybrid zones in which populations with divergent genomes underlying divergent genes behave neutrally and readily introgress have the potential to exchange genes. These zones have been shown upon secondary contact (Grant & Grant, 2002). A simple dilution of to act as semipermeable barriers to gene flow that selectively filter the parental phenotypic differences whereby hybrids display inter- introgression by preventing genomic regions involved in reproductive mediate phenotypes compared to the two parental species is often 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. 1394 | © 2016 The Authors. Ecology and Evolution www.ecolevol.org Ecology and Evolution 2017; 7: 1394–1402 published by John Wiley & Sons Ltd. SOUISSI ET AL. | 1395 observed in the populations located near the center of a hybrid zone however unclear whether this zone is stable or in the process of wid- (Mayr, 1963). Indeed, additive traits determined by quantitative traits ening, because the average hybrid index observed in 2008 (41.2%; loci (QTLs) with directional effects (with each QTL having an effect in Ouanes et al., 2011) increased by three times the value measured in one parental population but not in the other) should appear interme- the same place twenty years earlier (16.1%) by She et al. (1987). diate in hybrids compared to their parental populations (Albertson & In this study, we propose to assess morphological variation pat- Kocher, 2005; Rieseberg & Willis, 2007). Nevertheless, transgressive terns inside this zone and analyze the cosegregation of body shape hybrid phenotypes that exceed the range of parental phenotypic vari- and genetic variation. We use deviant segregation patterns at genetic ation have also been reported, in particular in the context of hybrid markers as a way to capture possible mechanisms of selection against zones (Rieseberg, Archer, & Wayne, 1999; Rieseberg, Widmer, Arntz, deleterious allelic combinations in introgressed genotypes. We also & Burke, 2003). This phenomenon, referred to as transgressive seg- use body shape variation in admixed populations to evaluate the con- regation (Bell & Travis, 2005; Rieseberg, Archer et al., 1999; Stelkens, sequence of gene flow on the condition of introgressed individuals. Schmid, Selz, & Seehausen, 2009), may be attributed on the contrary to traits encoded by QTLs with antagonistic effects in each parental 2 | MATERIALS AND METHODS population (Rieseberg, Archer et al., 1999). Alternatively, morphological differences between species can per- 2.1 | Sampling sist despite genetic introgression if they are themselves involved in re- productive isolation, or if the genes that control them are tightly linked We collected 88 adult individuals of S. senegalensis and S. aegyptiaca with genomic regions involved in reproductive isolation (Harrison & from four localities spanning as much as possible the hybrid zone Larson, 2014). In this case, a link between morphological trait varia- between the two species along the Tunisian coast: Tabarka (n = 8), tion and individual fitness is expected (Arnold & Hodges, 1995). Some Bizerte Lagoon (n = 47), Gulf of Tunis (n = 15), and Kerkennah Islands incompatible genotypic combinations may be eliminated, thereby pre- (n = 14) (Figure 1). According to the previous study of Ouanes et al. venting hybrids to reach the full range of phenotypic variation that (2011), these locations display variable amounts of genetic admixture. could be potentially generated by recombining the parental genomes. Tabarka contains S. senegalensis individuals introgressed by ca. 15% of Disentangling the role of the different mechanisms that can be in- S. aegyptiaca alleles. Conversely, on the opposite side, the Kerkennah volved in producing morphological variation in hybrids remains fairly sample contains mostly pure S. aegyptiaca individuals. These two loca- poorly studied in many taxa. Yet, it remains an important question for tions constitute our peripheral samples. For the two inner samples, the study of hybrid zones (Gay, Crochet, Bell, & Lenormand, 2008), Bizerte Lagoon is considered as the nearest to the hybrid zone center as it may help reveal the underlying architecture of reproductive iso- and contains S. senegalensis genotypes admixed with ca. 41,2% of lation (Rieseberg, Whitton, & Gardner, 1999) as well as the origin of S. aegyptiaca alleles, while Gulf of Tunis contains S. aegyptiaca individ- evolutionary novelties (Nichols et al., 2015; Parsons, Son, & Albertson, uals introgressed by ca. 17% of S. senegalensis alleles. Individuals were 2011). collected from small fishing boats and transported immediately on ice Here, as a first step toward understanding the evolutionary con- to the laboratory for morphological and genetic experiments. straints limiting gene flow across a species boundary, we explore body shape variation patterns along a natural hybrid zone transect 2.2 | Genetic analysis between two species of sole, Solea senegalensis and Solea aegyptiaca. These two taxa, which geographical distributions partially overlap in Whole genomic DNA (40 ng/μl) was extracted from fin clips using the Mediterranean, are recognized as distinct sister
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