Colonial-driven extinction of the blue antelope despite genomic adaptation to low population size.

Low genomic diversity is generally indicative of small population size and is considered detrimental by decreasing long-term adaptability.1,2,3,4,5,6 Moreover, small population size may promote gene flow with congeners and outbreeding depression.7,8,9,10,11,12,13 Here, we examine the connection between habitat availability, effective population size (Ne), and extinction by generating a 40× nuclear genome from the extinct blue antelope (Hippotragus leucophaeus). Historically endemic to the relatively small Cape Floristic Region in southernmost Africa,14,15 populations were thought to have expanded and contracted across glacial-interglacial cycles, tracking suitable habitat.16,17,18 However, we found long-term low Ne, unaffected by glacial cycles, suggesting persistence with low genomic diversity for many millennia prior to extinction in ∼AD 1800. A lack of inbreeding, alongside high levels of genetic purging, suggests adaptation to this long-term low Ne and that human impacts during the colonial era (e.g., hunting and landscape transformation), rather than longer-term ecological processes, were central to its extinction. Phylogenomic analyses uncovered gene flow between roan (H. equinus) and blue antelope, as well as between roan and sable antelope (H. niger), approximately at the time of divergence of blue and sable antelope (∼1.9 Ma). Finally, we identified the LYST and ASIP genes as candidates for the eponymous bluish pelt color of the blue antelope. Our results revise numerous aspects of our understanding of the interplay between genomic diversity and evolutionary history and provide the resources for uncovering the genetic basis of this extinct species' unique traits.

Plio-Pleistocene African megaherbivore losses associated with community biomass restructuring.

Fossil abundance data can reveal ecological dynamics underpinning taxonomic declines. Using fossil dental metrics, we reconstructed body mass and mass-abundance distributions in Late Miocene to recent African large mammal communities. Despite collection biases, fossil and extant mass-abundance distributions are highly similar, with unimodal distributions likely reflecting savanna environments. Above 45 kilograms, abundance decreases exponentially with mass, with slopes close to -0.75, as predicted by metabolic scaling. Furthermore, communities before ~4 million years ago had considerably more large-sized individuals, with a greater proportion of total biomass allocated in larger size categories, than did later communities. Over time, individuals and biomass were redistributed into smaller size categories, reflecting a gradual loss of large-sized individuals from the fossil record paralleling the long-term decline of Plio-Pleistocene large mammal diversity.

Is it inappropriate to ask for your age? Evaluating parameter impact on tree dating in a challenging clade (Macroscelidea).

Sengis (order Macroscelidea) are small mammals endemic to Africa. The taxonomy and phylogeny of sengis has been difficult to resolve due to a lack of clear morphological apomorphies. Molecular phylogenies have already significantly revised sengi systematics, but until now no molecular phylogeny has included all 20 extant species. In addition, the age of origin of the sengi crown clade and the divergence age of its two extant families remain unclear. Two recently published studies based on different datasets and age-calibration parameters (DNA type, outgroup selection, fossil calibration points) proposed highly different divergent age estimates and evolutionary scenarios. We obtained nuclear and mitochondrial DNA from mainly museum specimens using target enrichment of single-stranded DNA libraries to generate the first phylogeny of all extant macroscelidean species. We then explored the effects of different parameters (type of DNA, ratio of ingroup to outgroup sampling, number and type of fossil calibration points) and their resulting impacts on age estimates for the origin and initial diversification of Macroscelidea. We show that, even after correcting for substitution saturation, both using mitochondrial DNA in conjunction with nuclear DNA or alone results in much older ages and different branch lengths than when using nuclear DNA alone. We further show that the former effect can be attributed to insufficient amounts of nuclear data. If multiple calibration points are included, the age of the sengi crown group fossil prior has minimal impact on the estimated time frame of sengi evolution. In contrast, the inclusion or exclusion of outgroup fossil priors has a major effect on the resulting node ages. We also find that a reduced sampling of ingroup species does not significantly affect overall age estimates and that terminal specific substitution rates can serve as a means to evaluate the biological likeliness of the produced temporal estimates. Our study demonstrates how commonly varied parameters in temporal calibration of phylogenies affect age estimates. Dated phylogenies should therefore always be seen in the context of the dataset which was used to produce them.

Ruminant inner ear shape records 35 million years of neutral evolution.

Extrinsic and intrinsic factors impact diversity. On deep-time scales, the extrinsic impact of climate and geology are crucial, but poorly understood. Here, we use the inner ear morphology of ruminant artiodactyls to test for a deep-time correlation between a low adaptive anatomical structure and both extrinsic and intrinsic variables. We apply geometric morphometric analyses in a phylogenetic frame to X-ray computed tomographic data from 191 ruminant species. Contrasting results across ruminant clades show that neutral evolutionary processes over time may strongly influence the evolution of inner ear morphology. Extant, ecologically diversified clades increase their evolutionary rate with decreasing Cenozoic global temperatures. Evolutionary rate peaks with the colonization of new continents. Simultaneously, ecologically restricted clades show declining or unchanged rates. These results suggest that both climate and paleogeography produced heterogeneous environments, which likely facilitated Cervidae and Bovidae diversification and exemplifies the effect of extrinsic and intrinsic factors on evolution in ruminants.

Blue Turns to Gray: Paleogenomic Insights into the Evolutionary History and Extinction of the Blue Antelope (Hippotragus leucophaeus).

The blue antelope (Hippotragus leucophaeus) is the only large African mammal species to have become extinct in historical times, yet no nuclear genomic information is available for this species. A recent study showed that many alleged blue antelope museum specimens are either roan (Hippotragus equinus) or sable (Hippotragus niger) antelopes, further reducing the possibilities for obtaining genomic information for this extinct species. While the blue antelope has a rich fossil record from South Africa, climatic conditions in the region are generally unfavorable to the preservation of ancient DNA. Nevertheless, we recovered two blue antelope draft genomes, one at 3.4× mean coverage from a historical specimen (∼200 years old) and one at 2.1× mean coverage from a fossil specimen dating to 9,800-9,300 cal years BP, making it currently the oldest paleogenome from Africa. Phylogenomic analyses show that blue and sable antelope are sister species, confirming previous mitogenomic results, and demonstrate ancient gene flow from roan into blue antelope. We show that blue antelope genomic diversity was much lower than in roan and sable antelope, indicative of a low population size since at least the early Holocene. This supports observations from the fossil record documenting major decreases in the abundance of blue antelope after the Pleistocene-Holocene transition. Finally, the persistence of this species throughout the Holocene despite low population size suggests that colonial-era human impact was likely the decisive factor in the blue antelope's extinction.

Early Pleistocene large mammals from Maka'amitalu, Hadar, lower Awash Valley, Ethiopia.

The Early Pleistocene was a critical time period in the evolution of eastern African mammal faunas, but fossil assemblages sampling this interval are poorly known from Ethiopia's Afar Depression. Field work by the Hadar Research Project in the Busidima Formation exposures (~2.7-0.8 Ma) of Hadar in the lower Awash Valley, resulted in the recovery of an early Homo maxilla (A.L. 666-1) with associated stone tools and fauna from the Maka'amitalu basin in the 1990s. These assemblages are dated to ~2.35 Ma by the Bouroukie Tuff 3 (BKT-3). Continued work by the Hadar Research Project over the last two decades has greatly expanded the faunal collection. Here, we provide a comprehensive account of the Maka'amitalu large mammals (Artiodactyla, Carnivora, Perissodactyla, Primates, and Proboscidea) and discuss their paleoecological and biochronological significance. The size of the Maka'amitalu assemblage is small compared to those from the Hadar Formation (3.45-2.95 Ma) and Ledi-Geraru (2.8-2.6 Ma) but includes at least 20 taxa. Bovids, suids, and Theropithecus are common in terms of both species richness and abundance, whereas carnivorans, equids, and megaherbivores are rare. While the taxonomic composition of the Maka'amitalu fauna indicates significant species turnover from the Hadar Formation and Ledi-Geraru deposits, turnover seems to have occurred at a constant rate through time as taxonomic dissimilarity between adjacent fossil assemblages is strongly predicted by their age difference. A similar pattern characterizes functional ecological turnover, with only subtle changes in dietary proportions, body size proportions, and bovid abundances across the composite lower Awash sequence. Biochronological comparisons with other sites in eastern Africa suggest that the taxa recovered from the Maka'amitalu are broadly consistent with the reported age of the BKT-3 tuff. Considering the age of BKT-3 and biochronology, a range of 2.4-1.9 Ma is most likely for the faunal assemblage.

Evolution of the bovid cranium: morphological diversification under allometric constraint.

The role of environmental selection in generating novel morphology is often taken for granted, and morphology is generally assumed to be adaptive. Bovids (antelopes and relatives) are widely differentiated in their dietary and climatic preferences, and presumably their cranial morphologies are the result of adaptation to different environmental pressures. In order to test these ideas, we performed 3D geometric morphometric analyses on 141 crania representing 96 bovid species in order to assess the influence of both extrinsic (e.g. diet, habitat) and intrinsic (size, modularity) factors on cranial shape. Surprisingly, we find that bovid crania are highly clumped in morphospace, with a large number of ecologically disparate species occupying a very similar range of morphology clustered around the mean shape. Differences in shape among dietary, habitat, and net primary productivity categories are largely non-significant, but we found a strong interaction between size and diet in explaining shape. We furthermore found no evidence for modularity having played a role in the generation of cranial differences across the bovid tree. Rather, the distribution of bovid cranial morphospace appears to be mainly the result of constraints imposed by a deeply conserved size-shape allometry, and dietary diversification the result of adaptation of existing allometric pathways.

Diversity and Paleodemography of the Addax (Addax nasomaculatus), a Saharan Antelope on the Verge of Extinction.

Since the 19th century, the addax (Addax nasomaculatus) has lost approximately 99% of its former range. Along with its close relatives, the blue antelope (Hippotragus leucophaeus) and the scimitar-horned oryx (Oryx dammah), the addax may be the third large African mammal species to go extinct in the wild in recent times. Despite this, the evolutionary history of this critically endangered species remains virtually unknown. To gain insight into the population history of the addax, we used hybridization capture to generate ten complete mitochondrial genomes from historical samples and assembled a nuclear genome. We found that both mitochondrial and nuclear diversity are low compared to other African bovids. Analysis of mitochondrial genomes revealed a most recent common ancestor ~32 kya (95% CI 11-58 kya) and weak phylogeographic structure, indicating that the addax likely existed as a highly mobile, panmictic population across its Sahelo-Saharan range in the past. PSMC analysis revealed a continuous decline in effective population size since ~2 Ma, with short intermediate increases at ~500 and ~44 kya. Our results suggest that the addax went through a major bottleneck in the Late Pleistocene, remaining at low population size prior to the human disturbances of the last few centuries.

Differing effects of size and lifestyle on bone structure in mammals.

BACKGROUND: Mammals are a highly diverse group, with body mass ranging from 2 g to 170 t, and encompassing species with terrestrial, aquatic, aerial, and subterranean lifestyles. The skeleton is involved in most aspects of vertebrate life history, but while previous macroevolutionary analyses have shown that structural, phylogenetic, and functional factors influence the gross morphology of skeletal elements, their inner structure has received comparatively little attention. Here we analysed bone structure of the humerus and mid-lumbar vertebrae across mammals and their correlations with different lifestyles and body size. RESULTS: We acquired bone structure parameters in appendicular and axial elements (humerus and mid-lumbar vertebra) from 190 species across therian mammals (placentals + marsupials). Our sample captures all transitions to aerial, fully aquatic, and subterranean lifestyles in extant therian clades. We found that mammalian bone structure is highly disparate and we show that the investigated vertebral structure parameters mostly correlate with body size, but not lifestyle, while the opposite is true for humeral parameters. The latter also show a high degree of convergence among the clades that have acquired specialised (non-terrestrial) lifestyles. CONCLUSIONS: In light of phylogenetic, size, and functional factors, the distribution of each investigated structural parameter reveals patterns explaining the construction of appendicular and axial skeletal elements in mammalian species spanning most of the extant diversity of the clade in terms of body size and lifestyle. These patterns should be further investigated with analyses focused on specific lifestyle transitions that would ideally include key fossils.

Identifying the true number of specimens of the extinct blue antelope (Hippotragus leucophaeus).

Native to southern Africa, the blue antelope (Hippotragus leucophaeus) is the only large African mammal species known to have become extinct in historical times. However, it was poorly documented prior to its extinction ~ 1800 AD, and many of the small number of museum specimens attributed to it are taxonomically contentious. This places limitations on our understanding of its morphology, ecology, and the mechanisms responsible for its demise. We retrieved genetic information from ten of the sixteen putative blue antelope museum specimens using both shotgun sequencing and mitochondrial genome target capture in an attempt to resolve the uncertainty surrounding the identification of these specimens. We found that only four of the ten investigated specimens, and not a single skull, represent the blue antelope. This indicates that the true number of historical museum specimens of the blue antelope is even smaller than previously thought, and therefore hardly any reference material is available for morphometric, comparative and genetic studies. Our study highlights how genetics can be used to identify rare species in natural history collections where other methods may fail or when records are scarce. Additionally, we present an improved mitochondrial reference genome for the blue antelope as well as one complete and two partial mitochondrial genomes. A first analysis of these mitochondrial genomes indicates low levels of maternal genetic diversity in the 'museum population', possibly confirming previous results that blue antelope population size was already low at the time of the European colonization of South Africa.

Hyena paleogenomes reveal a complex evolutionary history of cross-continental gene flow between spotted and cave hyena.

The genus Crocuta (African spotted and Eurasian cave hyenas) includes several closely related extinct and extant lineages. The relationships among these lineages, however, are contentious. Through the generation of population-level paleogenomes from late Pleistocene Eurasian cave hyena and genomes from modern African spotted hyena, we reveal the cross-continental evolutionary relationships between these enigmatic hyena lineages. We find a deep divergence (~2.5 Ma) between African and Eurasian Crocuta populations, suggesting that ancestral Crocuta left Africa around the same time as early Homo. Moreover, we find discordance between nuclear and mitochondrial phylogenies and evidence for bidirectional gene flow between African and Eurasian Crocuta after the lineages split, which may have complicated prior taxonomic classifications. Last, we find a number of introgressed loci that attained high frequencies within the recipient lineage, suggesting some level of adaptive advantage from admixture.

Large-scale ruminant genome sequencing provides insights into their evolution and distinct traits.

The ruminants are one of the most successful mammalian lineages, exhibiting morphological and habitat diversity and containing several key livestock species. To better understand their evolution, we generated and analyzed de novo assembled genomes of 44 ruminant species, representing all six Ruminantia families. We used these genomes to create a time-calibrated phylogeny to resolve topological controversies, overcoming the challenges of incomplete lineage sorting. Population dynamic analyses show that population declines commenced between 100,000 and 50,000 years ago, which is concomitant with expansion in human populations. We also reveal genes and regulatory elements that possibly contribute to the evolution of the digestive system, cranial appendages, immune system, metabolism, body size, cursorial locomotion, and dentition of the ruminants.

Large mammal diets and paleoecology across the Oldowan-Acheulean transition at Olduvai Gorge, Tanzania from stable isotope and tooth wear analyses.

The well-dated Pleistocene sediments at Olduvai Gorge have yielded a rich record of hominin fossils, stone tools, and vertebrate faunal remains that, taken together, provide insight to hominin behavior and paleoecology. Since 2008, the Olduvai Geochronology and Archaeology Project (OGAP) has undertaken extensive excavations in Bed II that have yielded a large collection of early Pleistocene stone tools and fossils. The strata of Lower, Middle and Upper Bed II at Olduvai Gorge capture the critical transition from Oldowan to Acheulean technology and therefore provide an opportunity to explore the possible role of biotic and abiotic change during the transition. Here, we analyze newly discovered and existing fossil teeth from Bed II sites using stable isotope and tooth wear methods to investigate the diets of large mammals. We reconstruct the dietary ecology of Bed II mammals and evaluate whether vegetation or hydroclimate shifts are associated with the technological change. Combined isotope and tooth wear data suggest most mammals were C4 grazers or mixed feeders. Carbon isotope data from bulk enamel samples indicate that a large majority of Bed II large mammals analyzed had diets comprising mostly C4 vegetation (>75% of diet), whereas only a small number of individuals had either mixed C3-C4 or mostly C3 diets (<25% C4). Mesowear generally indicates an increase of the abrasiveness of the diet between intervals IIA and IIB (∼1.66 Ma), probably reflecting increased grazing. Microwear indicates more abrasive diets in interval IIA suggesting stronger seasonal differences at the time of death during this interval. This is also supported by the intratooth isotope profiles from Equus oldowayensis molars, which suggest a possible decrease in seasonality across the transition. Neither stable isotope nor tooth wear analyses indicate major vegetation or hydrological change across the Oldowan-Acheulean transition.

Author Correction: The rise and fall of the Old World savannah fauna and the origins of the African savannah biome.

In the version of this Article originally published, each of the five panels in Fig. 5 incorrectly contained a black diagonal line across the plot. This has now been corrected.

The rise and fall of the Old World savannah fauna and the origins of the African savannah biome.

Despite much interest in the ecology and origins of the extensive grassland ecosystems of the modern world, the biogeographic relationships of savannah palaeobiomes of Africa, India and mainland Eurasia have remained unclear. Here we assemble the most recent data from the Neogene mammal fossil record in order to map the biogeographic development of Old World mammalian faunas in relation to palaeoenvironmental conditions. Using genus-level faunal similarity and mean ordinated hypsodonty in combination with palaeoclimate modelling, we show that savannah faunas developed as a spatially and temporally connected entity that we term the Old World savannah palaeobiome. The Old World savannah palaeobiome flourished under the influence of middle and late Miocene global cooling and aridification, which resulted in the spread of open habitats across vast continental areas. This extensive biome fragmented into Eurasian and African branches due to increased aridification in North Africa and Arabia during the late Miocene. Its Eurasian branches had mostly disappeared by the end of the Miocene, but the African branch survived and eventually contributed to the development of Plio-Pleistocene African savannah faunas, including their early hominins. The modern African savannah fauna is thus a continuation of the extensive Old World savannah palaeobiome.

Dietary traits of the ungulates from the HWK EE site at Olduvai Gorge (Tanzania): Diachronic changes and seasonality.

The Oldowan site HWK EE (Olduvai Gorge, Tanzania) has yielded a large fossil and stone tool assemblage at the transition from Lower to Middle Bed II, ∼1.7 Ma. Integrated tooth wear and stable isotope analyses were performed on the three most abundant ungulate taxa from HWK EE, namely Alcelaphini, cf. Antidorcas recki (Antilopini) and Equus oldowayensis (Equini), to infer dietary traits in each taxon. Some paleodietary changes were observed for cf. A. recki and E. oldowayensis based on tooth wear at the transition from the Lemuta to the Lower Augitic Sandstone (LAS) interval within the HWK EE sequence. Stable carbon and oxygen isotope data show no significant changes in bulk diet or hydroclimate between the Lemuta and LAS intervals. The combined tooth wear and stable isotope data suggest similar paleoecological conditions across the two HWK EE intervals, but that differences in vegetation consumed among ungulates may have resulted in changes in dietary niches. Integrating tooth wear and stable isotope analyses permits the characterization of ungulate diets and habitats at HWK EE where C4 dominated and minor mixed C3 and C4 habitats were present. Our results provide a better understanding of the paleoenvironmental conditions of the Lemuta and LAS intervals. The LAS assemblage was mostly accumulated during relatively dry periods at Olduvai Gorge when grasses were not as readily available and grazing animals may have been more nutritionally-stressed than during the formation of the Lemuta assemblage. This helps to contextualize variations in hominin and carnivore feeding behavior observed from the faunal assemblages produced during the two main occupations of the site.

Paleoecology of the Serengeti during the Oldowan-Acheulean transition at Olduvai Gorge, Tanzania: The mammal and fish evidence.

Eight years of excavation work by the Olduvai Geochronology and Archaeology Project (OGAP) has produced a rich vertebrate fauna from several sites within Bed II, Olduvai Gorge, Tanzania. Study of these as well as recently re-organized collections from Mary Leakey's 1972 HWK EE excavations here provides a synthetic view of the faunal community of Olduvai during Middle Bed II at ∼1.7-1.4 Ma, an interval that captures the local transition from Oldowan to Acheulean technology. We expand the faunal list for this interval, name a new bovid species, clarify the evolution of several mammalian lineages, and record new local first and last appearances. Compositions of the fish and large mammal assemblages support previous indications for the dominance of open and seasonal grassland habitats at the margins of an alkaline lake. Fish diversity is low and dominated by cichlids, which indicates strongly saline conditions. The taphonomy of the fish assemblages supports reconstructions of fluctuating lake levels with mass die-offs in evaporating pools. The mammals are dominated by grazing bovids and equids. Habitats remained consistently dry and open throughout the entire Bed II sequence, with no major turnover or paleoecological changes taking place. Rather, wooded and wet habitats had already given way to drier and more open habitats by the top of Bed I, at 1.85-1.80 Ma. This ecological change is close to the age of the Oldowan-Acheulean transition in Kenya and Ethiopia, but precedes the local transition in Middle Bed II. The Middle Bed II large mammal community is much richer in species and includes a much larger number of large-bodied species (>300 kg) than the modern Serengeti. This reflects the severity of Pleistocene extinctions on African large mammals, with the loss of large species fitting a pattern typical of defaunation or 'downsizing' by human disturbance. However, trophic network (food web) analyses show that the Middle Bed II community was robust, and comparisons with the Serengeti community indicate that the fundamental structure of food webs remained intact despite Pleistocene extinctions. The presence of a generalized meat-eating hominin in the Middle Bed II community would have increased competition among carnivores and vulnerability among herbivores, but the high generality and interconnectedness of the Middle Bed II food web suggests this community was buffered against extinctions caused by trophic interactions.

Bony labyrinth morphology clarifies the origin and evolution of deer.

Deer are an iconic group of large mammals that originated in the Early Miocene of Eurasia (ca. 19 Ma). While there is some consensus on key relationships among their members, on the basis of molecular- or morphology-based analyses, or combined approaches, many questions remain, and the bony labyrinth has shown considerable potential for the phylogenetics of this and other groups. Here we examine its shape in 29 species of living and fossil deer using 3D geometric morphometrics and cladistics. We clarify several issues of the origin and evolution of cervids. Our results give new age estimates at different nodes of the tree and provide for the first time a clear distinction of stem and crown Cervidae. We unambiguously attribute the fossil Euprox furcatus (13.8 Ma) to crown Cervidae, pushing back the origin of crown deer to (at least) 4 Ma. Furthermore, we show that Capreolinae are more variable in bony labyrinth shape than Cervinae and confirm for the first time the monophyly of the Old World Capreolinae (including the Chinese water deer Hydropotes) based on morphological characters only. Finally, we provide evidence to support the sister group relationship of Megaloceros giganteus with the fallow deer Dama.