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Introgressive Hybridization Between Two Iberian Endemic Cyprinid Fish

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Introgressive Hybridization Between Two Iberian Endemic Cyprinid Fish doi:10.1111/j.1420-9101.2010.01953.x Introgressive hybridization between two Iberian endemic cyprinid fish: a comparison between two independent hybrid zones M. A. ABOIM*1,J.MAVA´ REZ à1, L. BERNATCHEZà &M.M.COELHO* *Centro de Biologia Ambiental, Faculdade de Cieˆncias da Universidade de Lisboa, Campo Grande, Lisboa, Portugal Centro de Ecologı´a, Instituto Venezolano de Investigaciones Cientı´ficas, Apartado 20632, Caracas, Venezuela àIBIS (Institut de Biologie Inte´grative et des Syste`mes) Universite´ de Laval, QC, Canada Keywords: Abstract Achondrostoma oligolepis; Pseudochondrostoma duriense and Achondrostoma oligolepis are two Iberian hybridization; endemic cyprinid fish species that occur in sympatry over most of their Iberian Cyprinidae; distribution range and that are suspected to hybridize in nature. Here, we microsatellites; employed a combination of mitochondrial and microsatellite markers to mtDNA; explore the extent of introgressive hybridization between these fishes. Two Pseudochondrostoma duriense. natural hybrid zones were identified in different river basins. Introgression was bi-directional and both hybrid zones consisted mostly of parental genotypes ⁄ phenotypes (i.e. bimodal hybrid zones). Yet, they appeared to differ in the extent and direction of introgression, which supports the view that they constitute independent outcomes of different hybridization processes probably influenced by environmental features. Several discordances were found between mtDNA and microsatellite results, suggesting that this hybridization process has complex consequences and illustrating the impor- tance of using independent markers to define accurately the hybrid status of individuals in the presence of high levels of backcrossing. due to the fact that modern molecular techniques and Introduction analyses allow more powerful identification of hybrids The traditional view that hybridization is a rare phe- and introgressed species lineages (Mallet, 2005), but also nomenon in animals with little influence in speciation the realization that anthropogenically driven changes on and evolution is increasingly being challenged (Dowling the spatial distribution of species are increasing the & Secor, 1997; Barton, 2001; Mallet, 2005). Hybridiza- incidence of hybrid zones (Reusch & Wood, 2007). tion is now well known in several animal groups and has In spite of this interest, the evolutionary role of also proven to have, through introgression, a key introgressive hybridization in nature is controversial influence in several evolutionary phenomena such as (Seehausen, 2004). Research in stable hybrid zones have the origin of evolutionary novelties, adaptive radiation often revealed various kinds of hybrid unfitness, which and speciation (Dowling & Secor, 1997; Seehausen, could drive hybrids to evolutionary ‘dead ends’, whereas, 2004). It has also been one of the motivations behind in other biological frameworks, hybridization may have the recent reappraisal of the debate about species the potential to generate genetic diversity and create concepts (Hewitt, 2001; Mallet, 2005). This revived opportunities for novel adaptive radiations in natural interest in animal introgressive hybridization is partly populations (e.g. Barton, 2001). Moreover, many studies indicate that hybrids between the same complex of Correspondence: Jesu´ s Mava´rez, Centro de Ecologı´a, Instituto species may show high variation in fitness (Arnold et al., Venezolano de Investigaciones Cientı´ficas, Apartado 20632, 2001) and provide evidence for genotype–environment Caracas 1020-A, Venezuela. Tel.: +58 (0)212 5041886; fax: +58 (0)212 5041088; interactions (e.g. Campbell & Waser, 2001). Finally, in e-mail: [email protected] some cases, the outcome of hybridization has been 1These authors have contributed equally to this work. shown to vary dramatically with historical and ª 2010 THE AUTHORS. J. EVOL. BIOL. 23 (2010) 817–828 JOURNAL COMPILATION ª 2010 EUROPEAN SOCIETY FOR EVOLUTIONARY BIOLOGY 817 818 M. A. ABOIM ET AL. geographical factors (Nolte et al., 2009; Senn & Pember- Achondrostoma, Iberochondrostoma, Protochondrostoma and ton, 2009). It is therefore clear that, when possible, Parachondrostoma (Robalo et al., 2007). In particular, multiple independent hybrid zones between the same Pseudochondrostoma duriense and Achondrostoma oligolepis two species must be analysed to determine the relative are believed to have diverged around 11 million years importance of intrinsic (e.g. genetic) and extrinsic (e.g. ago (MYA) (Doadrio & Carmona, 2004) and current ecological) factors on the evolution of hybrid zones (e.g. records indicate extensive sympatry in northwestern Morgan-Richards & Wallis, 2003). Iberian basins. Pseudochondrostoma duriense is endemic of In terrestrial environments, a large number of hybrid Galiza and north of Portugal with a southern distribution zones represent contacts between divergent lineages limit in Vouga (Kottelat & Freyhof, 2007; Aboim et al., reunited after the extreme climate changes occurred 2009), whereas A. oligolepis distribution is limited to river during the Pleistocene, when glacial cycles forced range basins between Minho and Mondego and in Douro is expansions and contractions upon the fauna and flora restricted to tributaries in Portuguese territory, i.e. has an (Hewitt, 2001). This is particularly relevant in freshwater eastern delimitation near the boarder between Portugal fishes, where the literature on the distribution and and Spain (Robalo et al., 2006; Kottelat & Freyhof, 2007) evolutionary history of some groups, especially in (Fig. 1). Europe, has widely relied not only on major geographical Putative hybrids between the two species have been and climatic events (e.g. Briolay et al., 1998; Doadrio & characterized morphologically by Collares-Pereira & Carmona, 2004), but also on hybridization between Coelho (1983) in the Douro River basin. Morphological divergent lineages (Alves et al., 2001; Costedoat et al., evidence has led to the suggestion that introgression is 2006; Nolte et al., 2006). For example, cyprinids from unidirectional, from P. duriense into A. oligolepis, whereas southern European peninsulas such as Iberia are char- the absence of introgression at mtDNA markers has acterized by a high number of endemic species spread raised the interpretation that it is also sex biased (Gante throughout independent river basins, a pattern that has et al., 2004). However, the understanding of this hybrid- been explained by the colonization of a restricted ization case has been hampered by limited geographical number of lineages that underwent subsequent cladoge- coverage (i.e. only a particular hybrid zone, Ta´vora River, netic processes after the formation of the Pyrenees and Fig. 1) and trait analyses (i.e. only one type of marker, the isolation of the peninsula (Doadrio & Carmona, morphology or mtDNA), such that the results obtained 2004). However, other ecological and evolutionary pro- might be biased and incomplete (Gante et al., 2004). cesses such as hybridization seem also responsible for the Here, we analyse variation at a set of molecular patterns of genetic diversity observed in several Iberian markers (mtDNA and microsatellites) to investigate the cyprinids in the genera Chondrostoma (e.g. Elvira et al., potential for introgressive hybridization between 1990), Barbus (e.g. Almodo´ var et al., 2008) and Squalius A. oligolepis and P. duriense. In particular, we perform a (e.g. Alves et al., 2001). thorough characterization of individual hybrids to infer The genus Chondrostoma (Agassiz 1832) comprises the extend, direction and dynamics of introgression several Iberian lineages that have been recently recon- between the two species, aiming to test the hypothesis sidered as five different genera: Pseudochondrostoma, of Gante et al. (2004), which states that introgression in Fig. 1 Sampling Map. Distribution of Pseudochondrostoma duriense and Achondros- toma oligolepis in Portugal. The stippling ⁄ shading pattern represents areas of sympatry between the two species. Dots represent sampling sites and n = individuals sampled per site. ª 2010 THE AUTHORS. J. EVOL. BIOL. 23 (2010) 817–828 JOURNAL COMPILATION ª 2010 EUROPEAN SOCIETY FOR EVOLUTIONARY BIOLOGY Hybrid zones between two Iberian Cyprinidae 819 this case is unidirectional and sex biased. Besides, we also logical hybrids were not detected to generate 25 of each take advantage of the existence of two independent hybrid type. The simulated genotypes were used to carry hybrid zones, on different river basins, to compare the out admixture analyses with STRUCTURE 2.2 (Pritchard outcome of hybridization on each zone and test the et al., 2000) using K = 2 and 105 steps of the Markov hypothesis that hybrid zones can evolve differently Chain (preceded by a burn-in period of 105 steps), and ⁄ or result from independent hybridization processes assuming an admixture model and independent allelic (Landry & Aubin-Horth, 2007). frequencies (Pritchard et al., 2000). Results were evalu- ated aiming to assess the efficiency of admixture analyses Material and methods and to compute the proportion of hybrid individuals that were correctly identified as such in the simulated data set. In our case, the threshold q-values were arbitrarily Sampling and DNA extraction set up to q > 0.9 for Cluster I (P. duriense), q < 0.1 for We sampled all the river systems encompassing the Cluster II (A. oligolepis) and 0.1 < q < 0.9 for hybrids sympatric distribution range of the two species (Fig. 1). (Va¨ha¨ & Primmer,
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