Origin of adaptations to open environments and social behaviour in sabretoothed cats from the northeastern border of the Tibetan Plateau.

The iconic sabretooth Homotherium is thought to have hunted cooperatively, but the origin of this behaviour and correlated morphological adaptations are largely unexplored. Here we report the most primitive species of Amphimachairodus (Amphimachairodus hezhengensis sp. nov.), a member of Machairodontini basal to Homotherium, from the Linxia Basin, northeastern border of the Tibetan Plateau (9.8-8.7 Ma). The long snout, laterally oriented and posteriorly located orbit of Amphimachairodus suggest a better ability to observe the surrounding environment, rather than targeting single prey, pointing to an adaptation to the open environment or social behaviour. A pathological forepaw of Amphimachairodus provides direct evidence of partner care. Our analyses of trait evolutionary rates support that traits correlated with killing behaviour and open environment adaptation evolved prior to other traits, suggesting that changes in hunting behaviour may be the major evolutionary driver in the early evolution of the lineage. A. hezhengensis represents one of the most important transitions in the evolution of Machairodontini, leading to adaptation in open environments and contributing to their further dispersal and radiation worldwide. This rapid morphological change is likely to be correlated with increasingly arid environments caused by the rise of the Tibetan Plateau, and competition from abundant large carnivores in this area.

Ecological Specialization and Evolutionary Reticulation in Extant Hyaenidae.

During the Miocene, Hyaenidae was a highly diverse family of Carnivora that has since been severely reduced to four species: the bone-cracking spotted, striped, and brown hyenas, and the specialized insectivorous aardwolf. Previous studies investigated the evolutionary histories of the spotted and brown hyenas, but little is known about the remaining two species. Moreover, the genomic underpinnings of scavenging and insectivory, defining traits of the extant species, remain elusive. Here, we generated an aardwolf genome and analyzed it together with the remaining three species to reveal their evolutionary relationships, genomic underpinnings of their scavenging and insectivorous lifestyles, and their respective genetic diversities and demographic histories. High levels of phylogenetic discordance suggest gene flow between the aardwolf lineage and the ancestral brown/striped hyena lineage. Genes related to immunity and digestion in the bone-cracking hyenas and craniofacial development in the aardwolf showed the strongest signals of selection, suggesting putative key adaptations to carrion and termite feeding, respectively. A family-wide expansion in olfactory receptor genes suggests that an acute sense of smell was a key early adaptation. Finally, we report very low levels of genetic diversity within the brown and striped hyenas despite no signs of inbreeding, putatively linked to their similarly slow decline in effective population size over the last ∼2 million years. High levels of genetic diversity and more stable population sizes through time are seen in the spotted hyena and aardwolf. Taken together, our findings highlight how ecological specialization can impact the evolutionary history, demographics, and adaptive genetic changes of an evolutionary lineage.

Brain expansion in early hominins predicts carnivore extinctions in East Africa.

While the anthropogenic impact on ecosystems today is evident, it remains unclear if the detrimental effect of hominins on co-occurring biodiversity is a recent phenomenon or has also been the pattern for earlier hominin species. We test this using the East African carnivore fossil record. We analyse the diversity of carnivores over the last four million years and investigate whether any decline is related to an increase in hominin cognitive capacity, vegetation changes or climatic changes. We find that extinction rates in large carnivores correlate with increased hominin brain size and with vegetation changes, but not with precipitation or temperature changes. While temporal analyses cannot distinguish between the effects of vegetation changes and hominins, we show through spatial analyses of contemporary carnivores in Africa that only hominin causation is plausible. Our results suggest that substantial anthropogenic influence on biodiversity started millions of years earlier than currently assumed.

A contextual review of the Carnivora of Kanapoi.

The Early Pliocene is a crucial time period in carnivoran evolution. Holarctic carnivoran faunas suffered a turnover event at the Miocene-Pliocene boundary. This event is also observed in Africa but its onset is later and the process more drawn-out. Kanapoi is one of the earliest faunas in Africa to show evidence of a fauna that is more typical Pliocene than Miocene in character. The taxa recovered from Kanapoi are: Torolutra sp., Enhydriodon (2 species), Genetta sp., Helogale sp., Homotherium sp., Dinofelis petteri, Felis sp., and Parahyaena howelli. Analysis of the broader carnivoran context of which Kanapoi is an example shows that all these taxa are characteristic of Plio-Pleistocene African faunas, rather than Miocene ones. While some are still extant and some went extinct in the Early Pleistocene, P. howelli is unique in both originating and going extinct in the Early Pliocene.

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.

Revealing the maternal demographic history of Panthera leo using ancient DNA and a spatially explicit genealogical analysis.

BACKGROUND: Understanding the demographic history of a population is critical to conservation and to our broader understanding of evolutionary processes. For many tropical large mammals, however, this aim is confounded by the absence of fossil material and by the misleading signal obtained from genetic data of recently fragmented and isolated populations. This is particularly true for the lion which as a consequence of millennia of human persecution, has large gaps in its natural distribution and several recently extinct populations. RESULTS: We sequenced mitochondrial DNA from museum-preserved individuals, including the extinct Barbary lion (Panthera leo leo) and Iranian lion (P. l. persica), as well as lions from West and Central Africa. We added these to a broader sample of lion sequences, resulting in a data set spanning the historical range of lions. Our Bayesian phylogeographical analyses provide evidence for highly supported, reciprocally monophyletic lion clades. Using a molecular clock, we estimated that recent lion lineages began to diverge in the Late Pleistocene. Expanding equatorial rainforest probably separated lions in South and East Africa from other populations. West African lions then expanded into Central Africa during periods of rainforest contraction. Lastly, we found evidence of two separate incursions into Asia from North Africa, first into India and later into the Middle East. CONCLUSIONS: We have identified deep, well-supported splits within the mitochondrial phylogeny of African lions, arguing for recognition of some regional populations as worthy of independent conservation. More morphological and nuclear DNA data are now needed to test these subdivisions.

Pleistocene Chinese cave hyenas and the recent Eurasian history of the spotted hyena, Crocuta crocuta.

The living hyena species (spotted, brown, striped and aardwolf) are remnants of a formerly diverse group of more than 80 fossil species, which peaked in diversity in the Late Miocene (about 7-8 Ma). The fossil history indicates an African origin, and morphological and ancient DNA data have confirmed that living spotted hyenas (Crocuta crocuta) of Africa were closely related to extinct Late Pleistocene cave hyenas from Europe and Asia. The current model used to explain the origins of Eurasian cave hyena populations invokes multiple migrations out of Africa between 3.5-0.35 Ma. We used mitochondrial DNA sequences from radiocarbon-dated Chinese Pleistocene hyena specimens to examine the origin of Asian populations, and temporally calibrate the evolutionary history of spotted hyenas. Our results support a far more recent evolutionary timescale (430-163 kya) and suggest that extinct and living spotted hyena populations originated from a widespread Eurasian population in the Late Pleistocene, which was only subsequently restricted to Africa. We developed statistical tests of the contrasting population models and their fit to the fossil record. Coalescent simulations and Bayes Factor analysis support the new radiocarbon-calibrated timescale and Eurasian origins model. The new Eurasian biogeographic scenario proposed for the hyena emphasizes the role of the vast steppe grasslands of Eurasia in contrast to models only involving Africa. The new methodology for combining genetic and geological data to test contrasting models of population history will be useful for a wide range of taxa where ancient and historic genetic data are available.

Hypercanines: Not just for sabertooths.

Hypercanines are here defined as hypertrophied caniniform teeth, that is, canine teeth that are elongated to serve specific functions in different clades of mammals and their synapsid ancestors. This article presents an overview of the occurrence of hypercanines, their growth, and their function across a broad range of clades. Sabertooth felids and felid-like taxa are found to be unique in having determinate growth (although some Dinocerata may also have this). The most common function of hypercanines among herbivores is found to be sexual display and male-male competition. Three clades of small ruminants have evolved hypercanines that can move within their sockets, although the evolutionary details behind this convergent adaptation have not been worked out.

A hyaena on stilts: comparison of the limb morphology of Ictitherium ebu (Mammalia: Hyaenidae) from the Late Miocene of Lothagam, Turkana Basin, Kenya with extant Canidae and Hyaenidae.

The long, gracile morphology of the limb bones of the Late Miocene hyaenid Ictitherium ebu has led to the hypothesis that this animal was cursorial. The forelimb and femur of the holotype were compared with specimens of extant Hyaenidae and Canidae. Two morphometric methods were used. The first used measurements to calculate indices of different morphological characters. The second method involved capturing photographs of the anterior distal humerus of each specimen, mapping six landmarks on them, and calculating truss distances. These distances represent a schematic reproduction of the elbow. Multivariate statistical analysis primarily separated the data based on taxonomy, yet locomotor and habitat categories were also considered. Ictitherium ebu has an overall morphology similar to that of the maned wolf and a distal humerus reminiscent of that of the aardwolf. The long, gracile limb bones of I. ebu are suggested to be adaptations for pouncing on prey, for locomotor efficiency, and for looking over the tall grass of the open environments the animal lived in, much like the present-day maned wolf.

Fossil brains provide evidence of underwater feeding in early seals.

Pinnipeds (seals and related species) use their whiskers to explore their environment and locate their prey. Today they live mostly in marine habitats and are adapted for a highly specialised amphibious lifestyle with their flippers for locomotion and a hydrodynamically streamlined body. The earliest pinnipeds, however, lived on land and in freshwater habitats, much like mustelids today. Here we reconstruct the underwater foraging behaviour of one of these earliest pinnipeds (Potamotherium), focusing in particular on how it used its whiskers (vibrissae). For this purpose, we analyse the coronal gyrus of the brain of 7 fossil and 31 extant carnivorans. This region receives somatosensory input from the head. Our results show that the reliance on whiskers in modern pinnipeds is an ancestral feature that favoured survival of stem pinnipeds in marine habitats. This study provides insights into an impressive ecological transition in carnivoran evolution: from terrestrial to amphibious marine species. Adaptations for underwater foraging were crucial for this transition.

A 14,000-year-old genome sheds light on the evolution and extinction of a Pleistocene vulture.

The New World Vulture [Coragyps] occidentalis (L. Miller, 1909) is one of many species that were extinct by the end of the Pleistocene. To understand its evolutionary history we sequenced the genome of a 14,000 year old [Coragyps] occidentalis found associated with megaherbivores in the Peruvian Andes. occidentalis has been viewed as the ancestor, or possibly sister, to the extant Black Vulture Coragyps atratus, but genomic data shows occidentalis to be deeply nested within the South American clade of atratus. Coragyps atratus inhabits lowlands, but the fossil record indicates that occidentalis mostly occupied high elevations. Our results suggest that occidentalis evolved from a population of atratus in southwestern South America that colonized the High Andes 300 to 400 kya. The morphological and morphometric differences between occidentalis and atratus may thus be explained by ecological diversification following from the natural selection imposed by this new and extreme, high elevation environment. The sudden evolution of a population with significantly larger body size and different anatomical proportions than atratus thus constitutes an example of punctuated evolution.

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.

A genomic exploration of the early evolution of extant cats and their sabre-toothed relatives.

Background: The evolutionary relationships of Felidae during their Early-Middle Miocene radiation is contentious. Although the early common ancestors have been subsumed under the grade-group Pseudaelurus, this group is thought to be paraphyletic, including the early ancestors of both modern cats and extinct sabretooths. Methods: Here, we sequenced a draft nuclear genome of Smilodon populator, dated to 13,182 ± 90 cal BP, making this the oldest palaeogenome from South America to date, a region known to be problematic for ancient DNA preservation. We analysed this genome, together with genomes from other extinct and extant cats to investigate their phylogenetic relationships. Results: We confirm a deep divergence (~20.65 Ma) within sabre-toothed cats. Through the analysis of both simulated and empirical data, we show a lack of gene flow between Smilodon and contemporary Felidae. Conclusions: Given that some species traditionally assigned to Pseudaelurus originated in the Early Miocene ~20 Ma, this indicates that some species of Pseudaelurus may be younger than the lineages they purportedly gave rise to, further supporting the hypothesis that Pseudaelurus was paraphyletic.

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.

An ecometric analysis of the fossil mammal record of the Turkana Basin.

Although ecometric methods have been used to analyse fossil mammal faunas and environments of Eurasia and North America, such methods have not yet been applied to the rich fossil mammal record of eastern Africa. Here we report results from analysis of a combined dataset spanning east and west Turkana from Kenya between 7 and 1 million years ago (Ma). We provide temporally and spatially resolved estimates of temperature and precipitation and discuss their relationship to patterns of faunal change, and propose a new hypothesis to explain the lack of a temperature trend. We suggest that the regionally arid Turkana Basin may between 4 and 2 Ma have acted as a 'species factory', generating ecological adaptations in advance of the global trend. We show a persistent difference between the eastern and western sides of the Turkana Basin and suggest that the wetlands of the shallow eastern side could have provided additional humidity to the terrestrial ecosystems. Pending further research, a transient episode of faunal change centred at the time of the KBS Member (1.87-1.53 Ma), may be equally plausibly attributed to climate change or to a top-down ecological cascade initiated by the entry of technologically sophisticated humans.This article is part of the themed issue 'Major transitions in human evolution'.

Paleoanthropology. Late Pliocene fossiliferous sedimentary record and the environmental context of early Homo from Afar, Ethiopia.

Sedimentary basins in eastern Africa preserve a record of continental rifting and contain important fossil assemblages for interpreting hominin evolution. However, the record of hominin evolution between 3 and 2.5 million years ago (Ma) is poorly documented in surface outcrops, particularly in Afar, Ethiopia. Here we present the discovery of a 2.84- to 2.58-million-year-old fossil and hominin-bearing sediments in the Ledi-Geraru research area of Afar, Ethiopia, that have produced the earliest record of the genus Homo. Vertebrate fossils record a faunal turnover indicative of more open and probably arid habitats than those reconstructed earlier in this region, which is in broad agreement with hypotheses addressing the role of environmental forcing in hominin evolution at this time. Geological analyses constrain depositional and structural models of Afar and date the LD 350-1 Homo mandible to 2.80 to 2.75 Ma.

The evolution of cursorial carnivores in the Tertiary: implications of elbow-joint morphology.

The evolution of cursorial adaptations in Tertiary (65-1.65 Myr ago) carnivores has been a contentious issue. Most such studies have focused on the relationship between hind limb proportions and running speed. Here, we show morphometrically that in extant carnivores, the elbow joint has evolved in two distinct directions with mutually exclusive implications for locomotor ability and prey procurement. Some carnivores retain supinatory ability, allowing them to manipulate prey and other items with the forepaws. Such carnivores can become very large. Other carnivores lose the ability to supinate and become cursors. This allows for only moderate size increase. Modern carnivores above ca. 20 kg body mass are committed to one or other of these strategies. This threshold coincides with a postulated threshold in carnivore physiology. The biaxial pattern mostly follows phylogenetic lines, but a strong selective regime can override this signal, as shown by the extant cheetah. Oligocene (33.7-23.8 Myr ago) and early-middle Miocene (23.8-11.2 Myr ago) carnivores follow the same pattern, though in the Miocene the pattern is shifted towards larger body mass, which may be owing to the extraordinary richness of browsing ungulates at this time.

Temporal change in functional richness and evenness in the eastern African plio-pleistocene carnivoran guild.

We analyze functional richness and functional evenness of the carnivoran guild in eastern Africa from 3.5 Ma to 1.5 Ma, and compare them to the present day. The data consist of characters of the craniodental apparatus of 76 species of fossil and extant carnivorans, divided into four 0.5 Ma time slices from 3.5 to 1.5 Ma, together with the modern fauna. Focus is on large (>21.5 kg) carnivores. Results show that the large carnivore guild has lost nearly 99% of its functional richness since 3.5 Ma, in a process starting prior to 2 Ma. Measurement of functional evenness shows the modern large carnivore guild to be unique in being randomly distributed in morphospace while in all past time slices there is significant clustering of species. The results are analyzed in the light of known changes to climate and environment in eastern Africa. We conclude that climate change is unlikely to explain all of the changes found and suggest that the evolution of early hominins into carnivore niche space, especially the evolution of derived dietary strategies after 2 Ma, played a significant part in the reduction of carnivore functional richness.

Sabretoothed carnivores and the killing of large prey.

Sabre-like canines clearly have the potential to inflict grievous wounds leading to massive blood loss and rapid death. Hypotheses concerning sabretooth killing modes include attack to soft parts such as the belly or throat, where biting deep is essential to generate strikes reaching major blood vessels. Sabretoothed carnivorans are widely interpreted as hunters of larger and more powerful prey than that of their present-day nonsabretoothed relatives. However, the precise functional advantage of the sabretooth bite, particularly in relation to prey size, is unknown. Here, we present a new point-to-point bite model and show that, for sabretooths, depth of the killing bite decreases dramatically with increasing prey size. The extended gape of sabretooths only results in considerable increase in bite depth when biting into prey with a radius of less than ∼10 cm. For sabretooths, this size-reversed functional advantage suggests predation on species within a similar size range to those attacked by present-day carnivorans, rather than "megaherbivores" as previously believed. The development of the sabretooth condition appears to represent a shift in function and killing behaviour, rather than one in predator-prey relations. Furthermore, our results demonstrate how sabretoothed carnivorans are likely to have evolved along a functionally continuous trajectory: beginning as an extension of a jaw-powered killing bite, as adopted by present-day pantherine cats, followed by neck-powered biting and thereafter shifting to neck-powered shear-biting. We anticipate this new insight to be a starting point for detailed study of the evolution of pathways that encompass extreme specialisation, for example, understanding how neck-powered biting shifts into shear-biting and its significance for predator-prey interactions. We also expect that our model for point-to-point biting and bite depth estimations will yield new insights into the behaviours of a broad range of extinct predators including therocephalians (gorgonopsian + cynodont, sabretoothed mammal-like reptiles), sauropterygians (marine reptiles) and theropod dinosaurs.

Carnivoran remains from the Malapa hominin site, South Africa.

Recent discoveries at the new hominin-bearing deposits of Malapa, South Africa, have yielded a rich faunal assemblage associated with the newly described hominin taxon Australopithecus sediba. Dating of this deposit using U-Pb and palaeomagnetic methods has provided an age of 1.977 Ma, being one of the most accurately dated, time constrained deposits in the Plio-Pleistocene of southern Africa. To date, 81 carnivoran specimens have been identified at this site including members of the families Canidae, Viverridae, Herpestidae, Hyaenidae and Felidae. Of note is the presence of the extinct taxon Dinofelis cf. D. barlowi that may represent the last appearance date for this species. Extant large carnivores are represented by specimens of leopard (Panthera pardus) and brown hyaena (Parahyaena brunnea). Smaller carnivores are also represented, and include the genera Atilax and Genetta, as well as Vulpes cf. V. chama. Malapa may also represent the first appearance date for Felis nigripes (Black-footed cat). The geochronological age of Malapa and the associated hominin taxa and carnivoran remains provide a window of research into mammalian evolution during a relatively unknown period in South Africa and elsewhere. In particular, the fauna represented at Malapa has the potential to elucidate aspects of the evolution of Dinofelis and may help resolve competing hypotheses about faunal exchange between East and Southern Africa during the late Pliocene or early Pleistocene.