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Soricidae) Patterns in Iberia Shaped by the Arrival of C

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Soricidae) Patterns in Iberia Shaped by the Arrival of C 1 Competitive exclusion in phylogeography: Crocidura suaveolens 2 (Soricidae) patterns in Iberia shaped by the arrival of C. russula 3 Running title: Competitive exclusion of C. suaveolens 4 Luis Biedma1, Jacinto Román2, Javier Calzada1, Guillermo Friis3,*and José A. Godoy3 5 1Department of Integrated Sciences, Faculty of Experimental Sciences, University of Huelva, 6 Avenida de las Fuerzas Armadas, S/N, 21007 Huelva, Spain. 7 2Department of Conservation Biology , Doñana Biological Station, CSIC, C. Americo Vespucio 8 26, 41092 Sevilla, Spain. 9 3 Department of Integrative Ecology, Doñana Biological Station, CSIC, C. Americo Vespucio 26, 10 41092 Sevilla, Spain. 11 * Current address: National Museum of Natural Sciences, Spanish National Research Council 12 (CSIC), Madrid 28006, Spain 13 e-mails: [email protected], [email protected], 14 [email protected], [email protected], [email protected]. 15 Correspondence: José A. Godoy, Department of Integrative Ecology, Doñana Biological Station, 16 CSIC, C. Americo Vespucio 26, 41092 Sevilla, Spain. E-mail: [email protected] 17 18 Abstract 19 Despite their potential importance, biological processes like competitive exclusion have been 20 mostly neglected in phylogeographic studies. Here we analyze the role of glacial events and 21 competitive exclusion in the evolutionary history of the lesser white-toothed shrew, Crocidura 22 suaveolens, in Iberia based on cytochrome b sequences. All the Iberian samples grouped 23 together with the rest of western European populations within the previously described clade 24 IV. We identified three distinct evolutionary lineages within this major clade, two of them 25 occurring exclusively in Iberia. Iberian lineage B extends throughout the northwest with a 26 continuous distribution and diversity values from moderate to high, whereas Iberian lineage C 27 has a highly-patched distribution and is structured in four sublineages, all having low diversity 28 values. No signs of demographic growth were detected for any of the lineages. The 29 evolutionary history of C. suaveolens in Iberia supports the refugia-within-refugia scenario, but 30 ecological studies in areas of sympatry, molecular and fossil datings, and contrasting patterns 31 in the Italian Peninsula, suggest that competitive exclusion exerted by C. russula since its 32 arrival to Iberia has been the main factor shaping the distribution, phylogeograhy and 33 population genetics of lineage C. 34 35 Keywords: Competitive exclusion, Crocidura suaveolens, cytochrome b, genetic diversity, 36 glacial refugia, phylogeography 37 38 39 Introduction 40 Distribution ranges and patterns of genetic structure and diversity of most European 41 temperate species have been shaped by Quaternary climatic oscillations (Hewitt, 2000; Hewitt, 42 2004; Taberlet, Fumagalli, Wust-Saucy & Cosson, 1998). During glacial periods, species 43 survived in refuge areas located mainly in the peninsulas of Iberia, Italy and the Balkans 44 (Hewitt, 1999; Taberlet et al., 1998). Glacial periods of contraction and isolation were followed 45 by interglacial periods during which recolonization of the continent occurred through 46 northward expansion from southern refugia (Hewitt, 1999; Hewitt, 2001). Repeated glacial 47 cycles have given rise to divergent phylogeographic clades typically associated to separate 48 glacial refugia (Hewitt, 2004; Hewitt, 2011), and to a progressive reduction in diversity with 49 increasing latitude (Hewitt, 1999; Hewitt, 2000). 50 Recent evidence shows that southern refugia were indeed a heterogeneous mosaic of suitable 51 habitat isolated by unsuitable habitat that allowed the evolution of separate sublineages 52 within each peninsula (refugia-within-refugia scenario; Abellán & Svenning, 2014; Gómez & 53 Lunt, 2007; Weiss & Ferrand, 2007). This scenario resulted in the high levels of intra-specific 54 diversity, but also of species diversity and endemism when divergence progressed towards 55 speciation, that are characteristic of southern refuges (Abellán & Svenning, 2014; Vega, Amori, 56 Aloise, Cellini, Loy & Searle, 2010). The description of these intraspecific lineages within 57 European refugia is key for the setting of conservation priorities and for the elaboration of 58 effective management plans. 59 With the generalized emphasis on the role of the Quaternary climatic oscillations, other factors 60 that could also promote intraspecific divergence have been overlooked. In particular, 61 competitive exclusion (CE) by ecologically similar species, or even conspecific populations, has 62 been a process almost completely neglected in phylogeography (but see Ranjard, Welch, 63 Paturel & Guindon, 2014; Waters, 2011). CE is a basic principle of ecological theory, whereby 64 two species cannot coexist in a stable habitat if they compete for the same resources (Ayala, 65 1971; Gause, 1932; Hardin, 1960). The successful competitor may drive the other towards 66 extinction or promote its evolutionary shift towards a different ecological niche. Recent 67 evidence suggests CE is a widespread phenomenon that can explain the observed phylogenetic 68 overdispersion of mammal communities (Cooper, Rodríguez & Purvis, 2008). Interspecific CE 69 can become an agent of vicariance and cause isolation, eventually resulting in genetic 70 differentiation and lineage divergence (Gutierrez, Boria & Anderson, 2014). Even intraspecific 71 CE can contribute to the maintenance of spatially-segregated divergent lineages, which 72 explains the genetic homogeneity of the recolonized northern European areas (Hewitt, 1996; 73 Ranjard et al., 2014). Furthermore, CE during range expansion can create patterns at neutral 74 loci that mimic adaptive processes and resemble post-glacial segregation of clades from 75 distinct refuge areas (Excoffier & Ray, 2008). 76 The lesser white-toothed shrew, Crocidura suaveolens (Pallas, 1811), represents a suitable case 77 study to analyze the relative roles of the Quaternary climatic oscillations and CE in the genetic 78 divergence of temperate species in Europe. C. suaveolens is widely distributed throughout the 79 Palearctic, extending from the Atlantic coasts of Europe to Siberia (Hutterer, 2005; Palomo, 80 Kryštufek, Amori & Hutterer, 2016). From Central Europe to Asia its distribution is continuous 81 and the species is described as abundant and ubiquitous (Palomo et al., 2016). However, in 82 western Europe, C. suaveolens is less common and is absent from large areas, including most 83 of the Iberian Peninsula (Libois, Ramalhinho & Fons, 1999). 84 Like many other temperate species, C. suaveolens retreated to southern Eurasian refugia 85 during Pleistocene glaciations (Hewitt, 1999; Taberlet et al., 1998). As a result of these 86 processes, ten phylogeographic clades have been identified across its wide distribution, the 87 Iberian populations grouping in clade IV, which is the most western and basal clade in Europe 88 (Dubey, Cosson, Magnanou, Vohralík, Benda, Frynta, Hutterer, Vogel & Vogel, 2007; Dubey, 89 Zaitsev, Cosson, Abdukadier & Vogel, 2006). However, these previous studies included only 90 two Iberian samples, so that any possible internal genetic structure within Iberia might have 91 remained unnoticed. In addition, the most isolated continental populations of European C. 92 suaveolens are located in southwestern Iberia, being they separated more than 300 km from 93 any other populations (Palomo et al., 2016; Román & Ruiz, 2003)(Fig. 1). A plausible hypothesis 94 is that these marginal populations were unintentionally introduced by humans, as 95 demonstrated for some Mediterranean island populations (Dubey et al., 2007); shrews are 96 small and very discrete animals and southwestern Iberia has been a place with a huge 97 commercial marine traffic for millennia (Vives, 2015). 98 An intriguing possibility is that the recent history and current distribution of C. suaveolens in 99 western Europe, and especially in Iberia, have been influenced by its congeneric the greater 100 white-toothed shrew, C. russula. C. russula managed to reach Iberia from Africa 100 kya 101 (Arsuaga, Baquedano & Pérez-González, 2006; Laplana & Sevilla, 2006; López-García, 2008; 102 Ruiz-Bustos, 1997),being currently a very widespread and common species throughout 103 western Europe (Aulagnier, Hutterer, Amori, Kryštufek, Yigit, Mitsain & Palomo, 2016). Several 104 lines of evidence suggest that C. russula competitively exclude C. suaveolens in areas of 105 sympatry (Cosson, Pascal & Bioret, 1996; Kraft, 2000; Libois et al., 1999; Niethammer, 1979; 106 Pascal, Lorvelec & Vigne, 2006; Poitevin, Catalan, Fons & Croset, 1987; Román & Ruiz, 2003). 107 CE could thus explain the fragmented distribution of C. suaveolens and, if so, it may have also 108 caused genetic isolation leading to intraspecific divergence in this area. 109 Therefore, in the present study we aimed to: (1) infer the evolutionary history of C. suaveolens 110 in the Iberian Peninsula by identifying the main mitochondrial evolutionary lineages and 111 estimating divergence times among them; (2) clarify the origin of the southwestern Iberian 112 populations of C. suaveolens and (3) discuss the phylogeographic and demographic processes 113 that have shaped the species genetic variation and its current distribution, with explicit 114 consideration of the possible contribution of competitive exclusion by C. russula. 115 116 Materials and Methods 117 Sample collection 118 Samples of 119 specimens of C. suaveolens were
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