Comparative phylogeography of two African carnivorans presumably introduced into Europe: disentangling natural versus human-mediated dispersal across the Strait of Gibraltar

Aim Natural processes of colonization and human-mediated introductions have shaped current patterns of biodiversity in the Mediterranean Basin. We use a comparative phylogeographic approach to investigate the genetic structure of Herpestes ichneumon and Genetta genetta (Carnivora) across the Strait of Gibraltar, and test for their supposedly contemporaneous introduction into Iberia. Location Mediterranean Basin and Africa. Methods We sequenced two mitochondrial fragments (cytochrome b and control region) of 91 (H. ichneumon) and 185 (G. genetta) individuals, including the sole archaeological record of G. genetta in Iberia, dating from the Muslim occupation. We used phylogenetic and tokogenetic methods, summary statistics, neutrality tests, geographic–genetic pairwise comparisons and coalescent estimates to explore the history of the two species in the Mediterranean Basin. Results In North Africa, an autochthonous (Clade I) and a western African mtDNA clade, coalescing in the Middle to Late Pleistocene, co-occurred in both species. Only Clade I was present in Europe. In H. ichneumon, the European pool showed deep coalescence (median = 335 kyr) and high genetic differentiation and diversity compared with its North African counterpart, suggesting long-term stability of female effective population size. In sharp contrast, G. genetta in Europe exhibited lower genetic diversity, weak differentiation with North Africa and recent demographic expansion; however, Andalusia and Catalonia (Spain) showed distinctly higher genetic diversity, and the archaeological specimen had the predominant European haplotype. Main conclusions The co-occurrence of autochthonous and sub-Saharan lineages in North Africa (1) supports a new, emerging biogeographic scenario in North Africa, and (2) suggests a connection through the Sahara, possibly from the Middle Pleistocene onwards. Our results refute the idea that H. ichneumon was introduced into Europe contemporaneously with G. genetta. Instead, they support a scenario of sweepstake dispersal during Late Pleistocene sea-level fluctuations, followed by long-term in situ evolution throughout the last glaciation cycles. Genetta genetta appears to have undergone a recent spread from at least two independent introduction ‘hotspots’ in Catalonia and Andalusia, possibly following antique trade routes and/or Muslim invasions. Despite their contrasting histories, the European gene pools of both species represent unusual cases leading to the preservation of autochthonous, North African lineages.

We thank Jacques Cuisin (Muséum National d’Histoire Naturelle, Paris, France), Cédric Crémière (Muséum d’Histoire Naturelle du Havre, France), Josefina Barreiro and Luis Castelo (Museo Nacional de Ciencias Naturales, Madrid, Spain), Frieder Mayer (Museum für Naturkunde der Humboldt-Universität, Berlin, Germany), and Claudio Torres and Santiago Macías (Campo Arqueológico de Mértola, Portugal), who authorized the work on collection specimens. We thank the late Marina Alcobendas (Museo Nacional de Ciencias Naturales, Madrid, Spain), Ana Piriz and Laura Sauriano (Estación Biológica de Donãna, Sevilla, Spain), and Annie Tillier, Céline Bonillo and Josie Lambourdière (Muséum National d’Histoire Naturelle, Paris, France) for laboratory assistance. P.G. is grateful to Stéphane Peigné, Lars Werdelin and Cécile Callou for sharing their databases, and to Julien Lorion and Fabien Leprieur for analytical guidance. Charlène Letenneur kindly helped in the figure design. Warren Johnson significantly improved an earlier version of the manuscript. P.G. received support from the SYNTHESYS Project http:// www.synthesys.info/ (ES-TAF-2107), financed by the European Community Research Infrastructure Action under the FP6 ‘Structuring the European Research Area’ program. This work was supported by the ‘Consortium National de Recherche en Génomique’, and the ‘Service de Systématique Moléculaire’ of the Muséum National d’Histoire Naturelle (USM 2700). It is part of agreement 2005/67 between Genoscope and the Muséum National d’Histoire Naturelle on the project ‘Macrophylogeny of life’ directed by Guillaume Lecointre. The publication cost of Fig. 4 was supported by the project ‘ANR-09-PEXT-004: MOHMIE – Influence de l’installation des hommes modernes au Maroc sur l’évolution de la biodiversité des petits vertébrés terrestres’, led by Christiane Denys.

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