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Cryptic diversity in Rhampholeon boulengeri (Sauria: Chamaeleonidae), a pygmy chameleon from the Albertine Rift biodiversity hotspot
Abstract
Several biogeographic barriers in the Central African highlands have reduced gene flow among populations of many terrestrial species in predictable ways. Yet, a comprehensive understanding of mechanisms underlying species divergence in the Afrotropics can be obscured by unrecognized levels of cryptic diversity, particularly in widespread species. We implemented a multilocus phylogeographic approach to examine diversity within the widely distributed Central African pygmy chameleon, Rhampholeon boulengeri. Gene-tree analyses coupled with a comparative coalescent-based species delimitation framework revealed R. boulengeri as a complex of at least six genetically distinct species. The spatiotemporal speciation patterns for these cryptic species conform to general biogeographic hypotheses supporting vicariance as the main factor behind patterns of divergence in the Albertine Rift, a biodiversity hotspot in Central Africa. However, we found that parapatric species and sister species inhabited adjacent habitats, but were found in largely non-overlapping elevational ranges in the Albertine Rift, suggesting that differentiation in elevation was also an important mode of divergence. The phylogeographic patterns recovered for the genus-level phylogeny provide additional evidence for speciation by isolation in forest refugia, and dating estimates indicated that the Miocene was a significant period for this diversification. Our results highlight the importance of investigating cryptic diversity in widespread species to improve understanding of diversification patterns in environmentally diverse regions such as the montane Afrotropics.
... Introduction Hughes et al. (2018) confirmed those three lineages plus identified two additional genetically distinct lineages. Importantly, Hughes et al. (2018) found that the six total lineages (including R. boulengeri [sensu stricto]) did not overlap with R. hattinghi from the southern Albertine Rift, a species initially considered to be a conspecific population .Several previous accounts drew attention to R. boulengeri as a candidate species complex in need of taxonomic revision (e.g., Tilbury 2018) and Hughes et al. (2018) further revealed the extent to which this species is not monotypic. ...
... confirmed those three lineages plus identified two additional genetically distinct lineages. Importantly, Hughes et al. (2018) found that the six total lineages (including R. boulengeri [sensu stricto]) did not overlap with R. hattinghi from the southern Albertine Rift, a species initially considered to be a conspecific population . ...
... Several previous accounts drew attention to R. boulengeri as a candidate species complex in need of taxonomic revision (e.g., Tilbury 2018) and Hughes et al. (2018) further revealed the extent to which this species is not monotypic. In this paper, we rectify the taxonomic problems present in the R. boulengeri complex by integrating new morphological data with the molecular data from Hughes et al. (2018) to formally describe five new species from the Albertine Rift. ...
In a recent molecular study, the pygmy chameleon Rhampholeon boulengeri Steindachner, 1911 was shown to contain six genetically distinct, but phenotypically cryptic lineages. Phylogenetic analyses of genetic data demonstrated that several well-supported clades occurred in non-overlapping elevational ranges across the Albertine Rift in Central Africa. In order to resolve the taxonomy of the R. boulengeri complex, we examined the morphology of specimens representing all six genetic lineages, including the type specimens. Results supported the notion that the current taxonomy does not reflect species diversity and further uncovered the extent to which morphological differences were dissociated from genetic divergence in this complex. We formally describe five new species of Albertine Rift Rhampholeon, which reflects the species diversity more accurately within the region. All of the species are morphologically conserved and seem to exhibit a pattern of cryptic speciation similar to that observed in the genus and in other chameleon genera. Several of the new species are distributed in adjacent habitats, but occur in parapatry where they are separated by elevation, while species that overlap in elevation are allopatric. At least one of the new species exhibited bone fluorescence from its facial tubercles when examined under ultraviolet light, which is the first published account for the genus. Our results highlight the importance of investigating cryptic diversity using an integrative framework, especially for widespread species that look similar, and the description of these new species reinforces the Albertine Rift as one of the world’s richest biodiversity hotspots.
... Rhampholeon species are forest leaf-litter specialists with notably reduced vagility [1] and despite the presence of suitable migration corridors, they are unlikely to disperse over long distances [4]. As a possible consequence of this ecological characterization, most Pygmy Chameleon species presently are considered endemic to the single mountains or isolated forest patches from where they were originally described [5][6][7]. Rhampholeon (Rhampholeon) spectrum [8] (Fig 1), originally described from Bonjongo South of Mount Cameroon, is the type species for the genus Rhampholeon [9]. It is the only species known to occur in West-Central Africa (also referred by some authors as the Lower Guinean Forest) and exhibits an atypical disjunct distribution from the east African sister clade (Fig 2) which renders it of particular interest to biogeographers [4]. ...
... Manengouba [4], Mt. Nlonako [5], Mt. Kupe [2], and Korup National Park [9]), Gabon (Ivindo [3] and Mekambo [1]), and Equatorial Guinea (Bioko Island [5]). ...
... Nlonako [5], Mt. Kupe [2], and Korup National Park [9]), Gabon (Ivindo [3] and Mekambo [1]), and Equatorial Guinea (Bioko Island [5]). Voucher specimens are deposited in the herpetology collection of the University of Kansas and the California Academy of Science. ...
Pygmy Chameleons of the genus Rhampholeon represent a moderately diverse, geographically circumscribed radiation, with most species (18 out of 19 extant taxa) limited to East Africa. The one exception is Rhampholeon spectrum, a species restricted to West-Central African rainforests. We set out to characterize the geographic basis of genetic variation in this disjunctly distributed Rhampholeon species using a combination of multilocus Sanger data and genomic sequences to explore population structure and range-wide phylogeographic patterns. We also employed demographic analyses and niche modeling to distinguish between alternate explanations to contextualize the impact of past geological and climatic events on the present-day distribution of intraspecific genetic variation. Phylogenetic analyses suggest that R. spectrum is a complex of five geographically delimited populations grouped into two major clades (montane vs. lowland). We found pronounced population structure suggesting that divergence and, potentially, speciation began between the late Miocene and the Pleistocene. Sea level changes during the Pleistocene climatic oscillations resulted in allopatric divergence associated with dispersal over an ocean channel barrier and colonization of Bioko Island. Demographic inferences and range stability mapping each support diversification models with secondary contact due to population contraction in lowland and montane refugia during the interglacial period. Allopatric divergence, congruent with isolation caused by geologic uplift of the East African rift system, the “descent into the Icehouse,” and aridification of sub-Saharan Africa during the Eocene-Oligocene are identified as the key events explaining the population divergence between R. spectrum and its closely related sister clade from the Eastern Arc Mountains. Our results unveil cryptic genetic diversity in R. spectrum, suggesting the possibility of a species complex distributed across the Lower Guinean Forest and the Island of Bioko. We highlight the major element of species diversification that modelled today’s diversity and distributions in most West-Central African vertebrates.
... Such climate cycles could lead to a similar pattern to that posited for the Pleistocene of fragmentation of vegetation types into refugia followed by re-expansion. This repeated habitat fragmentation and contraction could promote allopatric speciation through vicariance, particularly for the Oligocene and Miocene epochs as suggested by numerous dated molecular studies (Fjeldså, 1994;Plana, 2004;Couvreur et al., 2008;Voelker et al., 2010;Branch, Bayliss, & Tolley, 2014;Hughes et al., 2018). It has been invoked to explain major faunistic and floristic disjunctions between Guineo-Congolian and East African rain forest species (see Section III.2a), presumably resulting from climatic shifts from the Oligocene through the Pliocene Couvreur et al., 2008). ...
... Evidence for this fragmentation mechanism is abundant in rain forest-restricted animal lineages. For example, speciation has been linked to forest fragmentation during the Oligocene and Miocene for at least three genera of chameleons from tropical Africa (Tolley et al., 2013;Branch et al., 2014;Ceccarelli et al., 2014;Hughes et al., 2018). In birds, recurrent forest fragmentation from the Miocene through the Pliocene has been implicated as the main factor impacting diversification Njabo, Bowie, & Sorenson, 2008;Voelker et al., 2010). ...
... Evidence suggests that most montane sister species in the Eastern Arc Mountains are allopatric but located on different montane areas, refuting in situ speciation (Hemp et al., 2010;Voelker et al., 2010;Missoup et al., 2012;Ceccarelli et al., 2014;Taylor et al., 2014). This mechanism has also been proposed in other mountain regions of Africa such as the Albertine Rift and Kenyan Highlands (Demos et al., 2014;Hughes et al., 2018), the Cameroon Volcanic Line (Zimkus & Gvoždík, 2013;Taylor et al., 2014;Missoup et al., 2016) and the inselbergs of northern Mozambique (Branch et al., 2014;Bittencourt-Silva et al., 2016). ...
Tropical Africa is home to an astonishing biodiversity occurring in a variety of ecosystems. Past climatic change and geological events have impacted the evolution and diversification of this biodiversity. During the last two decades, around 90 dated molecular phylogenies of different clades across animals and plants have been published leading to an increased understanding of the diversification and speciation processes generating tropical African biodiversity. In parallel, extended geological and palaeoclimatic records together with detailed numerical simulations have refined our understanding of past geological and climatic changes in Africa. To date, these important advances have not been reviewed within a common framework. Here, we critically review and synthesize African climate, tectonics and terrestrial biodiversity evolution throughout the Cenozoic to the mid-Pleistocene, drawing on recent advances in Earth and life sciences. We first review six major geo-climatic periods defining tropical African biodiversity diversification by synthesizing 89 dated molecular phylogeny studies. Two major geo-climatic factors impacting the diversification of the sub-Saharan biota are highlighted. First, Africa underwent numerous climatic fluctuations at ancient and more recent timescales, with tectonic, greenhouse gas, and orbital forcing stimulating diversification. Second, increased aridification since the Late Eocene led to important extinction events, but also provided unique diversification opportunities shaping the current tropical African biodiversity landscape. We then review diversification studies of tropical terrestrial animal and plant clades and discuss three major models of speciation: (i) geographic speciation via vicariance (allopatry); (ii) ecological speciation impacted by climate and geological changes, and (iii) genomic speciation via genome duplication. Geographic speciation has been the most widely documented to date and is a common speciation model across tropical Africa. We conclude with four important challenges faced by tropical African biodiversity research: (i) to increase knowledge by gathering basic and fundamental biodiversity information; (ii) to improve modelling of African geophysical evolution throughout the Cenozoic via better constraints and downscaling approaches; (iii) to increase the precision of phylogenetic reconstruction and molecular dating of tropical African clades by using next generation sequencing approaches together with better fossil calibrations; (iv) finally, as done here, to integrate data better from Earth and life sciences by focusing on the interdisciplinary study of the evolution of tropical African biodiversity in a wider geodiversity context.
... Molecular systematics research has yielded robust phylogenies depicting well-supported evolutionary histories for all chameleon genera and nearly all species (Ceccarelli et al., 2014;Hughes, Kusamba, Behangana, & Greenbaum, 2017;Hughes, Tolley, et al., 2018a;Tolley et al., 2011), as well as reconstructions of their evolutionary ecology (Tolley, Townsend, & Vences, 2013a) and reproductive history (Andrews & Karsten, 2010). Such integrative works have substantially advanced our understanding of chameleon evolution and offer valuable frameworks for resolving questions of how often and under what ecological circumstances chameleon viviparity has originated. ...
... Two more oviparous species, T. johnstoni and an unnamed pygmy chameleon (Rhampholeon sp. 5: Hughes, Tolley, et al., 2018a), can also be found at high elevations in the Rwenzori Mountains (up to nearly 3,000 m) (Tilbury, 2010(Tilbury, , 2018. In contrast, ...
Historically, an understanding of viviparity and its evolution in Old World chameleons (Chamaeleonidae) has lagged behind that of other squamate families. Not only is reproductive information scarce or entirely absent for most chameleon species, but the literature reveals no consensus as to the frequency and ecological circumstances under which chameleon viviparity evolved. We integrated information on reproductive modes for nearly all chameleon species with recently published family‐scale phylogenetic and ecological analyses to clarify aspects of reproductive evolution in chameleons. Ancestral‐trait reconstructions, after accounting for phylogenetic uncertainty, indicated that viviparity has arisen a minimum of three times in Chamaeleonidae, with each origin of live birth in closed‐canopy forests. Our maximum‐likelihood optimization therefore did not support the previous hypotheses of one, two or four origins of viviparity in the family. Past claims that arboreality would not allow for evolution of viviparity were also not supported, nor was a recent suggestion that viviparity has reverted to oviparity. However, cold climates of high latitudes and elevations may have selected for viviparity in arboreal chameleons. While peritoneal pigmentation may facilitate viviparity, its role as an exaptation rather than an adaptation remains equivocal without data from a wider range of chameleon species. Based on a comprehensive review of reproductive modes throughout the family, our study has resolved the number of origins of viviparity in Chamaeleonidae and provided evidence that live birth evolved under arboreal conditions on three separate occasions in this enigmatic squamate group. This study also reveals the value of using phylogenetic analysis in a manner that is robust to uncertainty (rather than simple correlational approaches) when the goal is to reconstruct evolutionary sequences and selective pressures. We found three origins of viviparity in Chamaeleonidae, with each origin of live birth in closed‐canopy forests. Past claims that arboreality would not allow for evolution of viviparity were not supported, nor was a recent suggestion that viviparity has reverted to oviparity in chameleons. This study highlights the value of using phylogenetic comparative analysis in a manner that is robust to uncertainty when the goal is to reconstruct evolutionary sequences and selective pressures.
... Several new species of amphibians and reptiles have recently been discovered or recorded for the first time from Nyungwe Forest and its surroundings [17,[34][35][36][37][38]. The discovery of yet another new species from Nyungwe Forest and Cyamudongo Forest indicates that the herpetofaunal diversity of these forests is still not fully assessed. ...
A new, very small-sized species of Arthroleptis is described from western Rwanda. The new species occurs locally endemic in Nyungwe Forest and Cyamudongo Forest, where it inhabits the leaf litter of montane forests between 1800 and 2200 m a.s.l. It differs from all other members of the genus by a unique combination of morphological characters, including size (SVL of adult males 16.0-16.5 mm), skin texture, length of hindlimbs, and ventral colour pattern; by characteristics of its advertisement call that consists of a single note lasting 17.4 ± 6.4 [11-32] ms and has a dominant frequency of 5861 ± 188 [5531-6029] Hz; and also in the sequence of the 16S rRNA gene that differs from available homologous sequences of other species of the genus by an uncorrected p-distance of at least 4.6%. Details of the natural history as well as two additional call types are described.
... More attention has recently been focused on hidden biodiversity, phylogeography, speciation and multiple genetically divergent, but morphologically cryptic lineages for various taxa within the EAR (Bannikova et al., 2021;Demos et al., 2014;Hughes et al., 2018;Mairal et al., 2017;Onditi et al., 2021). Integrative approaches have proven extremely valuable in the detection of unrecognized diversity for rheophilic fishes of the region, particularly widespread taxa Chakona et al., 2018;Moritz et al., 2019;Schmidt et al., 2014Schmidt et al., , 2015Schmidt et al., , 2017Schmidt et al., , 2018. ...
The cyprinid genus Garra is so far represented in Mount Kenya streams by a single species, but which species it should be referred to as remains yet to be determined. Molecular phylogenetic analysis of Garra species from the mountain is still lacking. Here, an integrative analysis, based on morphological and molecular data, unravelled the hidden species diversity of Garra from Mount Kenya. In mitochondrial genes‐based trees, samples formerly identified as Garra dembeensis from the mountain nested into three distinct lineages that were distantly allied to the lineage constituted by topotypical samples of the species; the three lineages are morphologically distinguishable, and thus represent three distinct species: Garra hindii and two undescribed species, herein named as Garra alticauda sp. nov. and Garra minibarbata sp. nov., respectively, from the Mara River and the Ragati River of the mid‐upper Tana River basin. The phylogeographic pattern of the three species is incongruent with the present‐day basin pattern of Mount Kenya. The allopatry of the paired species G. alticauda and G. hindii points to river piracy ever incurring between the upper Ewaso Ngiro River and the middle Tana River basin in Mount Kenya. Besides, the molecular phylogenetic analysis of sampled African Garra species in this study, based on a broad set of sequences, provides evidence in support for the existing hypothesis of Asia‐to‐Africa biodispersal via the Arabian Peninsula to the Horn of Africa.
... A similar pattern occurred in the Sclerophrys superciliaris toad complex until the eastern DRC population was recognized as a distinct species, S. channingi (Barej et al. 2011), but in contrast to A. lacustris, the former species is now known to be widespread in the Congo Basin of DRC (Vaughan et al. 2019). More surprising were our findings that the AR and surrounding forests harbor two new cryptic species that are separated by elevation, but a similar pattern has been found in other AR taxa with homogeneous habitat requirements (e.g., Rhampholeon, Hughes et al. 2018). ...
... A similar pattern occurred in the Sclerophrys superciliaris toad complex until the eastern DRC population was recognized as a distinct species, S. channingi (Barej et al. 2011), but in contrast to A. lacustris, the former species is now known to be widespread in the Congo Basin of DRC (Vaughan et al. 2019). More surprising were our findings that the AR and surrounding forests harbor two new cryptic species that are separated by elevation, but a similar pattern has been found in other AR taxa with homogeneous habitat requirements (e.g., Rhampholeon, Hughes et al. 2018). ...
The geographically widespread species Afrixalus laevis (Anura: Hyperoliidae) currently has a disjunct distribution in western Central Africa (Cameroon, Equatorial Guinea, Gabon, and possibly adjacent countries) and the area in and near the Albertine Rift in eastern Democratic Republic of the Congo and neighboring countries. At least two herpetologists have previously suggested that these disjunct populations represent distinct species, and herein, we utilize an integrative taxonomic approach with molecular and morphological data to reconcile the taxonomy of these spiny reed frogs. We sequenced 1554 base pairs of the 16S and RAG1 genes from 34 samples of A. laevis and one sample of A. orophilus (sympatric with eastern populations of A. laevis), and combined these data with previously sequenced GenBank Afrixalus samples via the bioinformatics toolkit SuperCRUNCH. Phylogenetic trees, dated phylogenetic analyses, and species-delimitation analyses were generated with RAxML, BEAST, and BPP, respectively. Eleven mensural characters were taken from multiple specimens of A. laevis and A. orophilus, and compared with paired t-tests and analyses of covariance. These combined results suggested populations of A. laevis in western Central Africa (Cameroon and Bioko Island, Equatorial Guinea) represent one species, whereas populations from the Albertine Rift and nearby forests represent two undescribed taxa that are sister to A. dorsimaculatus. The two new species (A. lacustris sp. nov. and A. phantasma sp. nov.) are distinguished by our phylogenetic and species-delimitation analyses, significant differences in several mensural characters, qualitative morphological differences, and by their non-overlapping elevational distribution.
... Many species complexes are typified by morphological conservatism (Stuart et al. 2006;Oliver et al. 2009;Murray et al. 2012;Puckridge et al. 2013;Heinicke et al. 2017;Hughes et al. 2018;Tolley et al. 2018), yet identification of specimens relies heavily on morphological traits to distinguish species. In some cases, even experts may struggle to identify species using morphological characters alone, and locality information is sometimes used to ultimately make an identification by checking existing distribution maps. ...
It is commonly recognised that natural history datasets contain locality errors that can compromise the utility of those datasets. However, another source of error in these datasets is taxonomic misidentifications, and this type of error is potentially common, particularly with regards to morphologically conservative species. For example, in the African skinks, the Trachylepis striata and T. varia species complexes each contain morphologically similar species that are commonly confused, despite being genetically distinct. Some species also are partly sympatric, and misidentifications are likely to be especially problematic in those areas. Using DNA barcoding, we assessed misidentification rates between species and applied the updated identifications to known distribution maps to examine whether those maps are accurate representations. Existing banked samples and newly collected samples were DNA barcoded using the mitochondrial 16S gene and supplemented with GenBank data. Identifications were made by matching sequences using haplotype networks that included material from near type localities. The barcode-based identifications were compared with the original identifications recorded for those samples. Taxonomic error was common, particularly in areas of presumed sympatry (error for T. striata species complex: 28%; T. varia species complex: 31%) and this resulted in inaccurately represented species distributions and areas of sympatry. Areas of sympatry were, however, confirmed for T. spilogaster/T. punctatissima, T. striata/T. punctatissima and T. damarana/T. laevigata/T. varia. Our findings corroborate other studies that demonstrate taxonomic error in existing datasets is a significant, but typically unrecognised problem, particularly for morphologically conservative species. This has implications for the utility of historical collections, citizen science records and public databases used in the formulation of species distribution maps, but also for other downstream analyses that rely on these datasets.
... This Eastern Afromontane region (EAR) exhibits an outstanding level of species richness, endemism and diversification (Mittermeier et al. 2011;Demos et al. 2014;Mairal et al. 2017) and can be also considered an extraordinary biogeographical unit for chameleon diversity (Mariaux and Tilbury 2006;Ceccarelli et al. 2014;Menegon et al. 2015;Hughes et al. 2018). The geographical uniqueness of this region is shaped by the Great Rift Valley, a geological longitudinal split between the Somalian and Nubian Plate, running nearly 5,000 km through the African Plate from the Red Sea to Mozambique (Chorowicz 2005). ...
A new species of chameleon, Trioceros wolfgangboehmei sp. nov. , inhabiting the northern slopes of the Bale Mountains in Ethiopia, is described. It differs from its Ethiopian congeners by a combination of the following features: presence of a prominent dorsal crest with a low number of enlarged conical scales reaching along the anterior half of the tail as a prominent tail crest, a casque raised above the dorsal crest, heterogeneous body scalation, long canthus parietalis, rugose head scalation, high number of flank scales at midbody and unique hemipenial morphology. Based on morphological characteristics, phylogenetic discordances of previous studies and biogeographical patterns, this new species is assigned to the Trioceros affinis (Rüppell, 1845) species complex. An updated comprehensive key to the Trioceros found in Ethiopia is provided.
... Further analysis is necessary to determine if these divergences represent distinct species or genetically structured populations. The Albertine Rift highlands house an extremely high number of endemic species (Greenbaum 2017), especially birds (Stuart et al. 1990), amphibians (Greenbaum & Kusamba 2012) and reptiles (Hughes et al. 2018), and it is likely that some of the genetic diversity recovered here is representative of unrecognized taxonomic diversity. ...
The genus Trachylepis is widespread throughout most of continental Africa and its surrounding islands. However , the majority of phylogenetic studies on this genus have focused on species occurring in eastern and southern Africa. Herein, we examine relationships among ten Trachylepis taxa that occur in Central and West Africa: T. affinis, T. albilabris, T. aureogularis, T. gonwouoi, T. maculilabris, T. mekuana, T. perrotetii, T. polytropis polytropis, T. polytropis paucisquamis, and T. quinquetaeniata. Five genes (two mitochondrial and three nuclear) were sequenced for 153 individuals, revealing much higher levels of diversity than previously realized, and justifying the need for future taxonomic investigations. Because of high levels of morphological conservatism in Trachylepis, the taxonomy of each of these species is complex, and previously synonymized names may be available for several lineages. Molecular dating techniques suggest that while the two major clades of Trachylepis represented in this study diverged approximately 23 million years ago, the majority of diversification took place in the last 17 million years. Further work is needed to fill in sampling gaps and increase genetic coverage for some clades before the full genetic diversity of this group can be realized.
... We also used taxonomic rearrangements made by several specialists in herpetological taxonomy (Thys van Den Audaenerde, 1963a,b;Roux-Estève, 1974;Townsend et al., 2004;Vidal & Hedges, 2005;Hedges, 2014). Moreover, as Operational Taxonomic Units (OTU) are recognised globally (Sokal & Sneath, 1963;Blaxter et al., 2005;Cheng et al., 2013), we paid particular attention to all of them, and they were published by our teams as distinct lineages on which further ongoing taxonomic studies were undertaken and have already afforded new species (Larson et al., 2016;Hughes et al., 2017;Broadley et al., 2018;Hughes et al., 2018;Portillo et al., 2018;Wüster et al., 2018). This work is produced based on long-term and large-scale surveys. ...
To date, knowledge about the herpetological diversity and the species distribution in the Democratic Republic of the Congo remains largely incomplete. In order to fill this gap, we carried out long-term and large-scale herpetological surveys to improve the knowledge about the herpetofauna occurrence and species composition data. Site scanning, visual encounter, transect and quadrat methods were used along with call recordings for identifying and locating amphibians on each survey site. Additional data were gathered from literature reviews and museum collections. The herpetological diversity was assessed on twenty-eight survey sites located in both Congo Basin and Albertine Rift ecoregions. All surveyed localities and sites were georeferenced in order to generate distribution maps by using QGIS 2.14.0 software. Herpetological diversity indices were generated using the PAST software. Using morphological characters and information provided by DNA analysis, species lists were produced per site and on national level. The results show that the rich Congolese herpetofauna is composed of 605 species, including 247 (40.83%) amphibians and 358 (59.17%) reptiles. There are 57 endemic amphibian species (23.1%) and of these, 19 (32.7%) are located in Protected Areas. There are 38 endemic reptile species (10.6%) and of these, twelve (31.5%) are found in Protected Areas. Furthermore, there are nine and seventeen threatened amphibian and reptile species respectively; but only 20% of these have been detected inside of national parks. Concerning this situation, it appears that, if no action is undertaken for fighting against the human pressure on habitat, there will be a decline in populations and species in the Democratic Republic of the Congo. Based on relevant indices, including species richness, rarity, diversity, endemism, and presence of threatened species, and other objective criteria in respect to international standards, the following ten sites were identified as sites of priority for conservation: Marungu, Kabobo, Itombwe, Ituri, Tshopo, Mai Ndombe Tumba, Lualaba, Lukaya, Sankuru, and Ubangi Uele. These sites are proposed as new Protected Areas for reaching the government's national conservation targets of land preservation necessary for conserving the rich biodiversity.
... While all mammals, birds, and amphibians have been assessed on the IUCN Red List, many reptiles and plants have not, so that these numbers will increase as more of these taxa are assessed. As the taxonomy of amphibians and reptiles is in flux in the region, it is also likely that more species will be identified and many of these may be threatened (Hughes et al., 2018;Hughes, Kusamba, Behangana, & Greenbaum, 2018;Portillo, Greenbaum, Menegon, Kusamna, & Dehling, 2015). The national red listing process identified 208 terrestrial vertebrates and 80 plants as threatened in Uganda (Table 2), with an additional 135 DD species. ...
Uganda is one of the most species rich countries in Africa because of the presence of several major biomes. However, it is also a country that has lost much of its natural habitat to agriculture. Uganda is a country that has been better surveyed for its biodiversity than many African countries, but despite this, there has not been a comprehensive analysis of the critical sites that contribute to biodiversity conservation at a global, as well as at a national level. We here present such an assessment using mammals, birds, reptiles, amphibians, and plants as surrogate taxa. We identified 36 terrestrial sites that are of sufficient global importance to qualify as Key Biodiversity Areas (KBAs), using the Global Standard for the Identification of KBAs, which complement an additional nine freshwater sites. National red listing of species and ecosystems was used to identify sites of national importance for conservation. We employ a conservation planning approach using Marxan to identify the minimum set of sites needed to conserve all the globally and nationally threatened species and nationally threatened habitats in Uganda. The findings show that most of the remaining natural habitat in Uganda is important for the conservation of globally and nationally threatened species and threatened habitat. Large areas of irreplaceable habitat occur outside protected areas, although more extensive surveys of these areas would likely reduce the area that is irreplaceable. Priority areas for conservation of both globally and nationally threatened species are identified for the first time in Uganda. Our analysis shows that most natural habitat remaining in the country is critical for the conservation of the rich biodiversity of this country.
... While all mammals, birds, and amphibians have been assessed on the IUCN Red List, many reptiles and plants have not, so that these numbers will increase as more of these taxa are assessed. As the taxonomy of amphibians and reptiles is in flux in the region, it is also likely that more species will be identified and many of these may be threatened (Hughes et al., 2018;Hughes, Kusamba, Behangana, & Greenbaum, 2018;Portillo, Greenbaum, Menegon, Kusamna, & Dehling, 2015). The national red listing process identified 208 terrestrial vertebrates and 80 plants as threatened in Uganda (Table 2), with an additional 135 DD species. ...
Uganda is one of the most species rich countries in Africa because of the presence of several major biomes. However, it is also a country that has lost much of its natural habitat to agriculture. Uganda is a country that has been better surveyed for its biodiversity than many African countries, but despite this, there has not been a comprehensive analysis of the critical sites that contribute to biodiversity conservation at a global, as well as at a national level. We here present such an assessment using mammals, birds, reptiles, amphibians, and plants as surrogate taxa. We identified 36 terrestrial sites that are of sufficient global importance to qualify as Key Biodiversity Areas (KBAs), using the Global Standard for the Identification of KBAs, which complement an additional nine freshwater sites. National red listing of species and ecosystems was used to identify sites of national importance for conservation. We employ a conservation planning approach using Marxan to identify the minimum set of sites needed to conserve all the globally and nationally threatened species and nationally threatened habitats in Uganda. The findings show that most of the remaining natural habitat in Uganda is important for the conservation of globally and nationally threatened species and threatened habitat. Large areas of irreplaceable habitat occur outside protected areas, although more extensive surveys of these areas would likely reduce the area that is irreplaceable. Priority areas for conservation of both globally and nationally threatened species are identified for the first time in Uganda. Our analysis shows that most natural habitat remaining in the country is critical for the conservation of the rich biodiversity of this country.
... Taking this into consideration, it seems likely that SJ diverged from the other clusters of P. brevirostris due to parapatric speciation via niche differentiation (Moritz et al., 2000). Evidence for this process is particularly convincing in the case of montane ectotherm vertebrates (e.g., Arteaga et al., 2016;Hughes et al., 2018;Hutter et al., 2013) and has also been documented in other highland Mexican taxa (e.g., Mastretta-Yanes et al., 2015;Rovito et al., 2013). More detailed niche analyses could possibly detect ecological differentiation between SJ and OX, which was not detected by our iBPP analysis. ...
Integrative taxonomy has been generally considered as a goal in systematics for more than a decade. Here, we employed environmental, molecular, and morphological data to evaluate the species boundaries within the short-nosed skink Plestiodon brevirostris from south-central Mexico, one member of the morphologically conservative P. brevirostris group. Our molecular dataset includes one mitochondrial and two nuclear loci. The mitochondrial fragment includes the full length of the gene coding for the NADH dehydrogenase subunit 1 protein, a segment of the gene coding for 16S ribosomal RNA, and flanking tRNAs. The nuclear dataset includes fragments of the genes coding for the megakaryoblastic leukemia 1 and RNA fingerprint 35 proteins. We employed phylogenetic reconstruction, analyses of population structure and morphological variation, and species delimitation methods (including the integration of the three kinds of data in a unified probabilistic framework) to evaluate species limits. Our results suggest that P. brevirostris represents four distinct species. The information provided by each kind of data allowed us to discern between alternative explanations for the observed patterns of geographic structure. Two of the newly recognized lineages are poorly differentiated morphologically but apparently differ in environmental preferences and are allopatric. Additionally, one lineage is microendemic and parapatric with respect to another one. Moreover, our phylogenetic analyses suggest that other taxa within the P. brevirostris group may represent species complexes. We discuss our results in the context of integrative species delimitation.
... As an example, it has been shown that the relationship between species richness and geography, the basis of determining global biodiversity hotspots, can be greatly biased if the number of species is underestimated (Hortal et al., 2015). These knowledge gaps in species-level taxonomy, the so-called Linnean shortfall, are particularly prevalent in tropical species (e.g., Hughes et al., 2017); they also characterize recently diverged and morphologically conservative clades where cryptic species are present (Fišer et al., 2018) and incomplete lineage sorting is expected due to recency of common ancestry (Hudson and Coyne, 2002). Coalescent species delimitation methods take advantage of multi-locus sequence data now available for many taxa in need of systematic revision and offer more objective assessments of diversity in these groups (Fujita et al., 2012;Yang and Rannala, 2014). ...
The genus Scotophilus contains 21 currently recognized species ranging throughout Africa and Southeast Asia. Among the 13 species recognized from continental Africa, systematic relationships remain poorly understood. Taxonomic uncertainty regarding names, suggestions of polytypic species complexes, and undescribed cryptic diversity all contribute to the current confusion. To gain insights into the systematics of this group, we inferred single locus and multi-locus phylogenies and conducted lineage delimitation analyses using seven unlinked genes for specimens from across Africa. Recent collections from Kenya allowed us to carry out population-level analyses for the diverse assemblage of East African Scotophilus. Multi-locus coalescent delimitation methods indicated strong support for three recently named lineages thought to be restricted to Kenya and Tanzania; it also uncovered two new distinctive lineages at present known only from Kenya. Subsequent taxonomic assessments that integrate these genetic data with phenotypic, distributional, and/or ecological traits are needed to establish these lineages as valid species. Nevertheless, as many as 15 Scotophilus species may occur in continental Africa, 10 of these in Kenya alone. Our analysis highlights the importance of population-level surveys for the detection of cryptic diversity in understudied regions such as the Afrotropics.
... these subspecies have also been referred to as sporadic variants of the typical C. dilepis and some of the recorded distributions are overlapping (see Tilbury 2010). Cryptic diversity is not unusual within chameleons, with reported cases in the Malagasy chameleon genus Calumma as well as in the African genera Bradypodion, Rhampholeon and Kinyongia; the presence of these cryptic lineages was uncovered through extensive genetic analyses (Tolley et al. 2004;Raxworthy and Nussbaum 2006;Gehring et al. 2012;Branch et al. 2014;Hughes et al. 2017Hughes et al. , 2018Prötzel et al. 2017). Should C. dilepis consist of multiple cryptic lineages, this would potentially have an effect on its IUCN Red List status. ...
The spatial genetic structure of a species, and whether distinct genetic lineages are present, is strongly influenced by their biology and habitat requirements. Given habitat specificity and low vagility, many herpetofaunal species are reservoirs for high levels of cryptic diversity; chameleons are a case in hand. The common flap-necked chameleon Chamaeleo dilepis has a large range that spans much of sub-Saharan Africa. Within South Africa, the species is largely confined to the north-eastern and central areas of the country, and occurs from the coastal forests in southern KwaZulu-Natal westwards into Namibia. Their large range, together with anecdotal evidence that there is considerable morphological and phenotypic diversity across the range, suggests a questionable taxonomy with possible cryptic lineages. The aims of the present study were to investigate whether C. dilepis is genetically structured across parts of its South African range, and whether this species (as it currently stands) might include cryptic lineages. To this end, 72 C. dilepis individuals sampled from four localities across South Africa (Gauteng, n = 2; KwaZulu-Natal, n = 2) were sequenced for two mitochondrial markers (ND4 and 16S). The phylogenetic results suggest that C. dilepis is indeed spatially structured. In addition, the large sequence divergence values between groups strongly suggests the presence of cryptic lineages and, pending the inclusion of more data from a larger geographic range, the group may be in need of a taxonomic revision.
Pyricularia oryzae and P. grisea are important agents of major diseases on a wide range of gramineous hosts. Whereas P. oryzae is the most important pathogen causing outbreaks of rice blast, P. grisea is mainly a pathogen of crabgrass. In this study, 103 P. oryzae and 20 P. grisea isolates were collected from seven species of plants, and we analyzed their phylogeny, pathogenicity, and relationship with host preferences to investigate the differences among them from different hosts. Based on phylogenetic analysis of multilocus sequences, 16 isolates from crabgrass and four isolates from green bristlegrass were identified as P. grisea and another 103 isolates from crabgrass, green bristlegrass, goose grass, foxtail millet, wild millet, rice, and sedge belonged to P. oryzae. Results of pathogenicity tests by artificial inoculation demonstrated that six of 10 P. oryzae isolates from rice and three of 44 P. oryzae isolates from green bristlegrass showed cross-infectivity on green bristlegrass and rice, respectively. Taken together, our results demonstrated that isolates from green bristlegrass and crabgrass consist of both P. oryzae and P. grisea and that P. oryzae isolates showed cross-infectivity between rice and green bristlegrass, suggesting that host shifts may occur for P. oryzae and P. grisea.
Jackson's Forest Lizard (Adolfus jacksoni) is widespread throughout the highlands of the Albertine Rift, southern Uganda, western and central Kenya, and northern Tanzania. To understand the population genetics and phylogenetic relationships of this widespread taxon, we sequenced two mitochondrial (16S and cyt b) and two nuclear (c-mos and RAG1) genes from multiple populations. Population genetics analyses suggested a high degree of genetic differentiation among A. jacksoni populations, reflecting the high-elevation montane "islands" that they inhabit. Populations connected by a network of mountain ranges generally showed lower levels of genetic partitioning than those isolated by low-elevation habitat. Results from phylogenetic analyses and additional morphological data indicated that Adolfus jacksoni occurs throughout the Albertine Rift, likely from the Kabobo Plateau to the Lendu Plateau of Democratic Republic of the Congo, as well as southern Uganda, Mt. Elgon, and the highlands of western Kenya on the western side of the Kenyan Rift. Adolfus kibonotensis is removed from the synonymy of the latter taxon, elevated to full species, and recognized from the central Kenyan highlands to northern Tanzania on the eastern side of the Kenyan Rift. A new Adolfus species is described from the Mathews Range in central Kenya.
We present the latest version of the Molecular Evolutionary Genetics Analysis (MEGA) software, which contains many sophisticated
methods and tools for phylogenomics and phylomedicine. In this major upgrade, MEGA has been optimized for use on 64-bit computing
systems for analyzing bigger datasets. Researchers can now explore and analyze tens of thousands of sequences in MEGA. The
new version also provides an advanced wizard for building timetrees and includes a new functionality to automatically predict
gene duplication events in gene family trees. The 64-bit MEGA is made available in two interfaces: graphical and command line.
The graphical user interface (GUI) is a native Microsoft Windows application that can also be used on Mac OSX. The command
line MEGA is available as native applications for Windows, Linux, and Mac OSX. They are intended for use in high-throughput
and scripted analysis. Both versions are available from www.megasoftware.net free of charge.
The genus Naja Laurenti, 1768, is partitioned into four subgenera. The typical form is restricted to 11 Asian species. The name Uraeus Wagler, 1830, is revived for a group of four non-spitting cobras inhabiting savannas and open formations of Africa and Arabia, while Boulengerina Dollo, 1886, is applied to four non-spitting African species of forest cobras, including terrestrial, aquatic and semi-fossorial forms. A new subgenus is erected for seven species of African spitting cobras. We recommend the subgenus rank as a way of maximising the phylogenetic information content of classifications while retaining nomenclatural stability.
Emerald Labyrinth is a scientist and adventurer’s chronicle of years exploring the rainforests of sub-Saharan Africa. The richly varied habitats of the Democratic Republic of the Congo offer a wealth of animal, plant, chemical, and medical discoveries. But the country also has a deeply troubled colonial past and a complicated political present. Author Eli Greenbaum is a leading expert in sub-Saharan herpetology—snakes, lizards, and frogs—who brings a sense of wonder to the question of how science works in the twenty-first century. Along the way he comes face to face with spitting cobras, silverback mountain gorillas, wild elephants, and the teenaged armies of AK-47-toting fighters engaged in the continent’s longest-running war.
As a bellwether of the climate and biodiversity crises now facing the planet, the Congo holds the key to our planet’s future. Writing in the tradition of books like The Lost City of Z, Greenbaum seeks out the creatures struggling to survive in a war-torn, environmentally threatened country. Emerald Labyrinth is an extraordinary book about the enormous challenges and hard-won satisfactions of doing science in one of the least known, least hospitable places on earth.
The Albertine Rift (AR) is a centre for vertebrate endemism in Central Africa, yet the mechanisms underlying line-age diversification of the region's fauna remain unresolved. We generated a multilocus molecular phylogeny consisting of two mitochondrial (16S and ND2) and one nuclear (RAG1) gene to reconstruct relationships and examine spatiotemporal diversification patterns in the AR endemic forest chameleon, Kinyongia adolfifriderici (Sternfeld, 1912). This widely distributed species was revealed to be a complex of four genetically distinct and geographically isolated species. Three new species are described based on molecular analyses and morphological examinations. We find that K. rugegensis sp. nov. (Rugege Highlands) and K. tolleyae sp. nov. (Kigezi Highlands) form a well-supported clade, which is sister to K. gyrolepis (Lendu Plateau). Kinyongia itombwensis sp. nov. (Itombwe Plateau) was recovered as sister to K. adolfifriderici (Ituri Rainforest). The phylogeographic patterns we recovered for Kinyongia suggest that speciation stemmed from isolation in forest refugia. Our estimated diversification dates in the Miocene indicate that most species of Kinyongia diverged prior to the aridification of Africa following climate fluctuations during the Pleistocene. Our results highlight the AR as a focal point of diversification for Kinyongia, further elevating the global conservation importance of this region.
Aim
Grammomys are mostly arboreal rodents occurring in forests, woodlands and thickets throughout sub‐Saharan Africa. We investigated whether the divergence events within the genus follow the existing evolutionary scenario for the development of African forests since the late Miocene.
Location
Sub‐Saharan African forests and woodlands.
Methods
We inferred the molecular phylogeny of Grammomys using Bayesian and maximum likelihood methods and DNA sequences of 351 specimens collected from across the distribution of the genus. We mapped the genetic diversity, estimated the divergence times by a relaxed clock model and compared evolution of the genus with forest history.
Results
Phylogenetic analysis confirms the monophyly of Grammomys and reveals five main Grammomys lineages with mainly parapatric distributions: (1) the poensis group in Guineo‐Congolese forests; (2) the selousi group with a distribution mainly in coastal forests of southern and eastern Africa; (3) the dolichurus group restricted to the easternmost part of South Africa; (4) the macmillani group in the northern part of eastern and Central Africa with one isolated species in Guinean forests; and (5) the surdaster group, widely distributed in eastern Africa south of the equator. Every group contains well supported sublineages suggesting the existence of undescribed species. The earliest split within the genus (groups 1 vs. 2–5) occurred in the late Miocene and coincides with the formation of the Rift Valley which resulted in the east–west division of the initially pan‐African forest. The subsequent separation between groups (2 vs. 3–5) also dates to the end of the Miocene and suggests the split between Grammomys from coastal to upland forests in eastern Africa followed by a single dispersal event into western Africa during the Pleistocene.
Conclusions
The evolutionary history of the genus Grammomys closely reflects the accepted scenario of major historical changes in the distribution of tropical African forests since the late Miocene.
This paper gives a historical overview of the African rain forest from its origins, towards, the end of the Cretaceous period. The areas around the Gulf of Guinea, in particular from Ivory Coast to Nigeria and especially Cameroon, Gabon and Congo, appear to have been already occupied at this time by wet tropical forest formations mainly composed of Angiosperms. In the course of the Tertiary period the combined effect of the equator being situated further north than now and the development of the Antarctic ice cap favoured the development of wet tropical conditions over a large part of North Africa. Towards the end of the Tertiary, the equator reached its present position and the northern hemisphere ice caps appeared, and these phenomena resulted in the disappearance of the forest formations spread across the north of Africa, and the concentration of these formations near the equatorial zone around the Gulf of Guinea and in the Congo-Zaire basin. From 800 000 years ago onwards the marked glacial variations at middle and high latitudes in both hemispheres, lowered temperatures in equatorial areas and brought arid climates at times of maximum glacial extension. -Author
Biodiversity hotspots, which harbor more endemic species than elsewhere on Earth, are increasingly threatened. There is a need to accelerate collection efforts in these regions before threatened or endangered species become extinct. The diverse geographical, ecological, genetic, morphological, and behavioral data generated from the on-site collection of an individual specimen are useful for many scientific purposes. However, traditional methods for specimen preparation in the field do not permit researchers to retrieve neuroanatomical data, disregarding potentially useful data for increasing our understanding of brain diversity. These data have helped clarify brain evolution, deciphered relationships between structure and function, and revealed constraints and selective pressures that provide context about the evolution of complex behavior. Here, we report our field-testing of two commonly used laboratory-based techniques for brain preservation while on a collecting expedition in the Congo Basin and Albertine Rift, two poorly known regions associated with the Eastern Afromontane biodiversity hotspot. First, we found that transcardial perfusion fixation and long-term brain storage, conducted in remote field conditions with no access to cold storage laboratory equipment, had no observable impact on cytoarchitectural features of lizard brain tissue when compared to lizard brain tissue processed under laboratory conditions. Second, field-perfused brain tissue subjected to prolonged post-fixation remained readily compatible with subsequent immunohistochemical detection of neural antigens, with immunostaining that was comparable to that of laboratory-perfused brain tissue. Third, immersion-fixation of lizard brains, prepared under identical environmental conditions, was readily compatible with subsequent iodine-enhanced X-ray microcomputed tomography, which facilitated the non-destructive imaging of the intact brain within its skull. In summary, we have validated multiple approaches to preserving intact lizard brains in remote field conditions with limited access to supplies and a high degree of environmental exposure. This protocol should serve as a malleable framework for researchers attempting to rescue perishable and irreplaceable morphological and molecular data from regions of disappearing biodiversity. Our approach can be harnessed to extend the numbers of species being actively studied by the neuroscience community, by reducing some of the difficulty associated with acquiring brains of animal species that are not readily available in captivity.
Comparative phylogeography allow us to understand how shared historical circumstances have shaped the formation of lineages, by examining a broad spectrum of co-distributed populations of different taxa. However, these types of studies are scarce in the Neotropics, a region that is characterized by high diversity, complex geology, and poorly understood biogeography. Here, we investigate the diversification patterns of five lineages of amphibians and reptiles, co-distributed across the Choco and Andes ecoregions in northwestern Ecuador. Mitochondrial DNA and occurrence records were used to determine the degree of geographic genetic divergence within species. Our results highlight congruent patterns of parapatric speciation and common geographical barriers for distantly related taxa. These comparisons indicate similar biological and demographic characteristics for the included clades, and reveal the existence of two new species of Pristimantis previously subsumed under P. walkeri, which we describe herein. Our data supports the hypothesis that widely distributed Chocoan taxa may generally experience their greatest opportunities for isolation and parapatric speciation across thermal elevational gradients. Finally, our study provides critical information to predict which unstudied lineages may harbor cryptic diversity, and how geology and climate are likely to have shaped their evolutionary history.
Modern tropical forests harbor an enormous diversity of squamates, but fossilization in such environments is uncommon and little is known about tropical lizard assemblages of the Mesozoic. We report the oldest lizard assemblage preserved in amber, providing insight into the poorly preserved but potentially diverse mid-Cretaceous paleotropics. Twelve specimens from the Albian-Cenomanian boundary of Myanmar (99 Ma) preserve fine details of soft tissue and osteology, and high-resolution x-ray computed tomography permits detailed comparisons to extant and extinct lizards. The extraordinary preservation allows several specimens to be confidently assigned to groups including stem Gekkota and stem Chamaleonidae. Other taxa are assignable to crown clades on the basis of similar traits. The detailed preservation of osteological and soft tissue characters in these specimens may facilitate their precise phylogenetic placement, making them useful calibration points for molecular divergence time estimates and potential keys for resolving conflicts in higher-order squamate relationships.
Upper Cretaceous deposits at Ukhaa Tolgod and adjacent localities in the Mongolian Gobi Desert have yielded a large number of superbly preserved lizard specimens, including representatives of several new taxa (described in this paper) and important supplementary material of several previously poorly known taxa. Study of these specimens gives important insight into the taxonomic diversity and systematics of the Late Cretaceous lizard fauna of the Gobi Desert. A preliminary survey indicates that the lizard assemblage from Ukhaa Tolgod and adjacent localities consists of some 30 species in four higher groups (Iguania, Gekkota, Scincomorpha, and Anguimorpha). The iguanians are documented by eight species, including three species newly recognized in this paper. The Scincomorpha are the most diverse group, represented by as many as 14 species including three new and II previously known species. The Anguimorpha are nearly as diverse as the Iguania, while the Gekkota is the least diverse group with a single species documented in the assemblage. The scincomorphs include forms that are highly specialized for burrowing life-styles, interpreted from their cranial morphology as possibly analogous to extant species. The anguimorphs include phylogenetically important basal members of several major anguimorph clades. The paleoecological significance of these lizards cannot be overlooked. According to tooth morphology, most lizards are predatory in terms of habit, while true herbivorous species are rare. Most specimens are preserved as skulls articulated with mandibles, but virtually complete skeletons in situ are quite common. Delicate parts of the skull, such as the braincase and ear ossicles, are undistorted and the surfaces of the bones show no sign of sand abrasion. These observations indicate not only relatively quick burial but also burial under relatively mesic climatic conditions with low-energy water involved during the taphonomic process.
The Eastern Afromontane biodiversity hotspot (EABH) has the highest concentration of biodiversity in tropical Africa, yet few studies have investigated recent historical diversification processes in EABH lineages. Herein, we analyze restriction-site associated DNA-sequences (RAD-Seq) to study recent historical processes in co-distributed mouse (Hylo-myscus) and shrew (Sylvisorex) species complexes, with an aim to better determine how historical paleoenvironmental processes might have contributed to the EABH's high diversity. We analyzed complete SNP matrices of > 50,000 RAD loci to delineate populations, reconstruct the history of isolation and admixture, and discover geographic patterns of genetic partitioning. These analyses demonstrate that persistently unsuitable habitat may have isolated multiple populations distributed across montane habitat islands in the Itombwe Massif and Albertine Rift to the west as well as Mt Elgon and Kenyan Highlands to the east. We detected low genetic diversity in Kenyan Highland populations of both genera, consistent with smaller historical population sizes in this region. We additionally tested predictions that Albertine Rift populations are older and more persistently isolated compared to the Kenyan Highlands. Phylogenetic analyses support greater historical isolation among Albertine Rift populations of both shrews and mice compared to the Kenyan Highlands and suggest that there are genetically isolated populations from both focal genera in the Itombwe Massif, Democratic Republic of Congo. The Albertine Rift ecoregion has the highest mammalian tropical forest species richness per unit area on earth. Our results clearly support accelerating efforts to conserve this diversity.
Timing and magnitude of surface uplift are key to understanding the impact of crustal deformation and topographic growth on atmospheric circulation, environmental conditions, and surface processes. Uplift of the East African Plateau is linked to mantle processes, but paleoaltimetry data are too scarce to constrain plateau evolution and subsequent vertical motions associated with rifting. Here, we assess the paleotopographic implications of a beaked whale fossil (Ziphiidae) from the Turkana region of Kenya found 740 km inland from the present-day coastline of the Indian Ocean at an elevation of 620 m. The specimen is similar to 17 My old and represents the oldest derived beaked whale known, consistent with molecular estimates of the emergence of modern straptoothed whales (Mesoplodon). The whale traveled from the Indian Ocean inland along an eastward-directed drainage system controlled by the Cretaceous Anza Graben and was stranded slightly above sea level. Surface uplift from near sea level coincides with paleoclimatic change from a humid environment to highly variable and much drier conditions, which altered biotic communities and drove evolution in east Africa, including that of primates.
Significance
An enigmatic fossil representing the deep-diving, open-ocean whale family Ziphiidae found 740 km inland and at 620 m elevation in West Turkana, Kenya was rediscovered after it went missing for more than 30 years. This stranded whale fossil provides the first constraint on the initiation of east African uplift from near sea level at 17 Ma, limiting the timing and initial elevation of environmental change indicated by geodynamic and climatic modeling, paleosols, isotopes, paleobotany, and the mammalian fossil record. At 17 Ma, elevation was low, rainfall was high, vegetation was forested, and mammalian communities contained immigrants and native African species, including diverse primates. Uplift resulted in increasing aridity and open habitats that drove human evolution.
The Central African house snake Boaedon olivaceus has a large distribution from the forests of West Africa to Mabira Forest in Uganda. We sequenced two mitochondrial (cyt b and ND4) and two nuclear (c-mos and RAG1) genes from several populations of B. olivaceus in Central Africa and recovered two highly divergent lineages (Congo Basin and Albertine Rift) attributable to this species. Dating analyses with BEAST suggest the two lineages last shared a common ancestor during the mid-Miocene approximately 12 million years ago, and data from RAG1 showed consistent differences in two amino acids for topotypic Congo Basin B. olivaceus compared to the Albertine Rift lineage and all other examined species of Boaedon. Based on these striking molecular differences and significant differences in ventral scale counts and the number of supralabials contacting the eye, we describe the Albertine Rift lineage as a new species. The recognition of this new species bolsters the importance of the Albertine Rift as an important region for endemism and conservation in continental Africa. Based on the results of our phylogenetic analyses, the poorly known taxon Lycodonomorphus subtaeniatus upembae is elevated to full species status and transferred to the genus Boaedon. http://zoobank.org/urn:lsid:zoobank.org:pub:D0C0E5B5-DBE9-4D21-B5FE-86221DDF60BA
Describing biological diversity is a challenging endeavour, especially for the small, cryptic animals that make up the meiofauna. The field of DNA taxonomy, i.e., the use of DNA to delineate species boundaries, is rapidly growing and changing; herein we review the recent advances in the acquisition of DNA sequence data and the analytical tools for DNA-based species delimitation, with a focus on applications to the meiofauna. After providing general guidelines on the data collection and analysis steps (sampling design, sequencing, phasing of nuclear markers, and sequence alignment), we explain the rationale and usage of several widely used or promising methods developed for delineating species from single-locus data sets (distance-based DNA barcoding, automated barcode gap discovery, K/θ, generalized mixed Yule–coalescent models, Poisson tree process model, and haplowebs). As it is increasingly recognised that several loci are required to delineate species accurately, we then briefly outline multilocus species delimitation approaches (Structure, Structurama, Bayesian phylogenetics & phylogeography, SpedeSTEM, O’Meara’s heuristic search, and several newly published Bayesian approaches based on the multispecies coalescent).
Two new species of chameleons from the genera Rhampholeon and Kinyongia are described from an isolated montane forest remnant situated toward the southern end of the Albertine Rift bordering Lake Tanganyika. The closest known localities of species from these genera are 200km and 400km to the north respectively, separated by large intervening tracts of lowland savannah and Brachystegia (Miombo) woodland - habitats not normally inhabited by species of these genera. Rhampholeon hattinghi sp. nov. and Kinyongia mulyai sp. nov. bear superficial resemblances to previously described species (Rh. boulengeri Steindachner and K. adolfifriderici (Sternfeld)). Rhampholeon hattinghi sp. nov. has a relatively smooth supra-orbital ridge, deep axillary but absent inguinal mite pockets, prominent white spots on the base of the tail and a uniquely derived hemipenal morphology with billowing parasulcal evaginations. Like K. adolfifriderici, Kinyongia mulyai sp. nov. is devoid of a rostral appendage but differs in having a longer and narrower head, a higher upper labial scale count and by the absence of a dorsal crest in the male. To place these new chameleons within the context of their respective genera, Bayesian and maximum likelihood phylogenetic analyses were carried out utilising two mitochondrial (ND2 and 16S) and one nuclear marker (RAG1). Both chameleons were found to have morphological features that distinguish them from other congeners. Based on phylogenetic analysis they are clearly separate evolutionary lineages and are described as new species.
Approximately one-third of the Earth's vegetative cover comprises savannas, grasslands, and other grass-dominated ecosystems. Paleobotanical, paleofaunal, and stable carbon isotope records suggest five major phases in the origin of grass-dominated ecosystems: (1) the late Maastrichtian (or Paleocene) origin of Poaceae; (2) the opening of Paleocene and Eocene forested environments in the early to middle Tertiary; (3) an increase in the abundance of C3 grasses during the middle Tertiary; (4) the origin of C4 grasses in the middle Miocene; and (5) the spread of C4 grass-dominated ecosystems at the expense of C3 vegetation in the late Miocene. Grasses are known from all continents except Antarctica between the early Paleocene and middle Eocene. Herbivore morphology indicative of grazing, and therefore suggestive of grass-dominated ecosystems, appears in South America by the Eocene-Oligocene boundary, prior to the occurrence of grazing morphology elsewhere, and persists throughout the Cenozoic. Clear vertebrate and paleobotanical evidence of widespread grass-dominated ecosystems in northern continents does not occur until the early to middle Miocene. C4 grasses are present from approximately 15 Ma and undergo a dramatic expansion in the lower latitudes of North America, South America, East Africa, and Pakistan between 9 and 4 Ma. The expansion may have taken place in a shorter interval in some regions. C4 grasses are characteristic of seasonal, arid, and warm environments and are more tolerant of lower atmospheric CO2 (< 400 ppmv) than C3 plants. C4 grass distribution, therefore, is climatically controlled. The late Miocene spread of C4 grasses possibly involved a decrease in atmospheric CO2 and heralded the establishment of modern seasonality and rainfall patterns.
The Great Lakes of East Africa are collectively the earth's most remarkable and species-rich freshwater feature. Intrinsic biological factors and extrinsic ecological opportunities allowed much of the lakes' spectacular biological diversity to evolve through evolutionary (often adaptive) radiation and ex-plosive speciation. Beyond evolutionary patterns and processes that led to this remarkable biodiversity and its astonishing morphological disparity, we highlight ecosystem functioning and complex biotic interactions such as co-evolution. Comparative biogeographic patterns for vertebrates and inverte-brates are discussed, as are patterns of diversity and disparity through the late Cenozoic. We demonstrate that the African Great Lakes, because of excellent fossil archives, are a phenomenal setting to integrate micro-and macroevolution. Unfortunately, these amazing ecosystems are also subject to various anthropogenic stressors at global and regional scales, which have already impacted their stability and threaten part of their extraordinary bio-diversity with extinction.
Compared with other African apes, eastern gorillas (Gorilla beringei) have been little studied genetically. We used analysis of autosomal DNA genotypes obtained from non-invasively collected faecal samples to estimate the evolutionary histories of the two extant mountain gorilla populations and the closely related eastern lowland gorillas. Our results suggest that eastern lowland gorillas and mountain gorillas split beginning some 10 000 years ago, followed 5000 years ago by the split of the two mountain gorilla populations of Bwindi Impenetrable National Park and the Virungas Massif. All three populations have decreased in effective population size, with particularly substantial 10-fold decreases for the mountain gorillas. These dynamics probably reflect responses to habitat changes resulting from climate fluctuations over the past 20 000 years as well as increasing human influence in this densely populated region in the last several thousand years.
Eastern African rain forests are remarkable in their high level of endemism. Miocene uplift of the central African plateau separated these montane and coastal forests from the main Guineo-Congolian forest of west and central Africa. Since then, stable Indian Ocean temperatures maintained a region of high rainfall throughout Pleistocene droughts that devastated forest elsewhere on the continent. Relics of the former Pan-African rain forest survived here, the study of which provides a unique insight into tropical evolutionary processes. This book brings together research on the animals, plants and geography of this intriguing residual forest, and highlights the need for effective management practices to conserve its exceptional biodiversity in the face of increasing pressure for land for cultivation.
The recently-developed statistical method known as the "bootstrap" can be used to place confidence intervals on phylogenies. It involves resampling points from one's own data, with replacement, to create a series of bootstrap samples of the same size as the original data. Each of these is analyzed, and the variation among the resulting estimates taken to indicate the size of the error involved in making estimates from the original data. In the case of phylogenies, it is argued that the proper method of resampling is to keep all of the original species while sampling characters with replacement, under the assumption that the characters have been independently drawn by the systematist and have evolved independently. Majority-rule consensus trees can be used to construct a phylogeny showing all of the inferred monophyletic groups that occurred in a majority of the bootstrap samples. If a group shows up 95% of the time or more, the evidence for it is taken to be statistically significant. Existing computer programs can be used to analyze different bootstrap samples by using weights on the characters, the weight of a character being how many times it was drawn in bootstrap sampling. When all characters are perfectly compatible, as envisioned by Hennig, bootstrap sampling becomes unnecessary; the bootstrap method would show significant evidence for a group if it is defined by three or more characters.
The prevailing explanation for the observed distributional patterns and areas of endemism of tropical forest organisms is the Pleistocene refuge hypothesis, which proposes that wide-ranging ancestral taxa were isolated into forest refuges during certain glacial periods, and that this isolation provided them with the opportunity to speciate. John Endler has recently argued that two predictions of the refuge hypothesis-that contact zones between vicars should be between refuges and that contact zones of rapidly reproducing butterflies should be wider than those of more slowly reproducing birds-are not borne out by the evidence. Endler therefore rejects the refuge hypothesis. We show that the data available are far too imprecise to permit any conclusions regarding contact zone widths and that, according to our reanalysis of the African bird data used by Endler, all the contact zones between vicars do indeed occur between refuges, exactly where they are expected. Additional strong support for the refuge hypothesis comes from the existence of many taxa endemic to the particular forest areas which have been postulated as refuges and from fragmented taxa which are still allopatric, never having come into secondary contact.
Climate change is likely to shift the distributions of ecosystems worldwide. Most assessments of climate change are primarily species-focused and do not directly estimate how entire ecosystems may change. Using an ecosystem-based modelling approach, we provide a region-wide climate change vulnerability assessment of the seven major ecosystems across Africa's Albertine Rift. The Albertine Rift is a global biodiversity hotspot, containing more endemic vertebrates than anywhere else in Africa. We used Maxent to estimate each ecosystem's extent using current climate data, then we projected the potential distribution of each ecosystem for 2050 and 2070. We found that suitable conditions for most ecosystems are predicted to contract rapidly in extent and shift upwards in altitude. High-altitude ecosystems and the endemic species they support are at immediate risk, owing to rapid predicted shrinkage in their suitable extent. Only the Combretum-grasslands savannah ecosystem is predicted to expand, with suitable conditions increasing by 32% in area by 2050. The extent and structure of boundary zones between the Rift's ecosystems may change significantly through time, due to the contractions and shifts of the environmental conditions for existing ecosystem distributions. By 2070, 44% of the region could be climatically unsuitable for the current ecosystems. Conservation planning across the Rift will need to account for these ecosystem shifts and rapidly changing boundary zones to ensure the long-term persistence of the many endemic species. Beyond the Albertine Rift, this ecosystem-based modelling technique can be adapted to any terrestrial region, providing critical information for conservation vulnerability assessments.
Significance
Despite its widespread application to the species delimitation problem, our study demonstrates that what the multispecies coalescent actually delimits is structure. The current implementations of species delimitation under the multispecies coalescent do not provide any way for distinguishing between structure due to population-level processes and that due to species boundaries. The overinflation of species due to the misidentification of general genetic structure for species boundaries has profound implications for our understanding of the generation and dynamics of biodiversity, because any ecological or evolutionary studies that rely on species as their fundamental units will be impacted, as well as the very existence of this biodiversity, because conservation planning is undermined due to isolated populations incorrectly being treated as distinct species.
The endangered warbler Bradypterus graueri is endemic to the Albertine Rift, where it is restricted to montane swamps above 1900 m across the region. We studied genetic structure among six populations sampled across the species' distribution in northern Burundi, Rwanda, Uganda and the eastern Democratic Republic of Congo. A total of 2117 base pairs of mitochondrial data were sequenced. Phylogenetic analyses and network reconstruction of B. graueri haplotypes recovered three clades with a defined geographical pattern: clade 1, Virunga Volcanoes and Kigezi Highlands; clade 2, Rugege Highlands; and clade 3, Kahuzi-Biega Highlands; clades 2 and 3 are sisters to each other. Both landscape dynamics and historical climate are likely to have played a role in the diversification of this species. The divergence between clade 1 and clades 2 and 3 (168.5 ka, 95% HPD 108.5, 244.4) coincides with a prolonged period of aridity in tropical Africa between 130 and 270 ka. Similarly, the divergence between clades 2 and 3 (99.4 ka, 95% HPD 55.4, 153.8) corresponds with a period of aridity just prior to 94 ka. Populations sampled from the eastern arm of the central Albertine Rift (Kigezi and Rugege Highlands) show a coincident increase in effective population size after the Last Glacial Maximum at c. 15 ka, whereas those sampled from Kahuzi-Biega on the western arm of the rift do not. Despite the perceived higher vagility of bird species relative to other vertebrates, the degree of phylogeographical structure among populations of B. graueri is similar to that reported for small mammals (Hylomyscus vulcanorum, Lophuromys woosnami, Sylvisorex vulcanorum) and a frog Hyperolius castaneus sampled across the central Albertine Rift. Collectively our results suggest that climate dynamics associated with late Pleistocene cycles had a significant influence on driving the population genetic structure and associated levels of genetic diversity in B. graueri and other small terrestrial vertebrates. Our results have implications for the conservation of B. graueri and other endemics to the Albertine Rift, particularly in the context of other phylogegeographical studies centred on this biodiversity hotspot.
The African river frog genus Amietia is found near rivers and other lentic water sources throughout central, eastern, and southern Africa. Because the genus includes multiple morphologically conservative species, taxonomic studies of river frogs have been relatively limited. We sampled 79 individuals of Amietia from multiple localities in and near the Albertine Rift (AR) of Burundi, Democratic Republic of the Congo, and Uganda. We utilized single-gene (16S) and concatenated (12S, 16S, cyt b and RAG1) gene-tree analyses and coalescent species-tree analyses to construct phylogenetic trees. Two divergence dating approaches were used in BEAST, including secondary calibration points with 12S, 16S, cyt b and RAG1, and a molecular clock with the 12S, 16S, and cyt b genes. All analyses recovered Amietia as monophyletic with strong support, and revealed several well-supported cryptic lineages, which is consistent with other recent phylogeography studies of AR amphibians. Dating estimates were similar, and Amietia diversification is coincident with global cooling and aridification events in the Miocene and Pliocene, respectively. Our results suggest additional taxonomic work is needed to describe multiple new species of AR Amietia, some of which have limited geographic distributions that are likely to be of conservation concern.
The development of savanna-type grasslands is a relatively recent phenomena in East Africa. The stable carbon isotopic composition of paleosol carbonates from fossil localities in East Africa show that C 4 vegetation was present by about 8-9 Ma but made up only a relatively small proportion of the total biomass. Although the proportion of C 4 vegetation increased in the Pliocene and Pleistocene there is no evidence for the development of virtually pure C 4 grasslands, as is characterized by tropical grasslands today, until Middle Pleistocene times. This has important implications concerning the evolution of mammals in Africa, including hominids.
Tropical forests provide critical ecosystem services worldwide. Nonetheless, ongoing agricultural expansion, timber extraction, and mining continue to jeopardize important forest resources. In addition, many tropical forests reside in countries that have experienced violent conflict in recent decades, posing an additional, yet poorly understood threat. Conflict may decrease or increase deforestation depending on the relationship between conflict and other causes of land use change, such as mining expansion or protected area establishment. The Democratic Republic of Congo (DRC), home of the second largest tropical forest in the world, has experienced 20. years of violent conflict, resulting in the death of over 100,000 combatants and up to 5 million civilians. Expanding mining concessions also threaten the DRC's forest, even though nearly 12% of it is under some form of protection. In this study, we used spatially-explicit data on conflict, mining, and protected areas, along with a host of control variables, to estimate the impacts of these factors on forest cover loss from 1990 to 2010. Through a panel instrumental variables approach we found that: i) conflict increased forest cover loss, ii) mining concessions increased forest cover loss, but in times of conflict this impact was lessened, and iii) protected areas reduced forest cover loss, even in high conflict regions. Our results thus suggest that policy interventions designed to reduce violent conflict may have the co-benefit of reducing deforestation, especially in areas with low mining potential. Likewise, protected areas can be effective even in times of war.
There are three main hypotheses regarding African Miocene climates. The most commonly cited one (accordion hypothesis) proposes that the ecoclimatic belts remained fixed in position but fluctuated in latitudinal width. The second (graticule shift hypothesis) is that the position of the ecoclimatic belts changed so that the equator was located further north in Africa than it is now. The third is that there are elements of truth in both the above. Evidence from the Kisegi Formation in Western Uganda provides support for the second hypothesis. -Author
The Rwenzori Mountains in Africa represent an extremely uplifted basement fault block at the eastern edge of the western branch of the East African Rift system, a large-scale rift system controlled by extensional stresses. The rugged alpine topography reaches an altitude of up to 5109 m, and the highest parts are ice-covered. Glacial landforms and moraines proof repeated more extensive glaciations during the last glacial cycles. In order to elucidate magnitudes and the varying role of erosional processes in shaping the relief of the Rwenzori Mountains over the past 2 mill. years, we performed numerical simulations with the landscape evolution programme ULTIMA THULE. It is controlled by a climate driver with temperature as a master variable as well as changing precipitation and evapotranspiration over time. The morphological processes considered are fluvial erosion, hillslope diffusion, and glacial abrasion, and the latter controlled by the simulated glaciation of the landscape. We provide three sets of model runs: the first one starting from the present-day topography and running for approx. 800 ka, the second one extending the modelling period to 2 Ma, and the third one starting from a peneplain and evolving for 2 Ma. Our results provide constraints on the temperature history of the Rwenzori Mountains, the interplay of morphological degradation and tectonic uplift, and a time frame for the formation of the mountain chain from a peneplain to the present relief. The modelled landscape evolves from a peneplain 2 Ma ago to a Rwenzori-type mountain range, when the fairly strong average rock uplift of 1-2 mm year−1 is compensated by a strong fluvial erosion component. The rock uplift rate is needed to obtain elevations above the equilibrium line altitude around 500 ka BP and results in surface uplift over time. Around that time, a periodic ice cap appears in the models, and glacial abrasion then limits the height of the Rwenzori Mountains to its present elevation.
This paper offers a review and reassessment of the biogeography of the Afromontane region. Much of the montane vegetation of Africa, expecially in the sourthern part of its distribution (the southern Afromontane region) is characterized by a mosaic of forest `islands' in a `sea' of grassland, with or without heathland elements. Controversy has arisen as to the origin of these grasslands and the view has emerged, based on a variety of phytogeographical, zoogeographical, ecological, pedological and historical evidence, that the grasslands element has been derived, or at least markeldy extended, in the recent past by forest clearance through human agency. An alternative hypothesis holds that the grassland is a much older component of the Afromontage landscape. The paper assesses these two opposing viewpoints in the light of published palaeoecological and biogeographical evidence not previously brought to bear on the problem of Afromontane grassland origins in general. The physical environment and vegetation of the southern Afromontane region is reviewed and the suggestions put forward to account for the widespread occurrence of grasslands in the region are presented. The competing hypotheses are then tested against data on plant species richness and diversity from a number of upland areas within the region and against published Quaternary palynological data from the Nyika Plateau, Malawi, the Inyaga Mountains, Zimbabwe and the Winterberg Escarpment area of South Africa. The resulting reassessment offers strong support for the idea that the grasslands have been prominent in the southern Afromontane region since before the permanent occupation of the mountains by people. Environmental changes, especially of the late Quaternary, are suggested as having been important in establishing the vegetation pattern and, while increased magnitude of human impact in recent times is apparent, the so-called `relict' nature of montane forest patches is questionable. It is argued that the southern Afromontane grasslands are themselves relict from a time, around the last glacial maximum, when the climatic conditions were more suited to these formations than to forest.
We investigated the land snail fauna of Nyungwe Forest National Park in south-western Rwanda. Fifty plots at altitudes between 1718 and 2573 m were studied. In total, 3461 specimens were collected and were assigned to 102 land snail species. With respect to land snail species, Nyungwe Forest is the richest forest known in Africa. A comparison with other forests in the northern Albertine Rift indicates that land snail species richness in this region is significantly correlated with distance from Pleistocene forest refugia. The high beta diversity in Nyungwe is the result of a high species turnover between sites, which has biogeographical and ecological origins. Nyungwe Forest is situated on the Congo–Nile divide where species of different geographical origin may meet. Moreover, Nyungwe Forest offers a high diversity of habitats because it extends across a wide range of altitudinal zones. Species richness decreased with increasing altitude. It was also correlated with the presence of bare rocks that offer additional microhabitats and shelter. Although the occurrences of different land snail species in Nyungwe Forest were significantly clustered, only a minority of the species could be assigned to a group of species with similar occurrences. The majority of the species respond individualistically to environmental variables. The significant nestedness of the occurrences of the land snail species in Nyungwe was mainly correlated with altitude. © 2015 The Linnean Society of London, Biological Journal of the Linnean Society, 2015, 114, 363–375.