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This Article Appeared in a Journal Published by Elsevier. the Attached This article appeared in a journal published by Elsevier. The attached copy is furnished to the author for internal non-commercial research and education use, including for instruction at the authors institution and sharing with colleagues. Other uses, including reproduction and distribution, or selling or licensing copies, or posting to personal, institutional or third party websites are prohibited. In most cases authors are permitted to post their version of the article (e.g. in Word or Tex form) to their personal website or institutional repository. Authors requiring further information regarding Elsevier’s archiving and manuscript policies are encouraged to visit: http://www.elsevier.com/copyright Author's personal copy Molecular Phylogenetics and Evolution 54 (2010) 427–436 Contents lists available at ScienceDirect Molecular Phylogenetics and Evolution journal homepage: www.elsevier.com/locate/ympev Temporal speciation pattern in the western Mediterranean genus Tudorella P. Fischer, 1885 (Gastropoda, Pomatiidae) supports the Tyrrhenian vicariance hypothesis Markus Pfenninger a,*, Errol Véla b, Ruth Jesse c, Miren Arantzazu Elejalde d, Fabio Liberto b, Frédéric Magnin b, Alberto Martínez-Ortí e a LabCentre, Research Centre Biodiversity & Climate, Siesmayerstrasse 70, 60323 Frankfurt, Germany b Institut Méditerranéen d’Ecologie et de Paléoécologie, Université Paul Cézanne, Europôle méditerranéen de L’Arbois, Domaine du Petit Arbois, bat. Villemin. BP 80, 13545 Aix-en-Provence, cedex 04, France c Institute of Ecology, Evolution and Diversity, Goethe University, Siesmayerstrasse 70 (Building A), 60054 Frankfurt, Germany d Departamento de Zoología y Biología Celular Animal, Facultad de Farmacia, Universidad del País Vasco, Paseo de la Universidad 7, 01006 Vitoria, Spain e Departamento de Zoología, Facultad de Ciencias Biológicas, Universitat de València & Museu Valencià d’Història Natural, Passeig de la Petxina 15, E-46008 Valencia, Spain article info abstract Article history: The land snail genus Tudorella shows a peculiar disjunct distribution around the western Mediterranean Received 25 April 2009 coasts. Despite high phenotypic plasticity, only two species with a disputed number of subspecific taxa Revised 14 September 2009 are currently recognised. We delimited the species with mitochondrial (COI & 16S) and nuclear (ITS-1) Accepted 16 September 2009 markers based on the unified species concept and suggested that there are eight species in the genus, Available online 20 September 2009 two of them currently undescribed. Applying Bayesian phylogenetic model selection, we tested four dif- ferent biogeographic hypotheses that could be causal for the current distribution pattern of extant Tudo- Keywords: rella species. A scenario involving vicariance events resulting from the repeated splits of the Tyrrhenian Western Mediterranean palaeogeography plate with subsequent dispersal events over land bridges during the Pliocene received greatest support in Species delimitation Tyrrhenian vicariance hypothesis the data. Ó 2009 Elsevier Inc. All rights reserved. 1. Introduction The land snail genus Tudorella P. Fischer, 1885 has a distribution that raises the question whether dispersal or vicariance were the It is a major challenge of biodiversity research to understand prevailing processes, as the genus range comprises areas currently the processes responsible for the current distribution of species. separated by the Mediterranean Sea. It is thus an example for the Particularly taxon ranges of organisms with low dispersal capaci- debated biogeographical dilemma that Northern Africa is faunisti- ties, but disjunct distributions, like terrestrial or freshwater organ- cally and botanically more related to southern–western Europe isms separated by the sea, require dispersal hypotheses that are than to the rest of Africa, to which it is geographical connected compatible with the taxon’s biology (Jesse et al., 2009). In these (Jeannel, 1952). The genus occurs along the western Mediterranean cases the processes of vicariance and dispersal as dominant forces coasts from the Iberian peninsula to Malta in Southern Europe and underlying biogeographical patterns are often controversially dis- from Morocco to Libya in Northern Africa (Sacchi, 1958; Giusti and cussed (Austin et al., 2003; Givnish et al., 2004; Yoder and Nowak, Manganelli, 1984) This disjunct distribution, accompanied by a 2006). Dispersal theory’s main principle is that of ‘‘centres of ori- high level of phenotypic variation and sexual dimorphism (Martí- gin”, from which taxa spread, became isolated and speciated nez-Ortí and Robles, 2005), has long since encouraged authors to (Dobzhansky, 1937; Mayr, 1954). In contrast, the central assump- describe new taxa, mostly on the subspecific level, within the tion of vicariance theory is that ancestral taxa were widespread genus (Potiez and Michaud, 1838; Sowerby, 1847; Pallary, 1898). and speciation was caused by subdivision of the ancestral range Apart from Tudorella ferruginea, all populations are therefore gen- (Yoder and Nowak, 2006; Sparks and Smith, 2005). erally attributed to Tudorella sulcata (Draparnaud, 1805) with the number of subspecific entities varying in dependence of the author from one (Giusti et al., 1995) to five (Sacchi, 1958). Tudorella has a * Corresponding author. quite covert life style. The snails are most of the time deeply bor- E-mail addresses: [email protected] (M. Pfenninger), errol.vela@- rowed in soil and debris under calcareous rocks. They are active free.fr (E. Véla), [email protected] (R. Jesse), mirenarantzazu.elejalde@e- only under suitable (i.e. moist) weather conditions. These behav- hu.es (M.A. Elejalde), [email protected] (F. Liberto), frederic.magnin@univ- cezanne.fr (F. Magnin), [email protected] (A. Martínez-Ortí). ioural characteristics render the rather large snails to unlikely can- 1055-7903/$ - see front matter Ó 2009 Elsevier Inc. All rights reserved. doi:10.1016/j.ympev.2009.09.024 Author's personal copy 428 M. Pfenninger et al. / Molecular Phylogenetics and Evolution 54 (2010) 427–436 didates for the suggested long range over-sea passive dispersal stituted opportunities to link several but not all current distribu- processes of snails (wind, bird migration, rafting on logs), apart tion areas. Lastly, as mentioned above, a relatively recent from anthropogenic dispersal. anthropogenic introduction from a single source area is also a pos- The origins of the genus Tudorella can be traced in the fossil re- sible scenario. cord to the beginning of the Miocene (Véla et al., 2008). Unfortu- Our goals for the present study were thus twofold: First, we nately, it is not possible to attribute these fossilised shells to aimed to delimit comprehensively the western Mediterranean taxa extant lineages, which precludes a fossil calibration of a molecular of the genus Tudorella, applying the unified species concept of De clock. This time frame includes several potential, mutually not Queiroz (2007). We have chosen this species concept, because it exclusive distribution scenarios that do not require transoceanic comprises the biological species concept without the need to prove dispersal. These start with the substantial tectonic processes, actual reproductive isolation. In short, the unified species concept including the split, dislocation and connection of continental mi- equates species with separately evolving metapopulation lineages, cro-plates, shaping the western Mediterranean Basin between which is appropriate in a case of allopatric relations. Second, we the Strait of Gibraltar and Malta in the last 30 my (Gueguen evaluated the relative support of several hypotheses on the tempo- et al., 1998; Rosenbaum et al., 2002a). Though debated in detail, ral and thus biogeographical splitting pattern of the identified evo- the scenario that during the Oligocene terranes now found in Cala- lutionary lineages, using a Bayesian phylogenetic model selection bria, Sicily, Corsica, Sardinia, Kabylies (Algeria), Balearic Islands approach. and Rif range in Morocco were part of the Tyrrhenian plate situated on the Southern European and Iberian margin is now widely ac- 2. Materials and methods cepted. From the late Oligocene on (30 million years ago) this plate split from mainland Europe. By 22 million years ago latest, 2.1. Sampling the component parts of the plate were already separated from each other, except for the Betis/Rif region that stuck together until The present study covered all putative taxonomical entities and 12 million years ago. About 10 million years ago, the joining of all described occurrences of the genus Tudorella in the western the Rif region with Northern Africa brought them into secondary Mediterranean region (Fig. 1). Forty-two sequences were made contact with the Kabylies region, having attached to this continent specifically for this study. Data on Algerian, French, Iberian, Moroc- some 5 millions years earlier. All other terranes reached their cur- can and Maltese localities were integrated from previous studies rent positions approximately in the late Pliocene (Rosenbaum (Martínez-Ortí et al., 2008; Véla et al., 2008). For each sampled et al., 2002a). Intriguingly, these terranes coincide largely with population, several individuals were preserved in 70–90% alcohol the current distribution of the genus Tudorella. Another major and with few exceptions, two to five specimen per locality were event, connecting most of the current distribution by land bridges
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