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Conservation Genetics of the Leopard Tortoise Stigmochelys Pardalis in Southern Africa Urban Dajčman1,2, Margaretha D

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Conservation Genetics of the Leopard Tortoise Stigmochelys Pardalis in Southern Africa Urban Dajčman1,2, Margaretha D SALAMANDRA 57(1): 139–145 Conservation genetics of Stigmochelys pardalis in southern Africa SALAMANDRA 15 February 2021 ISSN 0036–3375 German Journal of Herpetology Tortoise forensics: conservation genetics of the leopard tortoise Stigmochelys pardalis in southern Africa Urban Dajčman1,2, Margaretha D. Hofmeyr3, Paula Ribeiro Anunciação2, Flora Ihlow2 & Melita Vamberger2 1) University Ljubljana, Biotechnical Faculty, Department of Biology, Jamnikarjeva 101, 1000 Ljubljana, Slovenia 2) Museum of Zoology, Senckenberg Dresden, A. B. Meyer Building, 01109 Dresden, Germany 3) Chelonian Biodiversity and Conservation, Department of Biodiversity and Conservation Biology, University of the Western Cape, Bellville 7535, South Africa Corresponding author: Melita Vamberger, e-mail: [email protected] Manuscript received: 22 June 2020 Accepted: 17 October 2020 by Edgar Lehr Abstract. Sub-Saharan Africa harbours an outstanding diversity of tortoises of which the leopard tortoise Stigmochelys pardalis is the most widespread. Across its’ range the species is impacted by habitat transformation, over-collection for hu- man consumption and the pet trade, road mortality, and electrocution by electric fences. Most leopard tortoises in south- ern Africa are nowadays restricted to reserves and private farms. So far confiscated tortoises are frequently released into a nearby reserve without knowledge on their area of origin. This is problematic, as it has been demonstrated that the leopard tortoise harbours five distinct mitochondrial lineages, of which three occur in the southern portion of the species’ distri- butional range (South Africa, Namibia, and Botswana). Using 14 microsatellite loci corresponding to 270 samples collect- ed throughout southern Africa, we found a clear substructuring in the north constituting four clusters (western, central, north-eastern, and eastern). Genetic diversity was particularly high in the north-east and decreased towards the south. In addition, we found a significant size difference between the studied populations. Our basic morphological analysis showed that tortoises from the southern cluster tend to grow bigger than tortoises from the north. We established a comprehensive genetic database for South Africa and Namibia that can serve as a conservation management tool for the assignment and potential release of translocated or seized leopard tortoises based on genetic affiliation. Key words. Conservation management, management units, microsatellites, Namibia, pet trade, sub-Saharan Africa, South Africa, Testudinidae. Introduction already disappeared from few areas in eastern and west- ern South Africa (Hofmeyr & Baard 2014). Natural bush Tortoises and turtles are among the most imperilled bio- fires and deliberate fires set to promote regrowth and in- ta on the planet, with approximately 60.4% of 356 species crease forage quality for livestock account for a major pro- threatened or recently extinct (Lovich et al. 2018, Turtle portion of injuries and mortalities (Kabugumila 2001), Conservation Coalition 2018). Of 121 tortoises that ex- while severe droughts and road mortality also contribute isted since the Pleistocene, 69 (57%) already disappeared to population decline (Boycott & Bourquin 2000). To- (Lovich et al. 2018). The impacts that are responsible for day the vast majority of tortoises, including S. pardalis, are this alarming situation include habitat destruction, cli- found on privately owned fenced farm land and reserves. mate change, unsustainable overexploitation for human Unfortunately, their large body size and highly domed car- consumption as well as for the international pet trade, and apace make leopard tortoises susceptible to being killed by the introduction of pathogens (Wimberger et al. 2011, electric fences (Burger & Branch 1994, Arnot & Molteno Lovich et al. 2018). These also apply to the leopard tortoise 2017, Macray 2017). Stigmochelys pardalis (Bell, 1828) (Evans 1988). Between Recent molecular genetic analyses revealed the species to 1987 and 1991, S. pardalis accounted for 76% of tortoises constitute five distinct mitochondrial lineages Spitzweg( et exported from Africa for the international pet trade and al. 2019). One is distributed in the south, a second in the declines in some areas have been attributed to unsustain- north-west, and a third in the north-east of southern Africa, able collection and trade (Branch 2012). Over the last five while two additional lineages are distributed further north years 171,444 living S. pardalis, have been exported from (Spitzweg et al. 2019). Using micro satellites Spitzweg et al. Africa for commercial purposes (CITES trade database (2019) revealed the southern mitochondrial clade to match 2020). As a consequence, the once widespread species is with a well-defined southern nuclear cluster, whilst the now considered threatened in some regions, while it has north-western and north-eastern clades of southern Africa © 2021 Deutsche Gesellschaft für Herpetologie und Terrarienkunde e.V. (DGHT), Mannheim, Germany Open access at http://www.salamandra-journal.com 139 Urban Dajčman et al. corresponded to another nuclear cluster with three subclus- STRUCTURE searches for partitions which are, as far as ters. Besides the genetic diversity, the leopard tortoise ex- possible, in Hardy-Weinberg equilibrium and linkage equi- presses considerable geographic variation in body size, shell librium. Unsupervised analyses were selected because this shape, and colouration. Love ridge and Williams (1957) approach clusters samples strictly according to their genetic attributed these differences to subspecies variation. How- information, without making presumptions about popula- ever, the distribution of the mitochondrial lineages or the tion structuring (e.g. geographic distances, sampling sites). respective nuclear clusters does not match with the recog- All calculations were performed for K = 1–10, and the most nized subspecies (Fritz et al. 2010, Spitzweg et al. 2019). likely number of clusters (K) was determined using the ΔK These findings demonstrate the importance of the applica- method (Evanno et al. 2005) as implemented in the soft- tion of conservation genetic techniques to preserve the ge- ware STRUCTURE HARVESTER (Earl & von Holdt netic diversity of the species. While previous studies suf- 2012) and mean Ln probabilities. Calculations were repeat- fered from incomplete sampling in some areas (Spitzweg et ed 10 times for each K using a MCMC chain of 750,000 al. 2019) our present study adds crucial data from northern generations and a burn-in of 250,000 generations. Popu- South Africa completing these sampling gaps. lation structuring and individual admixture were visual- We examined the population structure and reveal ge- ized using DISTRUCT 1.1 (Rosenberg 2004). Individuals netic differentiation of S. pardalis using fine scale analyses with a membership proportion below 80% were considered of nuclear microsatellite markers. We deliver an essential to have admixed ancestries (Barilani et al. 2007, Randi database for future conservation relocation practices that 2008). STRUCTURE is prone to bias from uneven sample will improve the conservation management and preserva- sizes (Puechmaille 2016) and typically detects only the tion of the genetic diversity of S. pardalis. uppermost hierarchical level of population differentiation (Evanno et al. 2005). Therefore, the analysis was repeated for subsamples corresponding to previously identified clus- Material and methods ters but excluding admixed individuals (Supplementary Sampling, selection of microsatellite loci, document S1). In addition, STRUCTURE was repeated for and general data evaluation strategy each of the respective subclusters of the northern cluster. Further, Principal Component Analyses (PCAs) were In total, 270 leopard tortoises from all across South Africa, performed to examine population structuring using mi- adjacent Namibia, and southern Mozambique were studied crosatellite data and the package ADEGENET (Jombart (Supplementary document S1). These include 204 speci- 2008) for Cran R 3.2.3 (R Development Core Team 2015). mens previously sampled (Spitzweg et al. 2019). For genet- PCAs are less sensitive to sample size and are independ- ic analyses, a small amount of blood or tissue was collected ent from population genetic assumptions (Puechmaille from live tortoises in accordance with methods approved 2016). Two distinct PCAs were executed. In the first anal- by the Ethics Committee of the University of the Western ysis, all 270 individuals were included, and symbols were Cape (Ethics Reference Number (AR 19/4/1). All speci- coloured after STRUCTURE clusters (north, south, ad- mens were subsequently released at their respective col- mixed). The second PCA included only the tortoises from lection site. Blood samples were preserved on FTA classic the northern STRUCTURE cluster (151 individuals), with cards (Whatman, GE Healthcare, Munich, Germany) and symbol colours corresponding to STRUCTURE subclus- stored at room temperature. For most tortoises sampled in ters (N1, N2, N3, N4, Admixed). South Africa, the carapace length (CL) was measured to the nearest 1 mm using a measuring tape. Fieldwork and sampling in South Africa was permitted by the Limpopo Diversity within and divergence Provincial Government (ZA/LP/91608), the Department of between population clusters Environmental Affairs, Biodiversity Northern Cape Prov- ince (245/2015), Ezemvelo KZN Wildlife (OP 139/2017), and Diversity
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