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Spatial Genetic Structure in the Rock Hyrax (Procavia Capensis)

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Spatial Genetic Structure in the Rock Hyrax (Procavia Capensis) Canadian Journal of Zoology Spatial genetic structure in the rock hyrax (Procavia capensis) across the Namaqualand and western Fynbos areas of South Africa – a mitochondrial and microsatellite perspective Journal: Canadian Journal of Zoology Manuscript ID cjz-2019-0154.R3 Manuscript Type: Article Date Submitted by the 19-Mar-2020 Author: Complete List of Authors: Visser, Jacobus; Stellenbosch University, Department of Botany and Zoology; Cape Peninsula University of Technology, Department of ConservationDraft and Marine Sciences Robinson, Terence; Stellenbosch University, Department of Botany and Zoology Jansen van Vuuren, Bettine; University of Johannesburg, Department of Zoology Is your manuscript invited for consideration in a Special Not applicable (regular submission) Issue?: Afrotheria, Cape Flats, Knersvlakte, landscape connectivity, landscape Keyword: genetics, Procavia capensis, rock hyrax https://mc06.manuscriptcentral.com/cjz-pubs Page 1 of 61 Canadian Journal of Zoology Spatial genetic structure in the rock hyrax (Procavia capensis) across the Namaqualand and western Fynbos areas of South Africa – a mitochondrial and microsatellite perspective J.H. Visser a*†, T.J. Robinson a and B. Jansen van Vuuren b a Department of Botany and Zoology, University of Stellenbosch, Private Bag XI, Matieland 7602, South Africa b Centre for Ecological Genomics and Wildlife Conservation, Department of Zoology, University of Johannesburg, P.O. Box 524, Auckland Park 2000, South Africa * Current address: Department of DraftConservation and Marine Sciences, Cape Peninsula University of Technology, P.O. Box 652, Cape Town 8000, South Africa J.H. Visser: [email protected] T.J. Robinson: [email protected] B. Jansen van Vuuren: [email protected] †Corresponding author: J.H. Visser Address: Department of Conservation and Marine Sciences, Cape Peninsula University of Technology, P.O. Box 652, Cape Town 8000, South Africa e-mail: [email protected] Tel: +2721 903 1802 Spatial genetic structure in the rock hyrax across the Namaqualand and western Fynbos areas of South Africa – a mitochondrial and microsatellite perspective 1 https://mc06.manuscriptcentral.com/cjz-pubs Canadian Journal of Zoology Page 2 of 61 Jacobus H. Visser, Terence J. Robinson and Bettine Jansen van Vuuren Abstract The interplay between the biotic and abiotic environments is increasingly recognized as a major determinant of spatial genetic patterns. Among spatial genetic studies, saxicolous/rock- dwelling species remain underrepresented in spite of their strict dependence on landscape structure. Here we investigated patterns and processes operating at different spatial- (fine and regional scale) and time-scales (using mitochondrial and microsatellite markers) in the rock hyrax (Procavia capensis Pallas, 1766). Our focus was on the western seaboard of South Africa, and included two recognized biodiversityDraft hotspots (Cape Floristic Region and Succulent Karoo). At fine spatial scale, significant genetic structure was present between four rocky outcrops in an isolated population, likely driven by this species’ social system. At a broader spatial scale, ecological dependence on rocky habitat and population-level processes, in conjunction with landscape structure, appeared as the main drivers of genetic diversity and structure. Large areas devoid of suitable rocky habitat (e.g., the Knersvlakte, Sandveld and Cape Flats, South Africa) represent barriers to gene-flow in the species, although genetic clusters closely follow climatic/geological/phytogeographic regions, possibly indicating ecological specialisation or adaptation as contributing factors enforcing isolation. Taken together, our study highlights the need to consider both intrinsic and extrinsic factors when investigating spatial genetic structures within species. Key words: Afrotheria; Cape Flats; Knersvlakte; landscape connectivity; landscape genetics; phylogeography; Procavia capensis; rock hyrax 2 https://mc06.manuscriptcentral.com/cjz-pubs Page 3 of 61 Canadian Journal of Zoology Draft 3 https://mc06.manuscriptcentral.com/cjz-pubs Canadian Journal of Zoology Page 4 of 61 Introduction Fundamental drivers of biodiversity include the patterns of species distributions in conjunction with their genetic structures (Silvertown and Antonovics 2001). These aspects are both biotically (e..g, dispersal ability, life-history, social/mating system, ecological specificity, distribution) and abiotically (landscape structure, historical climatic- and geological changes) influenced (Avise et al. 1987; Hewitt 2001; Avise 2009; Papadopoulou and Knowles 2016). Among scientific disciplines, landscape genetics (sensu lato) offers a powerful framework to evaluate the intrinsic and extrinsic drivers of spatiotemporal genetic variation, drawing on landscape ecology, population genetics and spatial statistics to understand how landscape characteristicsDraft structure genetic variation across populations and individuals (Manel et al. 2003; Holderegger and Wagner 2006; Storfer et al. 2007). Most importantly, this approach analyzes spatial genetic data without a priori population assignment and therefore resolves patterns of micro-evolutionary processes at a finer scale compared to phylogeography or biogeography (Manel et al. 2003). Landscape genetic studies may therefore be successfully employed to evaluate species-specific ecological hypotheses, quantify the impact of landscape variables on genetic variation, identify (often cryptic) genetic breaks/barriers, secondary contact, source-sink dynamics as well as dispersal corridors. In sum, it is a powerful adjunct in conservation initiatives that seek to determine/assign conservation and management units in taxa (Manel et al. 2003; Storfer et al. 2007; Segelbacher et al. 2010; Storfer et al. 2010; Keller et al. 2015). Genetic studies are increasingly recognizing the biology/life-history and ecology of species as a major determinant of spatial genetic patterns (e.g., Papadopoulou and Knowles 2016; Zamudio et al. 2016). An ecological group which remains interesting in a landscape genetic 4 https://mc06.manuscriptcentral.com/cjz-pubs Page 5 of 61 Canadian Journal of Zoology context are taxa adapted to a saxicolous (rock-dwelling) existence. In South Africa, saxicolous species have received attention in phylogeographic investigations, especially along the western regions of the country. Among these studies, two geographic features namely the Knersvlakte (Matthee and Robinson 1996; Lamb and Bauer 2000; Matthee and Flemming 2002; Smit et al. 2007; Daniels et al. 2010; Portik et al. 2011; see Fig. 1b) and Cape Flats (Daniels et al. 2001; Wishart and Hughes 2001, 2003; Gouws et al. 2004, 2010; Swart et al. 2009; McDonald and Daniels 2012; see Fig. 1b), have been consistently identified as phylogeographic disruptors (barriers to gene-flow) in saxicolous vertebrate and invertebrate taxa respectively. These studies have, however, been based on coarse sampling methods and often suffered from small sample sizes and restricted number and variety of markers (especially hypervariable markers such as microsatellites, but see Portik et al. 2011) thus precluding landscape genetic inference.Draft Previous work suggest that landscape matrix and connectivity strongly influence genetic patterns in species restricted to saxicolous habitat given that rocky outcrops is often spatially heterogeneous (see e.g. Smit et al. 2010). The rock hyrax, Procavia capensis (Pallas 1766), which is tightly bound to this particular habitat type (especially granitic/metamorphic rock) and vegetation (Sale 1966; Hoeck 1975, 1989; Fourie 1983; Smithers 1983), would be particularly prone to its influence. The intervening areas, considered hostile due to predation and few refuge sites (Turner and Watson 1965; Fairall et al. 1986; Fairall and Hanekom 1987; Kotler et al. 1999; Druce et al. 2006), place a cost on dispersal which should, in turn, impact on rock hyrax genetic structure. Ecological preference aside, the rock hyrax exhibits several life-history attributes which should further impact genetic structure within and among populations. Rock hyrax population 5 https://mc06.manuscriptcentral.com/cjz-pubs Canadian Journal of Zoology Page 6 of 61 sizes fluctuate, sometimes leading to local extinctions (van der Horst 1941; Lensing 1979; Fairall et al. 1986; Fairall and Hanekom 1987; Hoeck 1989; Barry and Mundy 1998; Chiweshe 2007). It is conceivable that population declines result in bottlenecks and a loss of genetic diversity (Gerlach and Hoeck 2001). Conversely, in instances of population expansion, when marginal habitats are colonized (van der Horst 1941; Lensing 1979; Barocas et al. 2011) and there is exchange among previously isolated demes, increased genetic diversity may result. Moreover, the rock hyrax exhibits a polygynous social system, with social units comprised of a dominant territorial male which monopolizes several adult breeding females, and subadult and juvenile animals of both sexes (Fourie 1983; Gerlach and Hoeck 2001). Several peripheral males may be associated with colonies, but they are aggressively excluded by the dominant male (Fourie 1983). Peripheral males replace dominant males when the latter becomesDraft too old or weak to defend territories. In this social system, males disperse from their natal colonies either voluntarily (early) or through antagonistic interactions from the dominant male (later); females remain largely phylopatric (Coe 1962; Fourie and Perrin 1987; Hoeck 1982, 1989; Hoeck et al.
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