Climatic and topographic changes since the Miocene influenced the diversification and biogeography of the tent tortoise (Psammobates tentorius) species complex in Southern Africa

Adriaan Jordaan,Zhongning Zhao,Neil Heideman,Margaretha D Hofmeyr,Phillip Bester

doi:10.1186/s12862-020-01717-1

Abstract

BackgroundClimatic 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.ResultsWe 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 intensification of the cold Benguela current, which caused western aridification and rainfall seasonality. In the south, tectonic uplift and subsequent exhumation, together with climatic fluctuations seemed responsible for radiations among the four southern clades since the late Miocene. We found that each clade occurred in a habitat shaped by different climatic parameters, and that the niches differed substantially among the clades of the northern group but were similar among clades of the southern group.ConclusionClimatic shifts, and biome and geographic changes were possibly the three major driving forces shaping 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.

Highlights

Climatic and topographic changes function as key drivers in shaping genetic structure and cladogenic radiation in many organisms
The study provided strong evidence that cladogenesis in P. tentorius can be linked to climatic fluctuations and topographic changes in Southern Africa since the Miocene, supporting our hypothesis
It appears if climate was of greater importance than topographic changes in earlier diversification events, but that uplift events together with climate change played a significant role in later divergences

Summary

Introduction

Climatic and topographic changes function as key drivers in shaping genetic structure and cladogenic radiation in many organisms. Apart from global cooling, Southern Africa became progressively more arid since the Oligocene [7], and the development of the Benguela Current 14–10 Ma [8, 9] increased western aridity and established seasonal rainfall patterns over Southern Africa by the late Miocene [4, 8]. Landscape evolution contributed to genetic diversification of Southern Africa’s fauna and flora [5], with the Cape Fold Mountains (CFMs), Great Escarpment (GE), and Orange River (OR) identified as potential geographic barriers to gene exchange in some taxa [10,11,12]. The paleo OR (Kalahari River) drained most of Namibia and southern Botswana since the Cretaceous while the Karoo River (Orange and Vaal Rivers) drained most of South Africa and had its mouth further south at the current Olifants River [18]. The Kalahari River captured the upper courses of the Karoo River by the early Cenozoic [18, 19]

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