Southern Africa's Great Escarpment as an amphitheater of climate-driven diversification and a buffer against future climate change in bats.

Hosting 1460 plant and 126 vertebrate endemic species, the Great Escarpment (hereafter, Escarpment) forms a semi-circular "amphitheater" of mountains girdling southern Africa from arid west to temperate east. Since arid and temperate biota are usually studied separately, earlier studies overlooked the biogeographical importance of the Escarpment as a whole. Bats disperse more widely than other mammalian taxa, with related species and intraspecific lineages occupying both arid and temperate highlands of the Escarpment, providing an excellent model to address this knowledge gap. We investigated patterns of speciation and micro-endemism from modeled past, present, and future distributions in six clades of southern African bats from three families (Rhinolophidae, Cistugidae, and Vespertilionidae) having different crown ages (Pleistocene to Miocene) and biome affiliations (temperate to arid). We estimated mtDNA relaxed clock dates of key divergence events across the six clades in relation both to biogeographical features and patterns of phenotypic variation in crania, bacula and echolocation calls. In horseshoe bats (Rhinolophidae), both the western and eastern "arms" of the Escarpment have facilitated dispersals from the Afrotropics into southern Africa. Pleistocene and pre-Pleistocene "species pumps" and temperate refugia explained observed patterns of speciation, intraspecific divergence and, in two cases, mtDNA introgression. The Maloti-Drakensberg is a center of micro-endemism for bats, housing three newly described or undescribed species. Vicariance across biogeographic barriers gave rise to 29 micro-endemic species and intraspecific lineages whose distributions were congruent with those identified in other phytogeographic and zoogeographic studies. Although Köppen-Geiger climate models predict a widespread replacement of current temperate ecosystems in southern Africa by tropical or arid ecosystems by 2070-2100, future climate Maxent models for 13 bat species (all but one of those analyzed above) showed minimal range changes in temperate species from the eastern Escarpment by 2070, possibly due to the buffering effect of mountains to climate change.

Complex patterns of gene flow and convergence in the evolutionary history of the spiral-horned antelopes (Tragelaphini).

The Tragelaphini, also known as spiral-horned antelope, is a phenotypically diverse mammalian tribe comprising a single genus, Tragelaphus. The evolutionary history of this tribe has attracted the attention of taxonomists and molecular geneticists for decades because its diversity is characterised by conflicts between morphological and molecular data as well as between mitochondrial, nuclear and chromosomal DNA. These inconsistencies point to a complex history of ecological diversification, coupled by either phenotypic convergence or introgression. Therefore, to unravel the phylogenetic relationships among spiral-horned antelopes, and to further investigate the role of divergence and gene flow in trait evolution, we sequenced genomes for all nine accepted species of the genus Tragelaphus, including a genome each for the highly divergent bushbuck lineages (T. s. scriptus and T. s. sylvaticus). We successfully reconstructed the Tragelaphus species tree, providing genome-level support for the early Pliocene divergence and monophyly of the nyala (T. angasii) and lesser kudu (T. imberbis), the monophyly of the two eland species (T. oryx and T. derbianus) and, importantly, the monophyly of kéwel (T. s. scriptus) and imbabala (T. s. sylvaticus) bushbuck. We found strong evidence for gene flow in at least four of eight nodes on the species tree. Among the six phenotypic traits assessed here, only habitat type mapped onto the species tree without homoplasy, showing that trait evolution was the result of complex patterns of divergence, introgression and convergent evolution.

Tipping points induced by palaeo-human impacts can explain presence of savannah in Malagasy and global systems where forest is expected.

Models aimed at understanding C4-savannah distribution for Australia, Africa and South America support transition to forest at high mean annual precipitation (MAP), and savannah grasslands of Madagascar have recently been reported to be similarly limited. Yet, when savannah/grassland presence data are plotted against MAP for the various ecosystems across the Malagasy Central Highlands, the relationship does not hold. Furthermore, it does not always hold in other sites on other continents. Instead, in high-rainfall savannahs, palaeo-human impacts appear to have selected a fire-adapted habitat, creating tipping points that allow savannah persistence despite high rainfall, suppressing forest return. We conducted the largest systematic literature review to date for global evidence of palaeo-human impacts in savannahs, and conclude that impacts are widespread and should be incorporated into models aimed at understanding savannah persistence at elevated precipitation, particularly as more palaeodata emerges. Building on existing studies, we refine the MAP savannah relationship at higher MAP. Palaeoanthropogenic impact can help explain inconsistencies in the savannah/forest boundary at higher MAP, and points to a key role for palaeoecology in understanding systems. Including these effects presents a crucial change to our understanding of factors determining global savannah distribution, supporting a human hand in much of their formation.

Interspecific Gene Flow and the Evolution of Specialization in Black and White Rhinoceros.

Africa's black (Diceros bicornis) and white (Ceratotherium simum) rhinoceros are closely related sister-taxa that evolved highly divergent obligate browsing and grazing feeding strategies. Although their precursor species Diceros praecox and Ceratotherium mauritanicum appear in the fossil record ∼5.2 Ma, by 4 Ma both were still mixed feeders, and were even spatiotemporally sympatric at several Pliocene sites in what is today Africa's Rift Valley. Here, we ask whether or not D. praecox and C. mauritanicum were reproductively isolated when they came into Pliocene secondary contact. We sequenced and de novo assembled the first annotated black rhinoceros reference genome and compared it with available genomes of other black and white rhinoceros. We show that ancestral gene flow between D. praecox and C. mauritanicum ceased sometime between 3.3 and 4.1 Ma, despite conventional methods for the detection of gene flow from whole genome data returning false positive signatures of recent interspecific migration due to incomplete lineage sorting. We propose that ongoing Pliocene genetic exchange, for up to 2 My after initial divergence, could have potentially hindered the development of obligate feeding strategies until both species were fully reproductively isolated, but that the more severe and shifting paleoclimate of the early Pleistocene was likely the ultimate driver of ecological specialization in African rhinoceros.

Rapid ecological specialization despite constant population sizes.

BACKGROUND: The bushbuck, Tragelaphus scriptus, is a widespread and ecologically diverse ungulate species complex within the spiral-horned antelopes. This species was recently found to consist of two genetically divergent but monophyletic lineages, which are paraphyletic at mitochondrial (mt)DNA owing to an ancient interspecific hybridization event. The Scriptus lineage (T. s. scriptus) inhabits the north-western half of the African continent while Sylvaticus (T. s. sylvaticus) is found in the south-eastern half. Here we test hypotheses of historical demography and adaptation in bushbuck using a higher-resolution framework, with four nuclear (MGF, PRKCI, SPTBN, and THY) and three new mitochondrial markers (cytochrome b, 12S rRNA, and 16S rRNA). METHODS: Genealogies were reconstructed for the mitochondrial and nuclear data sets, with the latter dated using fossil calibration points. We also inferred the demographic history of Scriptus and Sylvaticus using coalescent-based methods. To obtain an overview of the origins and ancestral colonisation routes of ancestral bushbuck sequences across geographic space, we conducted discrete Bayesian phylogeographic and statistical dispersal-vicariance analyses on our nuclear DNA data set. RESULTS: Both nuclear DNA and mtDNA support previous findings of two genetically divergent Sylvaticus and Scriptus lineages. The three mtDNA loci confirmed 15 of the previously defined haplogroups, including those with convergent phenotypes. However, the nuclear tree showed less phylogenetic resolution at the more derived parts of the genealogy, possibly due to incomplete lineage sorting of the slower evolving nuclear genome. The only exception to this was the montane Menelik's bushbuck (Sylvaticus) of the Ethiopian highlands, which formed a monophyletic group at three of four nuclear DNA loci. We dated the coalescence of the two lineages to a common ancestor ∼2.54 million years ago. Both marker sets revealed similar demographic histories of constant population size over time. We show that the bushbuck likely originated in East Africa, with Scriptus dispersing to colonise suitable habitats west of the African Rift and Sylvaticus radiating from east of the Rift into southern Africa via a series of mainly vicariance events. DISCUSSION: Despite lower levels of genetic structure at nuclear loci, we confirmed the independent evolution of the Menelik's bushbuck relative to the phenotypically similar montane bushbuck in East Africa, adding further weight to previous suggestions of convergent evolution within the bushbuck complex. Perhaps the most surprising result of our analysis was that both Scriptus and Sylvaticus populations remained relatively constant throughout the Pleistocene, which is remarkable given that this was a period of major climatic and tectonic change in Africa, and responsible for driving the evolution of much of the continent's extant large mammalian diversity.

Phylogeography and population genetics of the endemic Malagasy bat, Macronycteris commersoni s.s. (Chiroptera: Hipposideridae).

Macronycteris commersoni (Hipposideridae), a bat species endemic to Madagascar, is widespread across the island and utilizes a range of habitat types including open woodland, degraded habitats, and forested areas from sea level to 1,325 m. Despite being widely distributed, there is evidence that M. commersoni exhibits morphological and bioacoustic variation across its geographical range. We investigated the fine-scale phylogeographic structure of populations in the western half of the island using extensive spatial sampling and sequence data from two mitochondrial DNA regions. Our results indicated several lineages within M. commersoni. Individuals collected from northern Madagascar formed a single monophyletic clade (clade C). A second clade (clade B) included individuals collected from the south-western portion of the island. This second clade displayed more phylogeographical partitioning with differences in mtDNA haplotypes frequency detected between populations collected in different bioclimatic regions. Lineage dispersal, genetic divergence, and timing of expansion events of M. commersoni were probably associated with Pleistocene climate fluctuations. Our data suggest that the northern and the central western regions of Madagascar may have acted as refugia for this species during periods of cooler and drier climate conditions associated with the Pleistocene.

Cryptic diversity in Hipposideros commersoni sensu stricto (Chiroptera: Hipposideridae) in the western portion of Madagascar.

BACKGROUND: The Commerson's leaf-nosed bat, Hipposideros commersoni sensu stricto, is endemic to Madagascar and is relatively common in the western portion of the island, where it is found in areas, including forested zones, from sea level to 1325 m. A previous study on morphological patterns of geographic variation within the species highlighted the presence of two distinct morphotypes; larger individuals in the north portion of the island and smaller individuals in the south. The main aim of this study was to use a combination of craniodental morphology and molecular data (mitochondrial and nuclear) to test previous hypotheses based on morphology and clarify the evolutionary history of the species group. METHODS: We sequenced mitochondrial and nuclear genes from Hipposideros commersoni obtained from the western portion of Madagascar, and compared them with other African species as outgroups. We analyzed the sequence data using Maximum Likelihood and Bayesian phylogenetic inference. Divergence dates were estimated using Bayesian molecular clock approach. Variation in craniodental variables was also assessed from sequenced individuals. RESULTS: The molecular analyses suggest that H. commersoni is not monophyletic, with strong support for the presence of several independently evolving lineages. Two individuals amongst those sequenced from Isalo (south central) and Itampolo (southwest) form a separate clade (Clade A), distinct from other H. commersoni, and sister to continental African H. vittatus and H. gigas. Within the H. commersoni clade, the molecular data support two geographically distributed clades; one from the south (Clade B) and the other from the north (Clade C), which diverged approximately 3.38 million years ago. Morphometric data were consistent with the molecular analyses, suggesting a north-south break within H. commersoni. However, at some localities, animals from both clades occurred in sympatry and these individuals could not be differentiated based on external and craniodental measurements. CONCLUSIONS: Using a combination of molecular and morphological characters, this study presents evidence of cryptic diversity in H. commersoni on Madagascar. Further fine-scale phylogeographic studies are needed to fully resolve the systematics of H. commersoni. This study highlights the utility of the combined approach in employing both morphological and molecular data to provide insights into the evolutionary history of Malagasy population currently assigned to H. commersoni.

Analysis of patterns of bushmeat consumption reveals extensive exploitation of protected species in eastern Madagascar.

Understanding the patterns of wild meat consumption from tropical forests is important for designing approaches to address this major threat to biodiversity and mitigate potential pathways for transmission of emerging diseases. Bushmeat consumption has been particularly poorly studied in Madagascar, one of the world's hottest biodiversity hotspots. Studying bushmeat consumption is challenging as many species are protected and researchers must consider the incentives faced by informants. Using interviews with 1154 households in 12 communes in eastern Madagascar, as well as local monitoring data, we investigated the importance of socio-economic variables, taste preference and traditional taboos on consumption of 50 wild and domestic species. The majority of meals contain no animal protein. However, respondents consume a wide range of wild species and 95% of respondents have eaten at least one protected species (and nearly 45% have eaten more than 10). The rural/urban divide and wealth are important predictors of bushmeat consumption, but the magnitude and direction of the effect varies between species. Bushmeat species are not preferred and are considered inferior to fish and domestic animals. Taboos have provided protection to some species, particularly the Endangered Indri, but we present evidence that this taboo is rapidly eroding. By considering a variety of potential influences on consumption in a single study we have improved understanding of who is eating bushmeat and why. Evidence that bushmeat species are not generally preferred meats suggest that projects which increase the availability of domestic meat and fish may have success at reducing demand. We also suggest that enforcement of existing wildlife and firearm laws should be a priority, particularly in areas undergoing rapid social change. The issue of hunting as an important threat to biodiversity in Madagascar is only now being fully recognised. Urgent action is required to ensure that heavily hunted species are adequately protected.