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Evolution of Population Genetic Structure of the British Roe Deer by Natural and Anthropogenic Processes (Capreolus Capreolus) Karis H

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Evolution of Population Genetic Structure of the British Roe Deer by Natural and Anthropogenic Processes (Capreolus Capreolus) Karis H Evolution of population genetic structure of the British roe deer by natural and anthropogenic processes (Capreolus capreolus) Karis H. Baker & A. Rus Hoelzel School of Biological and Biomedical Sciences, Durham University, South Road, Durham, DH1 3LE, UK Keywords Abstract Conservation genetics, deer, population bottleneck, population structure, Human influence typically impacts on natural populations of conservation translocation. interest. These interactions are varied and sometimes complex, and may be neg- ative and unintended or associated with conservation and management strategy. Correspondence Understanding the details of how these interactions influence and are A. Rus Hoelzel, School of Biological and influenced by natural evolutionary processes is essential to the development of Biomedical Sciences, Durham University, effective conservation strategies. In this study, we investigate a species in Britain South Road, Durham, DH1 3LE, UK. that has experienced both negative impact through overhunting in historical Tel: +0191-334-1325; Fax: +0191-334-2001; times and management efforts through culls and translocations. At the same E-mail: [email protected] time, there are regional populations that have been less affected by human influence. We use mtDNA and nuclear microsatellite DNA markers to investi- Funding Information gate patterns of connectivity and diversity and find multiple insular populations Supported by a Whitehead Trust studentship in Britain that probably evolved within the Holocene (when the habitat was free and the British Deer Society. of ice). We identify three concurrent processes. First, surviving indigenous populations show highly provincial patterns of philopatry, maintaining and Received: 6 September 2012; Revised: 17 October 2012; Accepted: 21 October 2012 generating population structure on a small geographic scale. Second, founder populations into habitat extirpated of native populations have expanded, but Ecology and Evolution 2013; 3(1): 89–102 remained largely insular. Third, introductions into established populations gen- erate some admixture. We discuss the implications for the evolution of diversity doi: 10.1002/ece3.430 of the integration of natural processes with anthropogenic influences on popu- lation size and distribution. Introduction naturally disperses and recolonizes formerly occupied areas. This process of natural recolonization usually Natural processes associated with vicariance, habitat occurs when degraded habitats are restored and dispersal dependence, local adaptation, and dispersal strategies corridors are available (see Hochkirch et al. 2007). Popu- (evolved to maximize fitness) promote the distribution of lations may also be restored through human intervention diversity among conspecific populations. These processes using translocations. There are various complications lead to the evolution of population structure over varying associated with this process including the loss of diversity geographic scales and eventual speciation. At the same and distortion of allele frequencies if the founder popula- time, anthropogenic activities are often superimposed, tion size used for the translocation is small (e.g., Ralls and the impact on population structure will depend on et al. 2000), and the possibility that interbreeding between how these different processes interact. Humans can cause introduced and native populations may result in reduced fragmentation, population declines, expansions (e.g., fitness if too dissimilar (e.g., Rhymer and Simberloff when non-native species are introduced), and extirpation. 1996). At the same time, translocations are often pro- For populations that have been influenced by declines, posed as a means of “genetic rescue” introducing new recovery in population size can be rapid, but there may genes into depauperate threatened or endangered popula- be a long-term impact on diversity (both through the ini- tions (e.g., Pimm et al. 2006; cf. Creel 2006). tial loss of allelic diversity and through drift over time). Introduced populations may remain relatively isolated Typically, population size recovery can occur as a species with low diversity following small reintroductions. This ª 2012 The Authors. Published by Blackwell Publishing Ltd. This is an open access article under the terms of the Creative 89 Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. Evolution of Deer Population Structure K. H. Baker & A. R. Hoelzel was found to be the case for the Alpine ibex, Capra ibex Table 1. Summary of all known successful roe deer introductions into ibex where founder populations had mostly been serially mainland Britain (after Whitehead 1964). bottlenecked (Biebach and Keller 2009), and the white- Site of introduction Date Site of origin Number released tailed deer, Odocoileus virginianus, where multiple source populations introduced into an area where the species Southern introductions had been extirpated retained founder signatures and Milton Abbas, Dorset 1800 Perth, Scotland 4 Abbotsbury, Dorset 1820 Unknown genetic structure (DeYoung et al. 2003). However, intro- Windsor Great Park, 1825 Dorset 4 duced populations that rapidly expand may retain more Berks variation and integrate with native populations more Windsor Great Park, 1850 Petworth readily (e.g., Zenger et al. 2003). This should also depend Berks on the interaction between population density, dispersal Epping Forest, Essex 1883 Dorset 6 behavior and range, and proximity to native populations Epping Forest, Essex 1884 Unknown 8 € (see Latch and Rhodes 2005). In this study, we investigate Thetford, Norfolk 1884 Wurttemberg, 12 Germany the effects of historical population declines followed by Petworth, Sussex 1800 Unknown more recent recolonization via natural and non-natural Petworth, Sussex 1890 Scotland dispersal among populations of the British roe deer Brentwood, Essex 1892 Unknown 2 (Capreolus capreolus). This set of population histories Horsham, Sussex 1931 Unknown provides an opportunity to investigate the implications of Northern introductions the interaction between natural processes associated with Maybole, Strathyclyde, 1820 Unknown population expansion and philopatry, and the influence Scotland Annandale, Dumfries, 1854 Unknown of anthropogenic impacts on population size and distri- Scotland butions. Drumlanrig, Dumfries, 1860 Unknown The only deer species indigenous to the United King- Scotland dom are the roe deer and red deer (Cervus elaphus). The Windermere, Cumbria 1913 Austria 12 first postglacial records of roe deer date back to between 10,050 and 9600 YBP from a site found at Thatcham in Berkshire (Yalden 1999). During the late medieval period, and population dynamics, as indicated above, more or British roe deer populations were severely reduced, proba- less isolation and structure may have evolved. One previ- bly as a result of overhunting and deforestation. Histori- ous study examined roe deer population genetics in the cal documents indicate that these declines were so severe United Kingdom using allozyme markers, and showed that roe deer were confined to parts of Scotland and pos- that roe deer exhibited polymorphism at only one locus, sibly some of the northern English border counties consistent with the expectation of reduced diversity. The (Whitehead 1964). In most of the midlands and southern one polymorphic locus indicated evidence of an east/west English counties, roe deer were reportedly absent by the cline in southern populations, which was described as 16th century (Ritson 1933). During the 1800s, roe deer consistent with the reintroduction records of roe deer populations began to recover and, since then, this recov- (Hewison 1995). However, the resolution of that study ery has been remarkable (see Ward 2005). Recovery in was low, given the small number of markers applied, and northern parts of the United Kingdom can generally be their relatively low diversity levels. attributed to natural expansion of remnant populations In this study, we investigate roe deer populations into formerly occupied areas following afforestation (Tay- sampled from areas in the northern and southern United lor 1948). In southern parts of the United Kingdom, all Kigndom (see Table 2) using 16 polymorphic microsatel- populations are believed to have descended from reintro- lite DNA markers together with 744 bp sequence data duction events (see Table 1 and Whitehead 1964). All from the mtDNA control region. These areas were chosen populations in the United Kingdom have now expanded as to best represent the differing population histories (as substantially in size, and numbers are currently controlled described above). We test the hypotheses that admixture in culls managed by either independent landowners or among native and introduced populations will have local collaboratively run Deer Management Groups (Phil- resulted in recovered diversity following the historical lips et al. 2010). The series of independent (from Euro- bottleneck, and minimized population structure among pean founders) and compounded bottlenecks from rapidly expanding populations over the restricted geo- translocated populations within the United Kingdom, graphic range represented by mainland Britain. These are together with the overall impact of the medieval bottle- realistic expectations, given the known histories and rate neck, could be expected to have reduced genetic diversity. of expansion. The very different reality of high levels
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