Reappraising the palaeobiology of Australopithecus.

The naming of Australopithecus africanus in 1925, based on the Taung Child, heralded a new era in human evolutionary studies and turned the attention of the then Eurasian-centric palaeoanthropologists to Africa, albeit with reluctance. Almost one hundred years later, Africa is recognized as the cradle of humanity, where the entire evolutionary history of our lineage prior to two million years ago took place-after the Homo-Pan split. This Review examines data from diverse sources and offers a revised depiction of the genus and characterizes its role in human evolution. For a long time, our knowledge of Australopithecus came from both A. africanus and Australopithecus afarensis, and the members of this genus were portrayed as bipedal creatures that did not use stone tools, with a largely chimpanzee-like cranium, a prognathic face and a brain slightly larger than that of chimpanzees. Subsequent field and laboratory discoveries, however, have altered this portrayal, showing that Australopithecus species were habitual bipeds but also practised arboreality; that they occasionally used stone tools to supplement their diet with animal resources; and that their infants probably depended on adults to a greater extent than what is seen in apes. The genus gave rise to several taxa, including Homo, but its direct ancestor remains elusive. In sum, Australopithecus had a pivotal bridging role in our evolutionary history owing to its morphological, behavioural and temporal placement between the earliest archaic putative hominins and later hominins-including the genus Homo.

New reptile shows dinosaurs and pterosaurs evolved among diverse precursors.

Dinosaurs and pterosaurs have remarkable diversity and disparity through most of the Mesozoic Era1-3. Soon after their origins, these reptiles diversified into a number of long-lived lineages, evolved unprecedented ecologies (for example, flying, large herbivorous forms) and spread across Pangaea4,5. Recent discoveries of dinosaur and pterosaur precursors6-10 demonstrated that these animals were also speciose and widespread, but those precursors have few if any well-preserved skulls, hands and associated skeletons11,12. Here we present a well-preserved partial skeleton (Upper Triassic, Brazil) of the new lagerpetid Venetoraptor gassenae gen. et sp. nov. that offers a more comprehensive look into the skull and ecology of one of these precursors. Its skull has a sharp, raptorial-like beak, preceding that of dinosaurs by around 80 million years, and a large hand with long, trenchant claws that firmly establishes the loss of obligatory quadrupedalism in these precursor lineages. Combining anatomical information of the new species with other dinosaur and pterosaur precursors shows that morphological disparity of precursors resembles that of Triassic pterosaurs and exceeds that of Triassic dinosaurs. Thus, the 'success' of pterosaurs and dinosaurs was a result of differential survival among a broader pool of ecomorphological variation. Our results show that the morphological diversity of ornithodirans started to flourish among early-diverging lineages and not only after the origins of dinosaurs and pterosaurs.

The oldest three-dimensionally preserved vertebrate neurocranium.

The neurocranium is an integral part of the vertebrate head, itself a major evolutionary innovation1,2. However, its early history remains poorly understood, with great dissimilarity in form between the two living vertebrate groups: gnathostomes (jawed vertebrates) and cyclostomes (hagfishes and lampreys)2,3. The 100 Myr gap separating the Cambrian appearance of vertebrates4-6 from the earliest three-dimensionally preserved vertebrate neurocrania7 further obscures the origins of modern states. Here we use computed tomography to describe the cranial anatomy of an Ordovician stem-group gnathostome: Eriptychius americanus from the Harding Sandstone of Colorado, USA8. A fossilized head of Eriptychius preserves a symmetrical set of cartilages that we interpret as the preorbital neurocranium, enclosing the fronts of laterally placed orbits, terminally located mouth, olfactory bulbs and pineal organ. This suggests that, in the earliest gnathostomes, the neurocranium filled out the space between the dermal skeleton and brain, like in galeaspids, osteostracans and placoderms and unlike in cyclostomes2. However, these cartilages are not fused into a single neurocranial unit, suggesting that this is a derived gnathostome trait. Eriptychius fills a major temporal and phylogenetic gap in our understanding of the evolution of the gnathostome head, revealing a neurocranium with an anatomy unlike that of any previously described vertebrate.

Postcranial evidence of late Miocene hominin bipedalism in Chad.

Bipedal locomotion is one of the key adaptations that define the hominin clade. Evidence of bipedalism is known from postcranial remains of late Miocene hominins as early as 6 million years ago (Ma) in eastern Africa1-4. Bipedality of Sahelanthropus tchadensis was hitherto inferred about 7 Ma in central Africa (Chad) based on cranial evidence5-7. Here we present postcranial evidence of the locomotor behaviour of S. tchadensis, with new insights into bipedalism at the early stage of hominin evolutionary history. The original material was discovered at locality TM 266 of the Toros-Ménalla fossiliferous area and consists of one left femur and two, right and left, ulnae. The morphology of the femur is most parsimonious with habitual bipedality, and the ulnae preserve evidence of substantial arboreal behaviour. Taken together, these findings suggest that hominins were already bipeds at around 7 Ma but also suggest that arboreal clambering was probably a significant part of their locomotor repertoire.

Cretaceous ornithurine supports a neognathous crown bird ancestor.

The bony palate diagnoses the two deepest clades of extant birds: Neognathae and Palaeognathae1-5. Neognaths exhibit unfused palate bones and generally kinetic skulls, whereas palaeognaths possess comparatively rigid skulls with the pterygoid and palatine fused into a single element, a condition long considered ancestral for crown birds (Neornithes)3,5-8. However, fossil evidence of palatal remains from taxa close to the origin of Neornithes is scarce, hindering strong inferences regarding the ancestral condition of the neornithine palate. Here we report a new taxon of toothed Late Cretaceous ornithurine bearing a pterygoid that is remarkably similar to those of the extant neognath clade Galloanserae (waterfowl + landfowl). Janavis finalidens, gen. et sp. nov., is generally similar to the well-known Mesozoic ornithurine Ichthyornis in its overall morphology, although Janavis is much larger and exhibits a substantially greater degree of postcranial pneumaticity. We recovered Janavis as the first-known well-represented member of Ichthyornithes other than Ichthyornis, clearly substantiating the persistence of the clade into the latest Cretaceous9. Janavis confirms the presence of an anatomically neognathous palate in at least some Mesozoic non-crown ornithurines10-12, suggesting that pterygoids similar to those of extant Galloanserae may be plesiomorphic for crown birds. Our results, combined with recent evidence on the ichthyornithine palatine12, overturn longstanding assumptions about the ancestral crown bird palate, and should prompt reevaluation of the purported galloanseran affinities of several bizarre early Cenozoic groups such as the 'pseudotoothed birds' (Pelagornithidae)13-15.

Morphology of Palaeospondylus shows affinity to tetrapod ancestors.

Palaeospondylus gunni, from the Middle Devonian period, is one of the most enigmatic fossil vertebrates, and its phylogenetic position has remained unclear since its discovery in Scotland in 1890 (ref. 1). The fossil's strange set of morphological features has made comparisons with known vertebrate morphotype diversity difficult. Here we use synchrotron radiation X-ray micro-computed tomography to show that Palaeospondylus was a sarcopterygian, and most probably a stem-tetrapod. The skeleton of Palaeospondylus consisted solely of endoskeletal elements in which hypertrophied chondrocyte cell lacunae, osteoids and a small fraction of perichondral bones developed. Despite the complete lack of teeth and dermal bones, the neurocranium of Palaeospondylus resembles those of stem-tetrapod Eusthenopteron2 and Panderichthys3, and phylogenetic analyses place Palaeospondylus in between them. Because the unique features of Palaeospondylus, such as the cartilaginous skeleton and the absence of paired appendages, are present in the larva of crown tetrapods, our study highlights an unanticipated heterochronic evolution at the root of tetrapods.

The oldest complete jawed vertebrates from the early Silurian of China.

Molecular studies suggest that the origin of jawed vertebrates was no later than the Late Ordovician period (around 450 million years ago (Ma))1,2. Together with disarticulated micro-remains of putative chondrichthyans from the Ordovician and early Silurian period3-8, these analyses suggest an evolutionary proliferation of jawed vertebrates before, and immediately after, the end-Ordovician mass extinction. However, until now, the earliest complete fossils of jawed fishes for which a detailed reconstruction of their morphology was possible came from late Silurian assemblages (about 425 Ma)9-13. The dearth of articulated, whole-body fossils from before the late Silurian has long rendered the earliest history of jawed vertebrates obscure. Here we report a newly discovered Konservat-Lagerstätte, which is marked by the presence of diverse, well-preserved jawed fishes with complete bodies, from the early Silurian (Telychian age, around 436 Ma) of Chongqing, South China. The dominant species, a 'placoderm' or jawed stem gnathostome, which we name Xiushanosteus mirabilis gen. et sp. nov., combines characters from major placoderm subgroups14-17 and foreshadows the transformation of the skull roof pattern from the placoderm to the osteichthyan condition10. The chondrichthyan Shenacanthus vermiformis gen. et sp. nov. exhibits extensive thoracic armour plates that were previously unknown in this lineage, and include a large median dorsal plate as in placoderms14-16, combined with a conventional chondrichthyan bauplan18,19. Together, these species reveal a previously unseen diversification of jawed vertebrates in the early Silurian, and provide detailed insights into the whole-body morphology of the jawed vertebrates of this period.

Insights into morphology and disease from the dog genome project.

Although most modern dog breeds are less than 200 years old, the symbiosis between man and dog is ancient. Since prehistoric times, repeated selection events have transformed the wolf into man's guardians, laborers, athletes, and companions. The rapid transformation from pack predator to loyal companion is a feat that is arguably unique among domesticated animals. How this transformation came to pass remained a biological mystery until recently: Within the past decade, the deployment of genomic approaches to study population structure, detect signatures of selection, and identify genetic variants that underlie canine phenotypes is ushering into focus novel biological mechanisms that make dogs remarkable. Ironically, the very practices responsible for breed formation also spurned morbidity; today, many diseases are correlated with breed identity. In this review, we discuss man's best friend in the context of a genetic model to understand paradigms of heritable phenotypes, both desirable and disadvantageous.

A regulatory variant impacting TBX1 expression contributes to basicranial morphology in Homo sapiens.

Changes in gene regulatory elements play critical roles in human phenotypic divergence. However, identifying the base-pair changes responsible for the distinctive morphology of Homo sapiens remains challenging. Here, we report a noncoding single-nucleotide polymorphism (SNP), rs41298798, as a potential causal variant contributing to the morphology of the skull base and vertebral structures found in Homo sapiens. Screening for differentially regulated genes between Homo sapiens and extinct relatives revealed 13 candidate genes associated with basicranial development, with TBX1, implicated in DiGeorge syndrome, playing a pivotal role. Epigenetic markers and in silico analyses prioritized rs41298798 within a TBX1 intron for functional validation. CRISPR editing revealed that the 41-base-pair region surrounding rs41298798 modulates gene expression at 22q11.21. The derived allele of rs41298798 acts as an allele-specific enhancer mediated by E2F1, resulting in increased TBX1 expression levels compared to the ancestral allele. Tbx1-knockout mice exhibited skull base and vertebral abnormalities similar to those seen in DiGeorge syndrome. Phenotypic differences associated with TBX1 deficiency are observed between Homo sapiens and Neanderthals (Homo neanderthalensis). In conclusion, the regulatory divergence of TBX1 contributes to the formation of skull base and vertebral structures found in Homo sapiens.

A Triassic stem lepidosaur illuminates the origin of lizard-like reptiles.

The early evolution of diapsid reptiles is marked by a deep contrast between our knowledge of the origin and early evolution of archosauromorphs (crocodiles, avian and non-avian dinosaurs) to that of lepidosauromorphs (squamates (lizards, snakes) and sphenodontians (tuataras)). Whereas the former include hundreds of fossil species across various lineages during the Triassic period1, the latter are represented by an extremely patchy early fossil record comprising only a handful of fragmentary fossils, most of which have uncertain phylogenetic affinities and are confined to Europe1-3. Here we report the discovery of a three-dimensionally preserved reptile skull, assigned as Taytalura alcoberi gen. et sp. nov., from the Late Triassic epoch of Argentina that is robustly inferred phylogenetically as the earliest evolving lepidosauromorph, using various data types and optimality criteria. Micro-computed tomography scans of this skull reveal details about the origin of the lepidosaurian skull from early diapsids, suggesting that several traits traditionally associated with sphenodontians in fact originated much earlier in lepidosauromorph evolution. Taytalura suggests that the strongly evolutionarily conserved skull architecture of sphenodontians represents the plesiomorphic condition for all lepidosaurs, that stem and crown lepidosaurs were contemporaries for at least ten million years during the Triassic, and that early lepidosauromorphs had a much broader geographical distribution than has previously been thought.

Effect of skull morphology on fox snow diving.

Certain fox species plunge-dive into snow to catch prey (e.g., rodents), a hunting mechanism called mousing. Red and arctic foxes can dive into snow at speeds ranging between 2 and 4 m/s. Such mousing behavior is facilitated by a slim, narrow facial structure. Here, we investigate how foxes dive into snow efficiently by studying the role of skull morphology on impact forces it experiences. In this study, we reproduce the mousing behavior in the lab using three-dimensional (3D) printed fox skulls dropped into fresh snow to quantify the dynamic force of impact. Impact force into snow is modeled using hydrodynamic added mass during the initial impact phase. This approach is based on two key facts: the added mass effect in granular media at high Reynolds numbers and the characteristics of snow as a granular medium. Our results show that the curvature of the snout plays a critical role in determining the impact force, with an inverse relationship. A sharper skull leads to a lower average impact force, which allows foxes to dive head-first into the snow with minimal tissue damage.

Skeleton of a Cretaceous mammal from Madagascar reflects long-term insularity.

The fossil record of mammaliaforms (mammals and their closest relatives) of the Mesozoic era from the southern supercontinent Gondwana is far less extensive than that from its northern counterpart, Laurasia1,2. Among Mesozoic mammaliaforms, Gondwanatheria is one of the most poorly known clades, previously represented by only a single cranium and isolated jaws and teeth1-5. As a result, the anatomy, palaeobiology and phylogenetic relationships of gondwanatherians remain unclear. Here we report the discovery of an articulated and very well-preserved skeleton of a gondwanatherian of the latest age (72.1-66 million years ago) of the Cretaceous period from Madagascar that we assign to a new genus and species, Adalatherium hui. To our knowledge, the specimen is the most complete skeleton of a Gondwanan Mesozoic mammaliaform that has been found, and includes the only postcranial material and ascending ramus of the dentary known for any gondwanatherian. A phylogenetic analysis including the new taxon recovers Gondwanatheria as the sister group to Multituberculata. The skeleton, which represents one of the largest of the Gondwanan Mesozoic mammaliaforms, is particularly notable for exhibiting many unique features in combination with features that are convergent on those of therian mammals. This uniqueness is consistent with a lineage history for A. hui of isolation on Madagascar for more than 20 million years.

Late Cretaceous neornithine from Europe illuminates the origins of crown birds.

Our understanding of the earliest stages of crown bird evolution is hindered by an exceedingly sparse avian fossil record from the Mesozoic era. The most ancient phylogenetic divergences among crown birds are known to have occurred in the Cretaceous period1-3, but stem-lineage representatives of the deepest subclades of crown birds-Palaeognathae (ostriches and kin), Galloanserae (landfowl and waterfowl) and Neoaves (all other extant birds)-are unknown from the Mesozoic era. As a result, key questions related to the ecology4,5, biogeography3,6,7 and divergence times1,8-10 of ancestral crown birds remain unanswered. Here we report a new Mesozoic fossil that occupies a position close to the last common ancestor of Galloanserae and fills a key phylogenetic gap in the early evolutionary history of crown birds10,11. Asteriornis maastrichtensis, gen. et sp. nov., from the Maastrichtian age of Belgium (66.8-66.7 million years ago), is represented by a nearly complete, three-dimensionally preserved skull and associated postcranial elements. The fossil represents one of the only well-supported crown birds from the Mesozoic era12, and is the first Mesozoic crown bird with well-represented cranial remains. Asteriornis maastrichtensis exhibits a previously undocumented combination of galliform (landfowl)-like and anseriform (waterfowl)-like features, and its presence alongside a previously reported Ichthyornis-like taxon from the same locality13 provides direct evidence of the co-occurrence of crown birds and avialan stem birds. Its occurrence in the Northern Hemisphere challenges biogeographical hypotheses of a Gondwanan origin of crown birds3, and its relatively small size and possible littoral ecology may corroborate proposed ecological filters4,5,9 that influenced the persistence of crown birds through the end-Cretaceous mass extinction.

Enigmatic dinosaur precursors bridge the gap to the origin of Pterosauria.

Pterosaurs were the first vertebrates to evolve powered flight1 and comprised one of the main evolutionary radiations in terrestrial ecosystems of the Mesozoic era (approximately 252-66 million years ago), but their origin has remained an unresolved enigma in palaeontology since the nineteenth century2-4. These flying reptiles have been hypothesized to be the close relatives of a wide variety of reptilian clades, including dinosaur relatives2-8, and there is still a major morphological gap between those forms and the oldest, unambiguous pterosaurs from the Upper Triassic series. Here, using recent discoveries of well-preserved cranial remains, microcomputed tomography scans of fragile skull bones (jaws, skull roofs and braincases) and reliably associated postcrania, we demonstrate that lagerpetids-a group of cursorial, non-volant dinosaur precursors-are the sister group of pterosaurs, sharing numerous synapomorphies across the entire skeleton. This finding substantially shortens the temporal and morphological gap between the oldest pterosaurs and their closest relatives and simultaneously strengthens the evidence that pterosaurs belong to the avian line of archosaurs. Neuroanatomical features related to the enhanced sensory abilities of pterosaurs9 are already present in lagerpetids, which indicates that these features evolved before flight. Our evidence illuminates the first steps of the assembly of the pterosaur body plan, whose conquest of aerial space represents a remarkable morphofunctional innovation in vertebrate evolution.

Evidence for high-performance suction feeding in the Pennsylvanian stem-group holocephalan Iniopera.

The Carboniferous (358.9 to 298.9 Ma) saw the emergence of marine ecosystems dominated by modern vertebrate groups, including abundant stem-group holocephalans (chimaeras and relatives). Compared with the handful of anatomically conservative holocephalan genera alive today-demersal durophages all-these animals were astonishingly morphologically diverse, and bizarre anatomies in groups such as iniopterygians hint at specialized ecological roles foreshadowing those of the later, suction-feeding neopterygians. However, flattened fossils usually obscure these animals' functional morphologies and how they fitted into these important early ecosystems. Here, we use three-dimensional (3D) methods to show that the musculoskeletal anatomy of the uniquely 3D-preserved iniopterygian Iniopera can be best interpreted as being similar to that of living holocephalans rather than elasmobranchs but that it was mechanically unsuited to durophagy. Rather, Iniopera had a small, anteriorly oriented mouth aperture, expandable pharynx, and strong muscular links among the pectoral girdle, neurocranium, and ventral pharynx consistent with high-performance suction feeding, something exhibited by no living holocephalan and never clearly characterized in any of the extinct members of the holocephalan stem-group. Remarkably, in adapting a distinctly holocephalan anatomy to suction feeding, Iniopera is more comparable to modern tetrapod suction feeders than to the more closely related high-performance suction-feeding elasmobranchs. This raises questions about the assumed role of durophagy in the evolution of holocephalans' distinctive anatomy and offers a rare glimpse into the breadth of ecological niches filled by holocephalans in a pre-neopterygian world.

The reconstructed cranium of Pierolapithecus and the evolution of the great ape face.

Pierolapithecus catalaunicus (~12 million years ago, northeastern Spain) is key to understanding the mosaic nature of hominid (great ape and human) evolution. Notably, its skeleton indicates that an orthograde (upright) body plan preceded suspensory adaptations in hominid evolution. However, there is ongoing debate about this species, partly because the sole known cranium, preserving a nearly complete face, suffers from taphonomic damage. We 1) carried out a micro computerized tomography (CT) based virtual reconstruction of the Pierolapithecus cranium, 2) assessed its morphological affinities using a series of two-dimensional (2D) and three-dimensional (3D) morphometric analyses, and 3) modeled the evolution of key aspects of ape face form. The reconstruction clarifies many aspects of the facial morphology of Pierolapithecus. Our results indicate that it is most similar to great apes (fossil and extant) in overall face shape and size and is morphologically distinct from other Middle Miocene apes. Crown great apes can be distinguished from other taxa in several facial metrics (e.g., low midfacial prognathism, relatively tall faces) and only some of these features are found in Pierolapithecus, which is most consistent with a stem (basal) hominid position. The inferred morphology at all ancestral nodes within the hominoid (ape and human) tree is closer to great apes than to hylobatids (gibbons and siamangs), which are convergent with other smaller anthropoids. Our analyses support a hominid ancestor that was distinct from all extant and fossil hominids in overall facial shape and shared many features with Pierolapithecus. This reconstructed ancestral morphotype represents a testable hypothesis that can be reevaluated as new fossils are discovered.

Age and context of mid-Pliocene hominin cranium from Woranso-Mille, Ethiopia.

A fossil hominin cranium was discovered in mid-Pliocene deltaic strata in the Godaya Valley of the northwestern Woranso-Mille study area in Ethiopia. Here we show that analyses of chemically correlated volcanic layers and the palaeomagnetic stratigraphy, combined with Bayesian modelling of dated tuffs, yield an age range of 3.804 ± 0.013 to 3.777 ± 0.014 million years old (mean ± 1σ) for the deltaic strata and the fossils that they contain. We also document deposits of a perennial lake beneath the deltaic sequence. Mammalian fossils associated with the cranium represent taxa that were widespread at the time and data from botanical remains indicate that the vegetation in the lake and delta catchment was predominantly dry shrubland with varying proportions of grassland, wetland and riparian forest. In addition, we report high rates of sediment accumulation and depositional features that are typical of a steep topographic relief and differ from younger Woranso-Mille fossil localities, reflecting the influence of active rift processes on the palaeolandscape.

Apidima Cave fossils provide earliest evidence of Homo sapiens in Eurasia.

Two fossilized human crania (Apidima 1 and Apidima 2) from Apidima Cave, southern Greece, were discovered in the late 1970s but have remained enigmatic owing to their incomplete nature, taphonomic distortion and lack of archaeological context and chronology. Here we virtually reconstruct both crania, provide detailed comparative descriptions and analyses, and date them using U-series radiometric methods. Apidima 2 dates to more than 170 thousand years ago and has a Neanderthal-like morphological pattern. By contrast, Apidima 1 dates to more than 210 thousand years ago and presents a mixture of modern human and primitive features. These results suggest that two late Middle Pleistocene human groups were present at this site-an early Homo sapiens population, followed by a Neanderthal population. Our findings support multiple dispersals of early modern humans out of Africa, and highlight the complex demographic processes that characterized Pleistocene human evolution and modern human presence in southeast Europe.

A 3.8-million-year-old hominin cranium from Woranso-Mille, Ethiopia.

The cranial morphology of the earliest known hominins in the genus Australopithecus remains unclear. The oldest species in this genus (Australopithecus anamensis, specimens of which have been dated to 4.2-3.9 million years ago) is known primarily from jaws and teeth, whereas younger species (dated to 3.5-2.0 million years ago) are typically represented by multiple skulls. Here we describe a nearly complete hominin cranium from Woranso-Mille (Ethiopia) that we date to 3.8 million years ago. We assign this cranium to A. anamensis on the basis of the taxonomically and phylogenetically informative morphology of the canine, maxilla and temporal bone. This specimen thus provides the first glimpse of the entire craniofacial morphology of the earliest known members of the genus Australopithecus. We further demonstrate that A. anamensis and Australopithecus afarensis differ more than previously recognized and that these two species overlapped for at least 100,000 years-contradicting the widely accepted hypothesis of anagenesis.