Review Article |
Corresponding author: Uwe Fritz ( uwe.fritz@senckenberg.de ) Academic editor: Ralf Britz
© 2022 Uwe Fritz, Krystal A. Tolley, Melita Vamberger, Flora Ihlow.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Fritz U, Tolley KA, Vamberger M, Ihlow F (2022) Phylogeny and phylogeography of chelonians from sub-Saharan Africa—A review of current knowledge in tribute to Margaretha D. Hofmeyr. Vertebrate Zoology 72: 951-969. https://doi.org/10.3897/vz.72.e95681
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Species-level phylogeny and especially phylogeography of African chelonians is a comparatively under-studied field of research. We review the current knowledge of phylogeny and phylogeography, highlight congruence of spatial phylogeographic patterns amongst chelonians and other taxa and suggest future research directions to address gaps in knowledge. Our review shows that phylogeographic and phylogenetic investigations have led to unexpected findings. For example, for Pelomedusa, a putatively wide-ranging monotypic terrapin genus, cryptic diversity was revealed, with more than ten species being uncovered. The formerly recognized tortoise genus Homopus sensu lato was found to be paraphyletic with respect to Chersina. To resolve this situation, Homopus was restricted to the four-toed species H. areolatus and H. femoralis and the genus Chersobius was resurrected for the five-toed species C. boulengeri, C. signatus, and C. solus. Three previously recognized taxa were shown to be invalid, viz. the putatively extinct terrapin species Pelusios seychellensis and the tortoise subspecies Chersobius signatus cafer and Stigmochelys pardalis babcocki. Together with taxonomy, the knowledge of phylogeographic structuring sets a solid foundation for conservation measures and allows the identification of Management and Conservation Units. However, the current legislation, in particular the enforcement of the Nagoya Protocol under the Convention of Biological Diversity (CBD), has largely halted research on widely distributed taxa and turned the well-intended concept of Access and Benefit Sharing into a major impediment for conservation and research. The current situation leads for many species to a continued usage of outdated and incorrect taxonomic classifications resulting in an error cascade of conservation decisions. This is counterproductive to the aims of the CBD, that is, the protection of biodiversity. Sequencing historical DNA from museum specimens using aDNA approaches could be a short-term approach to mitigate, but not solve, this impediment.
CBD, Nagoya Protocol, Pelomedusidae, Reptilia, systematics, taxonomy, terrapin, Testudines, Testudinidae, tortoise, Trionychidae, turtle
Sub-Saharan Africa, in particular southern Africa (the continental region south of the Kunene, Okavango, and Zambezi rivers), is renowned for its diversity in tortoises (Testudinidae). Out of 52 currently recognized extant or recently extinct tortoise species, not fewer than 32 occur in Africa and 30 of these in sub-Saharan Africa (including Madagascar and islands of the western Indian Ocean). Five of these species became extinct since the 18th century (Cylindraspis spp., Mascarene Islands) due to targeted collection and hunting by humans. Nearly all species living in Africa are endemic to this continent (29), and of these, 14 occur in southern Africa, with 11 species confined to this region. In addition to this unique diversity of tortoises, sub-Saharan Africa and the adjacent Arabian Peninsula are home to five soft-shelled turtles (Trionychidae) and the endemic terrapin family Pelomedusidae with currently 27 recognized species. In addition, Madagascar is home to the only extant Old World representative (Erymnochelys madagascariensis) of the Podocnemididae, a family of side-necked turtles now otherwise confined to South America (
The past twenty years have seen a steady increase in the knowledge of the phylogenetic relationships and the phylogeography of African tortoises and freshwater turtles. The late Margaretha D. Hofmeyr (1950–2020) was, besides the late William R. Branch (1946–2018), an outstanding promoter of this research, as reflected by their co-authorships in a myriad of studies on the topic (Table
Phylogeographic and phylogenetic publications on African chelonians co-authored by Margaretha D. Hofmeyr.
Family | Taxon | Reference |
Pelomedusidae | Pelomedusa |
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Pelomedusidae | Pelomedusa, Pelusios |
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Pelomedusidae | Pelusios sinuatus |
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Testudinidae | Chersina angulata |
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Testudinidae | Chersobius signatus |
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Testudinidae | Cylindraspis |
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Testudinidae | Homopus areolatus |
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Testudinidae | Kinixys |
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Testudinidae | Psammobates tentorius |
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Testudinidae | Stigmochelys pardalis |
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Testudinidae | Testudinidae |
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The Pelomedusidae, endemic to sub-Saharan Africa and the southwestern Arabian Peninsula, are the sister group of the Podocnemididae, extant in South America and Madagascar. Together with their successive sister group, the Chelidae from South America, Australia, and New Guinea, they constitute the suborder Pleurodira (side-necked turtles;
With the seminal papers by
Within Pelusios, the phylogenetic relationships of individual species are more entangled than in Pelomedusa, with several species groups and some phylogenetically unique and divergent species (Pelusios gabonensis, P. marani, P. nanus; see
The phylogeographic patterns of the majority of pelomedusid terrapins remain unstudied. For Pelomedusa, only species from southern Africa have been examined in detail (
Pelomedusa subrufa sensu stricto is widespread in southern Africa, ranging from southern Angola and Namibia eastward to Mozambique. The species also occurs beyond southern Africa in East Africa and has been introduced in Madagascar (
Using 1,850 bp mtDNA and two nuclear loci (1,840 bp),
Unlike P. subrufa, its South African congener P. galeata shows pronounced genetic differentiation with two deeply divergent genealogical lineages (
In addition to the larger scale patterns, the eastern lineage of P. galeata shows further phylogeographic differentiation, with three distinct mitochondrial clades (Fig.
The few data available for other Pelomedusa species indicate that phylogeographic structure is also present within P. neumanni and P. somalica, each of which contains two deeply divergent mitochondrial lineages. In P. neumanni, one of these lineages has been recorded from the Omo River region in southernmost Ethiopia and Marsabit County, Kenya. The other lineage of P. neumanni has been found in Kakamega County, Kenya, in the Lake Victoria Region, and the Tanzanian Manyara Region. In P. somalica, one lineage has been recorded from Lake Koka in Ethiopia (Oromia Region) and the Somali Awdal Region. The other lineage was found in close proximity in the Awdal Region and most likely also in the Shebelle River region (Oromia, Ethiopia;
Using 2,036 bp of mtDNA,
For another East African Pelusios species (P. sinuatus),
Using 2,117 bp mtDNA and three nuclear loci (2,012 bp),
An unexpected finding was the relationship of P. rhodesianus to the morphologically highly distinctive P. carinatus. Pelusios rhodesianus was found to comprise two deeply divergent mitochondrial clades (from the center and west versus from the center and east of the distribution range), which were not differentiated with respect to nuclear DNA. The mitochondrial clade from the center and east, and the nuclear sequences of all P. rhodesianus, were paraphyletic with respect to P. carinatus, which constituted a well-supported clade nested in the paraphyletic P. rhodesianus. Within P. carinatus two subclades were found, one from the northwest of the Democratic Republic of the Congo and the other from Congo-Brazzaville and Gabon (Fig.
Paraphyly of Pelusios rhodesianus with respect to P. carinatus. Detail of maximum likelihood tree using up to 2,117 bp of mtDNA from
The phylogeographic structure of P. castaneus with distinct clades in (1) Cameroon, (2) Nigeria, Ivory Coast plus São Tomé, and (3) Congo-Brazzaville could reflect Pleistocene range interruptions correlated with the fluctuating forest cover in West and Central Africa (
With respect to P. chapini, phylogenetic analyses of mtDNA suggested weak differentiation from P. castaneus (
Further research should be conducted to examine the phylogeography of these and other widely distributed Pelusios species and to close the sampling gaps in Pelomedusa north of southern Africa (see
The family of land tortoises, or simply tortoises (Testudinidae), is the sister group of the Old World pond turtles (Geoemydidae) and represents, like the Trionychidae (see below), a clade that originated on Laurasia—the Cryptodira or hidden-necked turtles (
Several studies have examined the phylogeny of tortoises using molecular markers, among them
Simplified ancestral range analysis for tortoises (Testudinidae) based on mitochondrial genomes (15,510 bp; modified from
Among the 52 extant or recently extinct tortoise species (including the five recently extinct Cylindraspis species), 44 (85%) have their phylogenetic roots in Africa or live in Africa. Three out-of-Africa dispersal waves led to (1) the extant South American tortoise radiation (Chelonoidis spp., i.e., including the extant and extinct tortoises from Galápagos and the Bahamas), (2) the western and central Palearctic plus Southeast and South Asian tortoise radiation (Indotestudo, Testudo—including Malacochersus from sub-Saharan Africa), and (3) the South Asian radiation (Geochelone;
The multiple out-of-Africa dispersals of testudinid lineages. Numbers at arrows are inferred divergence times (million years) for the mitochondrial genomes of the respective taxa from their African sister lineages (from
Regarding southern African tortoise species,
A study on the borderline between phylogeography and phylogeny focused on the relationships within the hinged-back tortoise genus Kinixys (
Mitochondrial phylogeny of Kinixys species based on a 2,273-bp-long alignment of mtDNA (Bayesian analysis). Numbers at nodes are posterior probabilities and bootstrap values from a maximum likelihood analysis; asterisks indicate maximum support under both approaches (redrawn from
Phylogeographic variation has been studied in several testudinid species from sub-Saharan Africa, even though for many species only superficial data are available. In this review, the taxa will be presented in sequence roughly from north to south.
Compared to C. sulcata, the phylogeography of the second widely distributed African testudinid, Stigmochelys pardalis, has been well studied (
Populations of S. pardalis beyond South Africa and Namibia are poorly studied and a rangewide investigation could yield valuable insights in population structuring and the correlation of morphological traits and genetic differentiation. For instance, it is well known that S. pardalis displays extreme differences in body size across its range (
One of the most promising genera for future phylogeographic investigation is Kinixys with six poorly studied but widely distributed species (K. belliana, K. erosa, K. homeana, K. nogueyi, K. spekii, K. zombensis) and two range-restricted species (K. lobatsiana, K. natalensis). Despite highly patchy sampling and small sample sizes, the pioneering study by
The phylogenetic analyses (Fig.
Current research by Flora Ihlow using fresh samples and historical DNA from collection material aims at clarifying the phylogeographic differentiation and distribution of several Kinixys species.
A series of four papers by
It is clear that additional research is required to clarify the species number in the P. tentorius complex. For this, the application of an explicit species concept is a necessary prerequisite. Furthermore, cline analyses across contact zones of distinct genetic clusters would be promising to elucidate genetic break zones, especially if making use of variable nuclear markers, such as microsatellites or SNPs, in combination with information from mtDNA (compare
An additional challenge in the P. tentorius complex is the confusing nomenclatural history. No less than 26 species group names are synonymized under the three currently recognized subspecies (
Another Psammobates species, P. geometricus, belongs to the most threatened tortoise species of the world (
The phylogeography of Chersobius signatus, endemic to South Africa, was studied by
Records of genetic lineages of Pelomedusa galeata, Chersina angulata, and Homopus areolatus (based on mtDNA; combined from
Microsatellite analyses indicated broad admixture in the geographic contact zone of the two lineages and supported that they are conspecific under the Biological Species Concept (
Species distribution models indicated that the ranges of the two lineages have probably not shifted substantially since the Last Glacial Maximum, in accordance with demographic population descriptors suggestive of stationary distributions that did not experience expansion.
The phylogeography of Homopus areolatus was studied by
Despite the potential of expansion into secondary contact for the clades, species distribution models revealed that suitable climatic space has contracted overall since the LGM, probably caused by reduced rainfall in the west and higher temperatures in most regions. However, this postulated range contraction appears to be most directly linked to sea level rise since the LGM that has now excluded this species from the former southern extent of the range. Models also suggested that the two clades may be in greater contact at the zone of sympatry at present than during the LGM.
Soft-shelled turtles (Trionychidae) are one of the most distinctive and most ancient turtle families dating back to the Early Cretaceous (
The phylogeography of African trionychids is poorly studied, even though such information would be of special importance for the Critically Endangered Cyclanorbis elegans (
Several studies examined the phylogeography of Trionyx triunguis (
The results from
Previous publications suggested for some chelonian taxa from sub-Saharan Africa broad spatial phylogeographic congruence (Fig.
Despite notable progress, phylogeny and in particular phylogeography of sub-Saharan chelonians remain poorly studied for the majority of species and offer plenty of future research possibilities. Past investigations contributed to the discovery of previously unknown taxa and genealogical lineages in Pelomedusa, Pelusios, and Psammobates and unexpected phylogenetic relationships within Kinixys. Application of phylogenetic methods has also assisted to clarify taxonomy in these groups and in testudinids in general. Some of the more notable discoveries are the recognition of an additional tortoise genus (Chersobius), the unexpected diversity of Pelomedusa, and the debunking of Pelusios seychellensis and the subspecies of Chersobius signatus and Stigmochelys pardalis. Further discoveries are expected with additional research.
Cline analyses across contact zones of distinct genetic lineages would be a promising novel tool especially for Pelomedusa and the Psammobates tentorius complex that could provide insights into the degree of gene flow and taxonomic status. The knowledge of the phylogeographic diversity of sub-Saharan chelonians, which include many imperiled species, would offer a solid foundation for taxonomy and the identification of genetically distinct Management and Conservation Units for targeted conservation actions. Unfortunately, a major impediment to the future of such basic biological research, particularly for widely distributed taxa, is the current local and global legislative quagmire of red tape (
The Nagoya Protocol was intended to ensure that financial benefits from commercialization of the biological resources of a sovereign nation were realized by the people of that nation. Regrettably, non-commercial research (i.e., academic quest for knowledge) is treated with the same broad brush in terms of Nagoya as that applied to commercial research. In addition, the same rationale now applies to a major emerging debate regarding commercialization of ‘digital sequence information’ or ‘DSI.’ That is, some opponents seek to restrict the use of DNA sequence data stored on global public databases (such as GenBank/NCBI, ENA, and DDBJ), as these sequence data have been perceived as belonging to the nation from which the original DNA samples were sourced. While the application of controls for DSI as applied to commercial ventures has legitimacy, it has been argued that non-commercial research use of DSI should not fall under the same blanket approach (see
A short-term alternative for the use of fresh genetic samples, and thus a method to circumvent the described Nagoya obstacles, is offered by the application of aDNA approaches for phylogeographic studies using museum material. Sequencing historical DNA using Sanger and Illumina technologies has already contributed to the clarification of the taxonomy, nomenclature, and distribution of extinct and extant African terrapin and tortoise species (Pelomedusa spp.:
Essentially, stakeholders and parties to the CBD must hearken back to the real aims of the CBD, first and foremost—the conservation of biodiversity. It is therefore crucial to acknowledge that the CBD targets cannot be met unless there is strong support for, and fostering of, academic-based research including phylogenetic, phylogeographic and taxonomic research. Fair and equitable sharing of resources is certainly imperative in today’s social and economic landscape, but the inclusion of non-commercial, academic research under protocols that were set up for the intended purpose of providing benefit from commercialization of biological resources is detrimental to progress. Without a resolution that allows for academic research, the continued usage of outdated and incorrect taxonomic classifications will result in an error cascade of conservation decisions. This is counterproductive to the aims of the CBD as the discovery and recognition of new species likely would shift conservation aims tremendously (see for instance
We dedicate this article to our late friend and colleague Margaretha D. Hofmeyr. Without her inspiration and unforgotten companionship during fieldwork many of the publications reviewed in this article would never have been written. Theunis Hofmeyr, Retha’s husband, was the best field assistant and braai chef we could ask for. The authors also thank the late Bill Branch, Luis Ceríaco, Václav Gvoždík, James Harvey, Tomáš Mazuch, and Pavel Široký for photos used in our figures. Edoardo Razzetti and one anonymous reviewer provided helpful comments on an earlier version of this paper.