Iberian Red Deer

Iberian red deer: paraphyletic nature at mtDNA but nuclear markers support its genetic identity Juan Carranza1, Marıa Salinas1, Damian de Andres 1,2 & Javier Perez-Gonz alez 1 1Ungulate Research Unit, Catedra de Recursos Cinegeticos y Piscıcolas (CRCP), Universidad de Cordoba, 14071 Cordoba, Spain 2Instituto de Agrobiotecnologıa, CSIC-UPNA-Gobierno de Navarra, 31192 Mutilva, Navarra, Spain Keywords Abstract Cervus elaphus hispanicus, conservation genetics, Iberian glacial refugia, paraphyletic Red deer populations in the Iberian glacial refugium were the main source for taxa, phylogeny, phylogeography. postglacial recolonization and subspecific radiation in north-western Europe. However, the phylogenetic history of Iberian red deer (Cervus elaphus Correspondence hispanicus) and its relationships with northern European populations remain Juan Carranza, Ungulate Research Unit, uncertain. Here, we study DNA sequences at the mitochondrial control region Catedra de Recursos Cinegeticos y Piscıcolas along with STR markers for over 680 specimens from all the main red deer pop- (CRCP), Universidad de Cordoba, 14071 Cordoba, Spain. ulations in Spain and other west European areas. Our results from mitochon- Tel: 34 957 212025; drial and genomic DNA show contrasting patterns, likely related to the nature E-mail: [email protected] of these types of DNA markers and their specific processes of change over time. The results, taken together, bring support to two distinct, cryptic maternal lin- Funding Information eages for Iberian red deer that predated the last glacial maximum and that have This work was partly supported by project maintained geographically well differentiated until present. Haplotype relation- CGL2010-17163/BOS from the Spanish ships show that only one of them contributed to the northern postglacial recolo- MInistry of Science and by Extremadura and nization. However, allele frequencies of nuclear markers evidenced one main Andalusian Regional Goverments. differentiation between Iberian and northern European subspecies although also Received: 20 October 2015; Revised: 7 supported the structure of both matrilines within Iberia. Thus, our findings October 2015; Accepted: 21 October 2015 reveal a paraphyletic nature for Iberian red deer but also its genetic identity and differentiation with respect to northern subspecies. Finally, we suggest that Ecology and Evolution 2016; 6(4): maintaining the singularity of Iberian red deer requires preventing not only – 905 922 restocking practices with red deer specimens belonging to other European populations but also translocations between both Iberian lineages. doi: 10.1002/ece3.1836 Introduction Various phylogeographic analyses have pointed to the Iberian Peninsula as the main refugium for postglacial During the Quaternary ice ages, most of northern Europe recolonization of north-western Europe for different was covered by ice, while permafrost extended through animal species (e.g., insects, Vila et al. 2005; amphibians, Central Europe, shaping the distribution of many temper- Martınez-Solano et al. 2006; reptiles, Paulo et al. 2008; ate species to ice-free glacial refugia during the Late Pleis- Miraldo et al. 2011; mammals, Branco et al. 2002; Vernesi tocene (Hewitt 2000). According to Sommer and Zachos et al. 2002; Centeno-Cuadros et al. 2009). Moreover, the (2009), during the last glacial maximum (LGM, 25,000– Iberian Peninsula harbors a high physiographic complex- 18,000 BP), the distribution ranges of extant species were ity that, in combination with concurrent Mediterranean more contracted than ever before in their history. Main and Atlantic influences responsible for a wide range of European glacial refugia corresponded to the southern climates, may favor the presence of subrefugia (Gomez peninsulas of Iberia, Italy, and the Balkans. These three and Lunt 2007) and opportunities for intraspecific diver- main refuges acted as sources for the postglacial recoloniza- gence (rev. Schmitt 2007). tion of the continent for different species, carrying distinct Phylogeography is normally constructed from genetic lineages as a legacy of their long isolation from each intraspecifically variable markers with phylogenetic signal other (Taberlet et al. 1998; Hewitt 1999; Torroni et al. such as DNA sequences (Lowe et al. 2004). Specifically, 2001; Schmitt 2007; Knopp and Meril€a 2009). mitochondrial DNA has proven to be an ideal sequence ª 2016 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd. 905 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. Paraphyletic Nature of Iberian Red Deer J. Carranza et al. for phylogeographic analyses due to its high rate of have confirmed that areas in north-west Europe were sequence evolution, uniparental inheritance, and lack of recolonized by red deer from the Iberian Peninsula after recombination (Avise 2000; Lowe et al. 2004). Other the last glacial maximum (Meiri et al. 2013). markers such as allozymes, RAPDs, or microsatellites pro- Since red deer populations persisted throughout the vide information about absolute differences but no infor- entire last glacial period in the Iberian Peninsula (Som- mation about genealogical relationships (e.g., Harris mer et al. 2008; Meiri et al. 2013), the identification of 1999). In particular, microsatellite markers have shown to refugial genetic clades and their current distribution may bear high rates of homoplasy (same alleles but different provide important insights into the historical processes ancestors) that might hinder the correct establishment of underlying the patterns of intraspecific variation in Ibe- phylogenetic relationships between species (Estoup et al. rian and other west European lineages. The most 2002). However, microsatellites can be useful in solving comprehensive analysis so far for Iberian red deer (C. e. particular questions that emerge in phylogeographic stud- hispanicus) phylogeography was recently performed by ies, mainly those affecting the divergence of closely related Fernandez-Garcıa et al. (2014). In that study the authors taxa over time periods shorter than those normally suggested the existence of two haplogroups related to two required to find signatures in mtDNA (Estoup et al. glacial refuges for red deer within Iberia. However, their 2002). Postglacial recolonization of northern Europe after phylogenetic differentiation remains uncertain from those the last glacial maximum (LGM) from southern refugia results (see Carranza and Martınez 2014). Additionally, may have taken place as recently as 16,000 years BP information on the degree of genetic differentiation at (Meiri et al. 2013), which is a short time to be tracked by nuclear markers between the Iberian and with other west mtDNA alone. By contrast, microsatellite markers can European lineages is lacking, which is especially important provide information for the most recent events during because such differentiation presumably took place very postglacial recolonization (e.g., Hewitt 1999; Palo et al. recently during postglacial recolonization. 2004; Knopp and Meril€a 2009; Dool et al. 2013). Further- Here, we use mtDNA and nuclear genetic markers to more, information provided by microsatellite markers is study the phylogeography of red deer. We focus on the especially important in species in which males are the dis- study of current Iberian red deer lineages in the context persing sex and females are philopatric (Petit and Excof- of West European red deer, to address the following fier 2009). This is because the existence of taxonomic objectives: distinctiveness found at mtDNA can be prevented by 1) To study the haplotype composition and phylogenetic male-driven gene flow (e.g., Nater et al. 2011). relationships between Iberian and other European The red deer (Cervus elaphus) is the most widely dis- clades. tributed species of large wild mammal in the main the 2) To infer the history of phylogenetic differentiation Palearctic (Geist 1998). It is an interesting model species between Iberian clades. whose distribution and genetic structure have been 3) To assess the genetic structure of red deer in western shaped by both natural and anthropogenic factors (Skog Europe using microsatellite markers. et al. 2009), with many recent human-mediated demo- 4) To provide basis for decisions on preserving the cur- graphic and biogeographic alterations that might blur the rent main Iberian populations from foreign restocking basal structure shaped by natural selection and biogeographic phenomena during the last ice age (Zachos and Material and Methods Hartl 2011). Paleontological findings have identified the Iberian Peninsula along with southern France, and south- Study area and sample collection eastern Europe from the Balkans up to the Carpathians, as refugial areas for the red deer during the LGM (Som- Most of current distribution of red deer in the Iberian mer et al. 2008). Studies on red deer phylogeography in Peninsula has resulted from many translocations, some of Europe based on mitochondrial DNA (Ludt et al. 2004; them documented, and others probably not, from a few Skog et al. 2009; Niedziałkowska et al. 2011) found three remaining populations (Cabrera 1914; Blanco 1998; Car- main lineages: a western lineage (A) that spread from Ibe- ranza 2010). We do not have evidence of any current red ria through the British Isles to Scandinavia, Germany, deer population in

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