Inner ear biomechanics reveals a Late Triassic origin for mammalian endothermy.

Endothermy underpins the ecological dominance of mammals and birds in diverse environmental settings1,2. However, it is unclear when this crucial feature emerged during mammalian evolutionary history, as most of the fossil evidence is ambiguous3-17. Here we show that this key evolutionary transition can be investigated using the morphology of the endolymph-filled semicircular ducts of the inner ear, which monitor head rotations and are essential for motor coordination, navigation and spatial awareness18-22. Increased body temperatures during the ectotherm-endotherm transition of mammal ancestors would decrease endolymph viscosity, negatively affecting semicircular duct biomechanics23,24, while simultaneously increasing behavioural activity25,26 probably required improved performance27. Morphological changes to the membranous ducts and enclosing bony canals would have been necessary to maintain optimal functionality during this transition. To track these morphofunctional changes in 56 extinct synapsid species, we developed the thermo-motility index, a proxy based on bony canal morphology. The results suggest that endothermy evolved abruptly during the Late Triassic period in Mammaliamorpha, correlated with a sharp increase in body temperature (5-9 °C) and an expansion of aerobic and anaerobic capacities. Contrary to previous suggestions3-14, all stem mammaliamorphs were most probably ectotherms. Endothermy, as a crucial physiological characteristic, joins other distinctive mammalian features that arose during this period of climatic instability28.

Author Correction: New infant cranium from the African Miocene sheds light on ape evolution.

An amendment to this paper has been published and can be accessed via a link at the top of the paper.

Maxillary morphology of chimpanzees: Captive versus wild environments.

Morphological studies typically avoid using osteological samples that derive from captive animals because it is assumed that their morphology is not representative of wild populations. Rearing environments indeed differ between wild and captive individuals. For example, mechanical properties of the diets provided to captive animals can be drastically different from the food present in their natural habitats, which could impact cranial morphology and dental health. Here, we examine morphological differences in the maxillae of wild versus captive chimpanzees (Pan troglodytes) given the prominence of this species in comparative samples used in human evolution research and the key role of the maxilla in such studies. Size and shape were analysed using three-dimensional geometric morphometric methods based on computed tomography scans of 94 wild and 30 captive specimens. Captive individuals have on average larger and more asymmetrical maxillae than wild chimpanzees, and significant differences are present in their maxillary shapes. A large proportion of these shape differences are attributable to static allometry, but wild and captive specimens still differ significantly from each other after allometric size adjustment of the shape data. Levels of shape variation are higher in the captive group, while the degree of size variation is likely similar in our two samples. Results are discussed in the context of ontogenetic growth trajectories, changes in dietary texture, an altered social environment, and generational differences. Additionally, sample simulations show that size and shape differences between chimpanzees and bonobos (Pan paniscus) are exaggerated when part of the wild sample is replaced with captive chimpanzees. Overall, this study confirms that maxillae of captive chimpanzees should not be included in morphological or taxonomic analyses when the objective is to characterise the species.

Naming Homo erectus: A review.

Following the discovery of hominin fossils at Trinil (Java, Indonesia) in 1891 and 1892, Eugène Dubois named a new species, now known as Homo erectus. Although the main historical events are well-known, there appears to be no consensus regarding two important aspects of the naming of the species, including what constitutes the original publication of the name, and what is the name-bearing type specimen. These issues are addressed in this paper with reference to original sources and the International Code of Zoological Nomenclature. Our review confirms earlier studies that cite the published quarterly fieldwork report covering the 3rd quarter of 1892 as the original publication naming the species erectus. However, until recently, the correct publication year of 1893 has consistently been cited as 1892, and it has rarely been recognized that the author of the publication was anonymous, even though the author of the species is specifically named. Importantly, Dubois assigns all three hominin fossils found at Trinil up to that moment to the new species, explicitly stating that they belong to a single individual. The three fossils, a molar, a calotte, and a femur, therefore jointly constitute the original holotype. However, the femur most likely derives from younger strata than the other hominins and shows fully modern human-like morphology, unlike subsequently discovered H. erectus femora. Moreover, there is no consensus over the affinities of the molar, and if it is H. erectus rather than an extinct ape, there is no evidence that it belongs to the same individual as the calotte. Excluding these two fossils from the holotype, the calotte is the appropriate fossil to retain the role as name-bearing specimen.

New infant cranium from the African Miocene sheds light on ape evolution.

The evolutionary history of extant hominoids (humans and apes) remains poorly understood. The African fossil record during the crucial time period, the Miocene epoch, largely comprises isolated jaws and teeth, and little is known about ape cranial evolution. Here we report on the, to our knowledge, most complete fossil ape cranium yet described, recovered from the 13 million-year-old Middle Miocene site of Napudet, Kenya. The infant specimen, KNM-NP 59050, is assigned to a new species of Nyanzapithecus on the basis of its unerupted permanent teeth, visualized by synchrotron imaging. Its ear canal has a fully ossified tubular ectotympanic, a derived feature linking the species with crown catarrhines. Although it resembles some hylobatids in aspects of its morphology and dental development, it possesses no definitive hylobatid synapomorphies. The combined evidence suggests that nyanzapithecines were stem hominoids close to the origin of extant apes, and that hylobatid-like facial features evolved multiple times during catarrhine evolution.

Morphological variation of the maxilla in modern humans and African apes.

Differences in morphology among modern humans and African apes are frequently used when assessing whether hominin fossils should be attributed to a single species or represent evidence for taxic diversity. A good understanding of the degree and structure of the intergeneric, interspecific, and intraspecific variation, including aspects such as sexual dimorphism and age, are key in this context. Here we explore the variation and differences shown by the maxilla of extant hominines, as maxillary morphology is central in the diagnosis of several hominin taxa. Our sample includes adults of all currently recognized hominine species and subspecies, with a balanced species sex ratio. In addition, we compared the adults with a small sample of late juveniles. The morphology of the maxillae was captured using three-dimensional landmarks, and the size and shape were analyzed using geometric morphometric methods. Key observations are that 1) the maxillae of all extant hominine species and subspecies show statistically significant differences, but complete separation in shape is only seen at the genus level; 2) the degree of variation is not consistent between genera, with subspecies of Gorilla being more different from each other than are species of Pan; 3) the pattern of sexual shape dimorphism is different in Pan, Gorilla, and Homo, often showing opposite trends; and 4) differentiation between maxillary shapes is increased after adjustment for static intraspecific allometry. These results provide a taxonomically up-to-date comparative morphological framework to help interpret the hominin fossil record, and we discuss the practical implications in that context.

Reconstructed Homo habilis type OH 7 suggests deep-rooted species diversity in early Homo.

Besides Homo erectus (sensu lato), the eastern African fossil record of early Homo has been interpreted as representing either a single variable species, Homo habilis, or two species. In the latter case, however, there is no consensus over the respective groupings, and which of the two includes OH 7, the 1.8-million-year-old H. habilis holotype. This partial skull and hand from Olduvai Gorge remains pivotal to evaluating the early evolution of the Homo lineage, and by priority names one or other of the two taxa. However, the distorted preservation of the diagnostically important OH 7 mandible has hindered attempts to compare this specimen with other fossils. Here we present a virtual reconstruction of the OH 7 mandible, and compare it to other early Homo fossils. The reconstructed mandible is remarkably primitive, with a long and narrow dental arcade more similar to Australopithecus afarensis than to the derived parabolic arcades of Homo sapiens or H. erectus. We find that this shape variability is not consistent with a single species of early Homo. Importantly, the jaw morphology of OH 7 is incompatible with fossils assigned to Homo rudolfensis and with the A.L. 666-1 Homo maxilla. The latter is morphologically more derived than OH 7 but 500,000 years older, suggesting that the H. habilis lineage originated before 2.3 million years ago, thus marking deep-rooted species diversity in the genus Homo. We also reconstructed the parietal bones of OH 7 and estimated its endocranial volume. At between 729 and 824 ml it is larger than any previously published value, and emphasizes the near-complete overlap in brain size among species of early Homo. Our results clarify the H. habilis hypodigm, but raise questions about its phylogenetic relationships. Differences between species of early Homo appear to be characterized more by gnathic diversity than by differences in brain size, which was highly variable within all taxa.

Hominin dental remains from the Pliocene localities at Lomekwi, Kenya (1982-2009).

Increasing evidence for both taxonomic diversity and early stone manufacture during the Pliocene highlights the importance of the hominin fossil record from this epoch in eastern Africa. Here, we describe dental remains from Lomekwi (West Turkana, Kenya), which date from between 3.2 and 3.5 Ma. The sample was collected between 1982 and 2009 and includes five gnathic specimens and a total of 67 teeth (mostly isolated permanent postcanine teeth). Standard linear dimensions indicate that, although the Lomekwi teeth are relatively small, there is broad overlap in size with contemporary Australopithecus afarensis and Australopithecus deyiremeda specimens at most tooth positions. However, some dental characters differentiate this sample from these species, including a relatively large P4 and M3 compared with the M1, a high incidence of well-developed protostylids, and specific accessory molar cuspules. Owing to a lack of well-preserved tooth crowns (and the complete absence of mandibular teeth) in the holotype and paratype of Kenyanthropus platyops, and limited comparable gnathic morphology in the new specimens, it cannot be determined whether these Lomekwi specimens should be attributed to this species. Attribution of these specimens is further complicated by a lack of certainty about position along the tooth row of many of the molar specimens. More comprehensive shape analyses of the external and internal morphology of these specimens, and additional fossil finds, would facilitate the taxonomic attribution of specimens in this taxonomically diverse period of human evolution.

Thoracic vertebral count and thoracolumbar transition in Australopithecus afarensis.

The evolution of the human pattern of axial segmentation has been the focus of considerable discussion in paleoanthropology. Although several complete lumbar vertebral columns are known for early hominins, to date, no complete cervical or thoracic series has been recovered. Several partial skeletons have revealed that the thoracolumbar transition in early hominins differed from that of most extant apes and humans. Australopithecus africanus, Australopithecus sediba, and Homo erectus all had zygapophyseal facets that shift from thoracic-like to lumbar-like at the penultimate rib-bearing level, rather than the ultimate rib-bearing level, as in most humans and extant African apes. What has not been clear is whether Australopithecus had 12 thoracic vertebrae as in most humans, or 13 as in most African apes, and where the position of the thoracolumbar transitional element was. The discovery, preparation, and synchrotron scanning of the Australopithecus afarensis partial skeleton DIK-1-1, from Dikika, Ethiopia, provides the only known complete hominin cervical and thoracic vertebral column before 60,000 years ago. DIK-1-1 is the only known Australopithecus skeleton to preserve all seven cervical vertebrae and provides evidence for 12 thoracic vertebrae with a transition in facet morphology at the 11th thoracic level. The location of this transition, one segment cranial to the ultimate rib-bearing vertebra, also occurs in all other early hominins and is higher than in most humans or extant apes. At 3.3 million years ago, the DIK-1-1 skeleton is the earliest example of this distinctive and unusual pattern of axial segmentation.

Morphological trends in arcade shape and size in Middle Pleistocene Homo.

OBJECTIVES: Middle Pleistocene fossil hominins, often summarized as Homo heidelbergensis sensu lato, are difficult to interpret due to a fragmentary fossil record and ambiguous combinations of primitive and derived characters. Here, we focus on one aspect of facial shape and analyze shape variation of the dental arcades of these fossils together with other Homo individuals. MATERIALS AND METHODS: Three-dimensional landmark data were collected on computed tomographic scans and surface scans of Middle Pleistocene fossil hominins (n = 8), Homo erectus s.l. (n = 4), Homo antecessor (n = 1), Homo neanderthalensis (n = 13), recent (n = 52) and fossil (n = 19) Homo sapiens. To increase sample size, we used multiple multivariate regression to reconstruct complementary arches for isolated mandibles, and explored size and shape differences among maxillary arcades. RESULTS: The shape of the dental arcade in H. erectus s.l. and H. antecessor differs markedly from both Neanderthals and H. sapiens. The latter two show subtle but consistent differences in arcade length and width. Shape variation among Middle Pleistocene fossil hominins does not exceed the amount of variation of other species, but includes individuals with more primitive and more derived morphology, all more similar to Neanderthals and H. sapiens than to H. erectus s.l. DISCUSSION: Although our results cannot reject the hypothesis that the Middle Pleistocene fossil hominins belong to a single species, their shape variation comprises a more primitive morph that represents a likely candidate for the shape of the last common ancestor of Neanderthals and H. sapiens, and a more derived morph resembling Neanderthals. The arcade shape difference between Neanderthals and H. sapiens might be related to different ways to withstand mechanical stress.

Morphology and function of Neandertal and modern human ear ossicles.

The diminutive middle ear ossicles (malleus, incus, stapes) housed in the tympanic cavity of the temporal bone play an important role in audition. The few known ossicles of Neandertals are distinctly different from those of anatomically modern humans (AMHs), despite the close relationship between both human species. Although not mutually exclusive, these differences may affect hearing capacity or could reflect covariation with the surrounding temporal bone. Until now, detailed comparisons were hampered by the small sample of Neandertal ossicles and the unavailability of methods combining analyses of ossicles with surrounding structures. Here, we present an analysis of the largest sample of Neandertal ossicles to date, including many previously unknown specimens, covering a wide geographic and temporal range. Microcomputed tomography scans and 3D geometric morphometrics were used to quantify shape and functional properties of the ossicles and the tympanic cavity and make comparisons with recent and extinct AMHs as well as African apes. We find striking morphological differences between ossicles of AMHs and Neandertals. Ossicles of both Neandertals and AMHs appear derived compared with the inferred ancestral morphology, albeit in different ways. Brain size increase evolved separately in AMHs and Neandertals, leading to differences in the tympanic cavity and, consequently, the shape and spatial configuration of the ossicles. Despite these different evolutionary trajectories, functional properties of the middle ear of AMHs and Neandertals are largely similar. The relevance of these functionally equivalent solutions is likely to conserve a similar auditory sensitivity level inherited from their last common ancestor.

Using the covariation of extant hominoid upper and lower jaws to predict dental arcades of extinct hominins.

Upper and lower jaws are well represented in the fossil record of mammals and are frequently used to diagnose species. Some hominin species are only known by either their maxillary or mandibular morphology, and in this study, we explore the possibility of predicting their complementary dental arcade shape to aid the recognition of conspecific specimens in the fossil record. To this end, we apply multiple multivariate regression to analyze 3D landmark coordinates collected on associated upper and lower dental arcades of extant Homo, Pan, Gorilla, Pongo, and Hylobates. We first study the extant patterns of variation in dental arcade shape and quantify how accurate predictions of complementary arcades are. Then we explore applications of this extant framework for interpreting the fossil record based on two fossil hominin specimens with associated upper and lower jaws, KNM-WT 15000 (Homo erectus sensu lato) and Sts 52 (Australopithecus africanus), as well as two non-associated specimens of Paranthropus boisei, the maxilla of OH 5 and the Peninj mandible. We find that the shape differences between the predictions and the original fossil specimens are in the range of variation within genera or species and therefore are consistent with their known affinity. Our approach can provide a reference against which intraspecific variation of extinct species can be assessed. We show that our method predicts arcade shapes reliably even if the target shape is not represented in the reference sample. We find that in extant hominoids, the amount of within-taxon variation in dental arcade shape often overlaps with the amount of between-taxon shape variation. This implies that whereas a large difference in dental arcade shape between two individuals typically suggests that they belong to different species or even genera, a small shape difference does not necessarily imply conspecificity.

Reconstruction, endocranial form and taxonomic affinity of the early Homo calvaria KNM-ER 42700.

When first described, the small calvaria KNM-ER 42700 from Ileret, Kenya, was considered a late juvenile or young adult and assigned to Homo erectus. However, this species attribution has subsequently been challenged because the specimen's neurocranial shape differs substantially from that of H. erectus adults. Here, (1) we describe the postmortem damage and deformation that could have influenced previous shape analyses, (2) present digital reconstructions based on computed tomographic scans correcting for these taphonomic defects, and (3) analyze the reconstructed endocranial shape and form, considering both static allometry among adults and ontogenetic allometry. To this end, we use geometric morphometrics to analyze the shape of digital endocasts based on landmarks and semilandmarks. Corroborating previous studies of the external surface, we find that the endocranial shape of KNM-ER 42700 falls outside the known adult variation of H. erectus. With an endocranial volume estimate between 721 and 744 ml, size cannot explain its atypical endocranial shape when static allometry within H. erectus is considered. However, the analysis of ontogenetic allometry suggests that it may be a H. erectus individual that is younger than previously thought and had not yet reached adult endocranial shape. Future work should therefore comprehensively review all cranial indicators of its developmental age, including closure of the spheno-occipital synchondrosis. An alternative hypothesis is that KNM-ER 42700 represents an as yet unidentified species of early Homo. Importantly, KNM-ER 42700 should not be included in the adult hypodigm of H. erectus.

New fossils from Koobi Fora in northern Kenya confirm taxonomic diversity in early Homo.

Since its discovery in 1972 (ref. 1), the cranium KNM-ER 1470 has been at the centre of the debate over the number of species of early Homo present in the early Pleistocene epoch of eastern Africa. KNM-ER 1470 stands out among other specimens attributed to early Homo because of its larger size, and its flat and subnasally orthognathic face with anteriorly placed maxillary zygomatic roots. This singular morphology and the incomplete preservation of the fossil have led to different views as to whether KNM-ER 1470 can be accommodated within a single species of early Homo that is highly variable because of sexual, geographical and temporal factors, or whether it provides evidence of species diversity marked by differences in cranial size and facial or masticatory adaptation. Here we report on three newly discovered fossils, aged between 1.78 and 1.95 million years (Myr) old, that clarify the anatomy and taxonomic status of KNM-ER 1470. KNM-ER 62000, a well-preserved face of a late juvenile hominin, closely resembles KNM-ER 1470 but is notably smaller. It preserves previously unknown morphology, including moderately sized, mesiodistally long postcanine teeth. The nearly complete mandible KNM-ER 60000 and mandibular fragment KNM-ER 62003 have a dental arcade that is short anteroposteriorly and flat across the front, with small incisors; these features are consistent with the arcade morphology of KNM-ER 1470 and KNM-ER 62000. The new fossils confirm the presence of two contemporary species of early Homo, in addition to Homo erectus, in the early Pleistocene of eastern Africa.

Late Pleistocene age and archaeological context for the hominin calvaria from GvJm-22 (Lukenya Hill, Kenya).

Kenya National Museums Lukenya Hill Hominid 1 (KNM-LH 1) is a Homo sapiens partial calvaria from site GvJm-22 at Lukenya Hill, Kenya, associated with Later Stone Age (LSA) archaeological deposits. KNM-LH 1 is securely dated to the Late Pleistocene, and samples a time and region important for understanding the origins of modern human diversity. A revised chronology based on 26 accelerator mass spectrometry radiocarbon dates on ostrich eggshells indicates an age range of 23,576-22,887 y B.P. for KNM-LH 1, confirming prior attribution to the Last Glacial Maximum. Additional dates extend the maximum age for archaeological deposits at GvJm-22 to >46,000 y B.P. (>46 kya). These dates are consistent with new analyses identifying both Middle Stone Age and LSA lithic technologies at the site, making GvJm-22 a rare eastern African record of major human behavioral shifts during the Late Pleistocene. Comparative morphometric analyses of the KNM-LH 1 cranium document the temporal and spatial complexity of early modern human morphological variability. Features of cranial shape distinguish KNM-LH 1 and other Middle and Late Pleistocene African fossils from crania of recent Africans and samples from Holocene LSA and European Upper Paleolithic sites.

Hominoid arcade shape: Pattern and magnitude of covariation.

The shape of the dental arcade and canine size distinguish extant humans from all apes. Humans are characterized by a parabolic arcade with short postcanine tooth rows and small canines, whereas apes have long, U-shaped arcades with large canines. The evolutionary and biomechanical mechanisms underlying arcade shape differences between and within groups are not well understood. It is unclear, for example, whether evolutionary changes in the covariation among modules comprising the upper and lower jaws are the cause and/or consequence of different arcade shapes. Here we use 3D geometric morphometric methods to explore to what extent the morphological differences in arcade shape between living hominoids are related to differences in covariation of upper and lower jaws, and the premaxilla and the maxilla. We show that all extant hominoids follow a very similar covariation pattern between upper and lower dental arcades, as well as between the premaxilla and the maxilla. We find comparably high magnitudes of covariation between the premaxilla and the maxilla in all groups. Between the upper and lower jaws, levels of covariation are similar in apes (Pan, Gorilla, Pongo, and Hylobates), but overall lower in extant humans. Our results demonstrate an independence of the pattern of arcade shape covariation from dental spatial arrangements. Importantly, we show that a shared hominoid pattern of covariation between premaxilla and maxilla together with the covariation of upper and lower jaw is consistent with major evolutionary arcade shape changes in hominoids. We suggest that with the reduction of canine and diastema size in hominins, the incisors move posteriorly and the tooth row becomes more parabolic. Our study provides a framework for addressing questions about fossil hominin dentognathic diversity, including inter- and intraspecific variation and associations of upper and lower jaw morphology.

Direct radiocarbon dating and DNA analysis of the Darra-i-Kur (Afghanistan) human temporal bone.

The temporal bone discovered in the 1960s from the Darra-i-Kur cave in Afghanistan is often cited as one of the very few Pleistocene human fossils from Central Asia. Here we report the first direct radiocarbon date for the specimen and the genetic analyses of DNA extracted and sequenced from two areas of the bone. The new radiocarbon determination places the find to ∼4500 cal BP (∼2500 BCE) contradicting an assumed Palaeolithic age of ∼30,000 years, as originally suggested. The DNA retrieved from the specimen originates from a male individual who carried mitochondrial DNA of the modern human type. The petrous part yielded more endogenous ancient DNA molecules than the squamous part of the same bone. Molecular dating of the Darra-i-Kur mitochondrial DNA sequence corroborates the radiocarbon date and suggests that the specimen is younger than previously thought. Taken together, the results consolidate the fact that the human bone is not associated with the Pleistocene-age deposits of Darra-i-Kur; instead it is intrusive, possibly re-deposited from upper levels dating to much later periods (Neolithic). Despite its Holocene age, the Darra-i-Kur specimen is, so far, the first and only ancient human from Afghanistan whose DNA has been sequenced.

Comparative anatomy of the middle ear ossicles of extant hominids--Introducing a geometric morphometric protocol.

The presence of three interconnected auditory ossicles in the middle ear is a defining characteristic of mammals, and aspects of ossicle morphology are related to hearing sensitivity. However, analysis and comparison of ossicles are complicated by their minute size and complex three-dimensional shapes. Here we introduce a geometric morphometric measurement protocol for 3D shape analysis based on landmarks and semilandmarks obtained from µCT images and apply it to ossicles of extant hominids (great apes and humans). We show that the protocol is reliable and reproducible over a range of voxel resolutions, and captures even subtle shape differences. Using this approach it is possible to distinguish the hominid taxa by mean shapes of their malleus and incus (p < 0.01). The stapes appears less diagnostic, although this may in part be related to the small sample size available. Using ancestral state estimation, we show that, within hominids, Homo sapiens is derived with respect to its malleus (short manubrium, long corpus, head anterior-posterior flattened, articular facet shape), incus (wide intercrural curvature, long incudal processes, articular facet shape) and stapes (high stapes with kidney-shaped footplate). H. sapiens also shows a number of plesiomorphic shape traits whereas Gorilla and Pan possess a number of autapomorphic characteristics. The Pongo ossicles appear to be close to the plesiomorphic hominid condition. The malleus shows little difference in size among hominids, and allometry is thus of little importance. In contrast, the incus and stapes are more variable in size, and their shape is more strongly related to size differences. Although the form-function relationships in the middle ear are not fully understood, some aspects of ossicle morphology suggest that interspecific differences in hearing capacities are present among hominids. Finally, the results of this study provide a comparative framework for morphometric studies analyzing ossicles of extinct hominids, with a bearing on taxonomy, phylogeny and auditory function.