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Climatic and Topographic Changes Since the Miocene Influenced the Diversification and Biogeography of the Tent Tortoise (

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Climatic and Topographic Changes Since the Miocene Influenced the Diversification and Biogeography of the Tent Tortoise ( Zhao et al. BMC Evol Biol (2020) 20:153 https://doi.org/10.1186/s12862-020-01717-1 RESEARCH ARTICLE Open Access Climatic and topographic changes since the Miocene infuenced the diversifcation and biogeography of the tent tortoise (Psammobates tentorius) species complex in Southern Africa Zhongning Zhao1* , Neil Heideman1, Phillip Bester2, Adriaan Jordaan1 and Margaretha D. Hofmeyr3 Abstract Background: Climatic and topographic changes function as key drivers in shaping genetic structure and cladogenic radiation in many organisms. Southern Africa has an exceptionally diverse tortoise fauna, harbouring one-third of the world’s tortoise genera. The distribution of Psammobates tentorius (Kuhl, 1820) covers two of the 25 biodiversity hotspots in the world, the Succulent Karoo and Cape Floristic Region. The highly diverged P. tentorius represents an excellent model species for exploring biogeographic and radiation patterns of reptiles in Southern Africa. Results: We investigated genetic structure and radiation patterns against temporal and spatial dimensions since the Miocene in the Psammobates tentorius species complex, using multiple types of DNA markers and niche modelling analyses. Cladogenesis in P. tentorius started in the late Miocene (11.63–5.33 Ma) when populations dispersed from north to south to form two geographically isolated groups. The northern group diverged into a clade north of the Orange River (OR), followed by the splitting of the group south of the OR into a western and an interior clade. The latter divergence corresponded to the intensifcation of the cold Benguela current, which caused western aridifcation and rainfall seasonality. In the south, tectonic uplift and subsequent exhumation, together with climatic fuctuations seemed responsible for radiations among the four southern clades since the late Miocene. We found that each clade occurred in a habitat shaped by diferent climatic parameters, and that the niches difered substantially among the clades of the northern group but were similar among clades of the southern group. Conclusion: Climatic shifts, and biome and geographic changes were possibly the three major driving forces shap- ing cladogenesis and genetic structure in Southern African tortoise species. Our results revealed that the cladogenesis of the P. tentorius species complex was probably shaped by environmental cooling, biome shifts and topographic uplift in Southern Africa since the late Miocene. The Last Glacial Maximum (LGM) may have impacted the distribution of P. tentorius substantially. We found the taxonomic diversify of the P. tentorius species complex to be highest in the Greater Cape Floristic Region. All seven clades discovered warrant conservation attention, particularly Ptt-B–Ptr, Ptt-A and Pv-A. *Correspondence: [email protected] 1 Department of Zoology and Entomology, University of the Free State, Biology Building B19, 205 Nelson Mandela Dr, Park West, Bloemfontein, South Africa Full list of author information is available at the end of the article © The Author(s) 2020. Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creat iveco mmons .org/licen ses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creat iveco mmons .org/publi cdoma in/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Zhao et al. BMC Evol Biol (2020) 20:153 Page 2 of 33 Keywords: Cladogenesis, Evolutionary driver, Miocene cooling, Refugia retracting, Biogeography, Hidden diversity Background Floral development in Southern Africa has been stud- Climate fuctuations have often been invoked to explain ied extensively, with strong evidence that late Neogene foral and faunal diversifcation on a global [1–3] as well climatic and geomorphic evolution (due to tectonic as a regional scale, e.g., in Southern Africa [4, 5]. Global events) shaped the development of most current cooling after the early Eocene Climatic Optimum led biomes [20, 21]. Reptile diversity is comparatively high to the formation of the Antarctic ice-sheet by the early in Southern Africa [22–24] and genetic diversifca- Oligocene, where after temperatures increased and tion in several taxa has been linked to climatic change, remained high from the late Oligocene to the mid-Mio- particularly during the Pliocene–Pleistocene period, cene Climatic Optimum, 17–15 Ma [6]. Subsequently, although some cladogenic events date back to the Mio- decreasing temperatures re-established the Antarctic cene [5]. In addition, landscape features have been pos- ice-sheet by 10 Ma and established the Arctic ice-sheet tulated as having demarcated phylogeographic clades in by 3.2 Ma [6]. Apart from global cooling, Southern some reptile taxa [25–27]. Africa became progressively more arid since the Oligo- Te shifting in climate and topographical features cene [7], and the development of the Benguela Current due to historical climate and geographical events plays 14–10 Ma [8, 9] increased western aridity and estab- important roles in driving diversifcation and changing lished seasonal rainfall patterns over Southern Africa of genetic structure of organisms [28]. Te Pleistocene by the late Miocene [4, 8]. climatic oscillations (2.58–0.01 Ma) in the Quaternary Besides climate, landscape evolution also contributed Epoch [29] proved to be the fundamental driver that to genetic diversifcation of Southern Africa’s fauna and shaped distribution patterns and cladogenesis in many fora [5], with the Cape Fold Mountains (CFMs), Great organismal groups [28, 30, 31], and therefore facilitated Escarpment (GE), and Orange River (OR) identifed as their genetic divergence and speciation [32–34]. During potential geographic barriers to gene exchange in some the cold phase, glaciations resulted in migrations and taxa [10–12]. Te CFMs were already formed before shrinking of populations into diferent subpopulations, rifting of Gondwanaland in the lower Cretaceous [13], thus functioning as major drivers subdividing popula- but diferential uplift and exhumation in the last 30 tions. During warm periods, the glaciers retracted, million years [14] may have contributed to the current leading to recolonization, dispersal, and population relief, and infuenced distribution corridors. Te GE expansion [32–34]. If under such climatic changes geo- runs 50–200 km inland from the coastline and sepa- graphical events took place simultaneously, diversifca- rates the coastal plains from an elevated plateau more tion and speciation would have been further reinforced than 1000 m above sea level [13, 15]. Many research- and accelerated under their combined efect. ers believe that the GE represents a passive, erosional Southern Africa has an exceptionally diverse tortoise remnant of the continental margin after the break-up of fauna, harbouring one-third of the world’s tortoise gen- Gondwanaland, with its current topography dating to era [35], six genera with 14 species occurring in this the end of the Cretaceous ([15] and references therein). region [35]. Cladogenesis of Southern African tortoises In contrast, some geomorphological and thermochro- at the genus level occurred mainly in the Eocene, with nological studies advocate that upward fexures 30 Ma most species diverging between the Oligocene and [7] or 20 to 5 Ma [16], followed by erosion, established mid-Miocene [36]. Te latter study could not resolve or altered the topography of the GE. Uplift events relationships among the three Psammobates species, changed the course of fuvial systems [17], which can possibly due to rapid speciation between the late Oli- also afect genetic exchange among populations [11]. gocene and early Miocene. Te study also showed Te current course of the OR represents the confuence substantial divergence within Psammobates tentorius, of two paleo river systems [18]. Te paleo OR (Kalahari indicating the possible existence of hidden species River) drained most of Namibia and southern Botswana diversity or possibly the results of localized extinctions. since the Cretaceous while the Karoo River (Orange However, a recent tortoise phylogenomic study based and Vaal Rivers) drained most of South Africa and had on the complete mtDNA genome revealed that the its mouth further south at the current Olifants River genus Psammobates branched-of from Stigmochelys in [18]. Te Kalahari River captured the upper courses of the late Oligocene, and that the split between Psammo- the Karoo River by the early Cenozoic [18, 19]. bates geometricus and Psammobates oculifer was esti- mated to have started in the early Miocene. Zhao et al. BMC Evol Biol (2020) 20:153 Page 3 of 33 Regarding nomenclature, Hewitt [37, 38] described strong support, with each clade occurring in a distinct many species and subspecies based
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