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Genetic Diversity and Population Structure of Scottish Highland Red Deer (Cervus Elaphus) Populations: a Mitochondrial Survey

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Genetic Diversity and Population Structure of Scottish Highland Red Deer (Cervus Elaphus) Populations: a Mitochondrial Survey Heredity (2009) 102, 199–210 & 2009 Macmillan Publishers Limited All rights reserved 0018-067X/09 $32.00 www.nature.com/hdy ORIGINAL ARTICLE Genetic diversity and population structure of Scottish Highland red deer (Cervus elaphus) populations: a mitochondrial survey SPe´rez-Espona1,2,FJPe´rez-Barberı´a2, WP Goodall-Copestake3, CD Jiggins1,4, IJ Gordon5 and JM Pemberton1 1Institute of Evolutionary Biology, School of Biological Sciences, The University of Edinburgh, Edinburgh, UK; 2The Macaulay Institute, Craigiebuckler, Aberdeen, UK; 3British Antarctic Survey, Natural Environment Research Council, Cambridge, UK; 4Department of Zoology, The University of Cambridge, Cambridge, UK and 5Sustainable Ecosystems, CSIRO Davies Laboratory, Aitkenvale, Australia The largest population of red deer (Cervus elaphus) in Europe network and population analyses indicated significant genetic is found in Scotland. However, human impacts through hunting structure (FST ¼ 0.3452, FST ¼ 0.2478), largely concordant and introduction of foreign deer stock have disturbed the with the geographical location of the populations. Mismatch population’s genetics to an unknown extent. In this study, we distribution analysis and neutrality tests indicated a significant analysed mitochondrial control region sequences of 625 population expansion for one of the main haplogroups found in individuals to assess signatures of human and natural the study area, approximately dated c. 8200 or 16 400 years historical influence on the genetic diversity and population ago when applying a fast or slow mutation rate, respectively. structure of red deer in the Scottish Highlands. Genetic Contrary to general belief, our results strongly suggest that diversity was high with 74 haplotypes found in our study area native Scottish red deer mtDNA haplotypes have persisted in (115 Â 87 km). Phylogenetic analyses revealed that none of the Scottish Highlands and that the population retains a largely the individuals had introgressed mtDNA from foreign species natural haplotype diversity and structure in our study area. or subspecies of deer and only suggested a very few localized Heredity (2009) 102, 199–210; doi:10.1038/hdy.2008.111; red deer translocations among British localities. A haplotype published online 12 November 2008 Keywords: mitochondrial DNA; control region; red deer; introgression; population structure; human influence Introduction the Highlands, namely Atholl, Black Mount, Glenartney, Glen Fiddich, Invercauld, Mar, Abergeldie, Badenoch, The red deer (Cervus elaphus) is one of the largest Birkall, Glen Isla and Rannoch (Sinclair, 1814; Black and and most widely distributed mammal game species Black, 1861; Whitehead, 1960, 1964; Clutton-Brock and in Europe. The largest population of wild red deer in Albon, 1989). In the nineteenth century, the range and Europe occurs in the British Isles, with the majority of abundance of red deer rose again due to a growing the population found in the Scottish mainland interest in deer hunting coupled with a decrease in (Clutton-Brock and Albon, 1989). In Scotland, red deer profits from sheep rearing, which allowed large areas of have been continuously present since the end of the last land to be re-colonized by deer (Lowe and Gardiner, glaciations (c.11 000 years BP; Lister, 1984) when forests 1974; Clutton-Brock and Albon, 1989). During the nine- interspersed with open areas were abundant throughout teenth and twentieth centuries, introductions of foreign the country (Clutton-Brock and Albon, 1989). However, stock also took place to improve hunting trophy quality due to hunting and deforestation associated with the (Whitehead, 1960, 1964; Lowe and Gardiner, 1974). development of farming cultures (c. 5000 years BP), red Although introductions and translocations were aimed deer were gradually displaced northwards into the to improve trophy hunting and therefore might have mountainous Highlands (Whitehead, 1964; Lister, 1984). involved movement of males, introduction and translo- Continued deforestation and hunting during the 16th– cation of females is also well documented. Furthermore, 18th Centuries caused a steep decline in Scottish red deer because of the polygynous mating system of red deer populations with the numbers of red deer at their lowest and competition among males to hold a harem, by the second half of the 18th Century (Clutton-Brock reproductive success of introduced females is likely to and Albon, 1989). However, quite large populations of have been higher than of introduced males. Severe past red deer are thought to have survived in some areas in population declines coupled with the introductions and translocations that occurred during the nineteenth and twentieth centuries have led some to believe that the Correspondence: Dr S Pe´rez-Espona, School of Biological Sciences, Scottish red deer population contains introgressed non- University of Bristol, Woodland Road, Bristol, BS8 1US, UK. E-mail: [email protected] native genes and that population genetic structure may Received 12 June 2008; revised 9 September 2008; accepted 12 have been blurred by human intervention. More recently, September 2008; published online 12 November 2008 protection of red deer from indiscriminate culling, mtDNA population structure of Scottish Highland red deer SPe´rez-Espona et al 200 coupled with a series of mild winters and lower Scottish mainland populations, two island populations competition with sheep, has led to increased red deer (Arran and Islay) and one English population, Hmwe numbers such that populations are thought to have et al. (2006) found that overall there was a lack of doubled in the past 40–50 years (Clutton-Brock et al., congruence between geographical and genetic structure, 2004). Nowadays, red deer are distributed across the which they attributed to the impact of past red deer Highlands, islands and southwest of Scotland; the management practices on some of the populations highest densities are found in the Highlands where c. studied. However, this study included some island 400 000 individuals are thought to occupy an area populations and one small English population of red covering 300 000 km2 of the Scottish mainland (Clutton- deer for which extensive introductions have been Brock and Albon, 1989; Clutton-Brock et al., 2004). documented. The two of the mainland Scottish popula- Despite the fact that the largest numbers of European tions studied by Hmwe et al. (2006), Dunarchy and red deer are found in Scotland, studies assessing Scottish Achnacarry, for which there are no documented intro- red deer genetic diversity are few and concentrated on ductions, presented higher genetic diversity and a deer on islands or peninsulas and have highlighted the population structure concordant with geography. influence of human activities on these populations. A recent study which included 695 red deer sampled Studies on the Kintyre peninsula (Argyll) using nuclear in 14 estates of the Scottish mainland and genotyped for microsatellite and mtDNA data revealed that sika deer 21 microsatellites found high genetic diversity and introduced from Japan have successfully interbred with significant population structure in the study area, with red deer (Abernethy, 1994; Goodman et al., 1999). A isolation by distance and landscape features playing an survey of the long-term study area on the island of Rum important role in population structure (Pe´rez-Espona using mtDNA markers showed that red deer haplotype et al., 2008). diversity was low and a divergent haplotype closely In this study, mtDNA control region sequences of 625 related to Corsican red deer (Cervus elaphus corsicanus) red deer individuals sampled in the Scottish Highlands was found in some individuals, both features presum- were analysed. On account of the extensive variation ably a result of the entire population having originated revealed, we first assessed whether there was any from documented introduction events (Nussey et al., evidence for exotic haplotypes as a result of past 2006). Low mtDNA variability was also found in the introductions of females. Second, we assessed the genetic island of Arran, where the current population also diversity and population structure of mtDNA diversity originated from introduced individuals, and the island in the study area and the likely historical processes of Islay where documented introductions are known to responsible for the observed pattern. have occurred in one studied locality (Hmwe et al., 2006). Genetic diversity and population genetic structure for red deer in the mainland of Scotland has not been widely Materials and methods assessed but has shown a higher diversity and less disturbed population structure than on the islands Study area and sample collection (Hmwe et al., 2006; Pe´rez-Espona et al., 2008). In a study The study area comprised 14 open hill estates distributed comparing data from 11 microsatellites and mtDNA across a 115 Â 87 km area in the Scottish Highlands sequences obtained from 69 individuals sampled in four (Figure 1). Samples consisted of an ear tip or a sample of K SA AR FL CON CO CL BA MA AG GCR GC GK GST 0 5 10 15 20 Kilometer Figure 1 Map of the study area showing sampling sites. Dots on the map do not correspond to the total of individuals sampled but to the culling areas (several individuals were sampled in the same location). Black arrows indicate location of the Great Glen. FL ¼ Forest Lodge (n ¼ 41), CL ¼ Clunes (n ¼ 60), BA ¼ Ben Alder (n ¼ 42), AR ¼ Ardverikie (n ¼ 55), CO ¼ Corrour
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