Auditory thresholds compatible with optimal speech reception likely evolved before the human-chimpanzee split.

The anatomy of the auditory region of fossil hominins may shed light on the emergence of human spoken language. Humans differ from other great apes in several features of the external, middle and inner ear (e.g., short external ear canal, small tympanic membrane, large oval window). However, the functional implications of these differences remain poorly understood as comparative audiometric data from great apes are scarce and conflicting. Here, we measure the sound transfer function of the external and middle ears of humans, chimpanzees and bonobos, using laser-Doppler vibrometry and finite element analysis. This sound transfer function affects auditory thresholds, which relate to speech reception thresholds in humans. Unexpectedly we find that external and middle ears of chimpanzees and bonobos transfer sound better than human ones in the frequency range of spoken language. Our results suggest that auditory thresholds of the last common ancestor of Homo and Pan were already compatible with speech reception as observed in humans. Therefore, it seems unlikely that the morphological evolution observed in the bony auditory region of fossil hominins was driven by the emergence of spoken language. Instead, the peculiar human configuration may be a by-product of morpho-functional constraints linked to brain expansion.

Palaeogenomics of Upper Palaeolithic to Neolithic European hunter-gatherers.

Modern humans have populated Europe for more than 45,000 years1,2. Our knowledge of the genetic relatedness and structure of ancient hunter-gatherers is however limited, owing to the scarceness and poor molecular preservation of human remains from that period3. Here we analyse 356 ancient hunter-gatherer genomes, including new genomic data for 116 individuals from 14 countries in western and central Eurasia, spanning between 35,000 and 5,000 years ago. We identify a genetic ancestry profile in individuals associated with Upper Palaeolithic Gravettian assemblages from western Europe that is distinct from contemporaneous groups related to this archaeological culture in central and southern Europe4, but resembles that of preceding individuals associated with the Aurignacian culture. This ancestry profile survived during the Last Glacial Maximum (25,000 to 19,000 years ago) in human populations from southwestern Europe associated with the Solutrean culture, and with the following Magdalenian culture that re-expanded northeastward after the Last Glacial Maximum. Conversely, we reveal a genetic turnover in southern Europe suggesting a local replacement of human groups around the time of the Last Glacial Maximum, accompanied by a north-to-south dispersal of populations associated with the Epigravettian culture. From at least 14,000 years ago, an ancestry related to this culture spread from the south across the rest of Europe, largely replacing the Magdalenian-associated gene pool. After a period of limited admixture that spanned the beginning of the Mesolithic, we find genetic interactions between western and eastern European hunter-gatherers, who were also characterized by marked differences in phenotypically relevant variants.

Variations in cochlea shape reveal different evolutionary adaptations in primates and rodents.

The presence of a coiled cochlea is a unique feature of the therian inner ear. While some aspects of the cochlea are already known to affect hearing capacities, the full extent of the relationships between the morphology and function of this organ are not yet understood-especially when the effect of body size differences between species is minimized. Here, focusing on Euarchontoglires, we explore cochlear morphology of 33 species of therian mammals with a restricted body size range. Using µCT scans, 3D models and 3D geometric morphometrics, we obtained shape information of the cochlea and used it to build phylogenetically corrected least square models with 12 hearing variables obtained from the literature. Our results reveal that different taxonomic groups differ significantly in cochlea shape. We further show that these shape differences are related to differences in hearing capacities between these groups, despite of similar cochlear lengths. Most strikingly, rodents with good low-frequency hearing display "tower-shaped" cochleae, achieved by increasing the degree of coiling of their cochlea. In contrast, primates present relatively wider cochleae and relative better high frequency hearing. These results suggest that primates and rodents increased their cochlea lengths through different morpho-evolutionary trajectories.

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.

The earliest Denisovans and their cultural adaptation.

Since the initial identification of the Denisovans a decade ago, only a handful of their physical remains have been discovered. Here we analysed ~3,800 non-diagnostic bone fragments using collagen peptide mass fingerprinting to locate new hominin remains from Denisova Cave (Siberia, Russia). We identified five new hominin bones, four of which contained sufficient DNA for mitochondrial analysis. Three carry mitochondrial DNA of the Denisovan type and one was found to carry mtDNA of the Neanderthal type. The former come from the same archaeological layer near the base of the cave's sequence and are the oldest securely dated evidence of Denisovans at 200 ka (thousand years ago) (205-192 ka at 68.2% or 217-187 ka at 95% probability). The stratigraphic context in which they were located contains a wealth of archaeological material in the form of lithics and faunal remains, allowing us to determine the material culture associated with these early hominins and explore their behavioural and environmental adaptations. The combination of bone collagen fingerprinting and genetic analyses has so far more-than-doubled the number of hominin bones at Denisova Cave and has expanded our understanding of Denisovan and Neanderthal interactions, as well as their archaeological signatures.

A genome sequence from a modern human skull over 45,000 years old from Zlatý kun in Czechia.

Modern humans expanded into Eurasia more than 40,000 years ago following their dispersal out of Africa. These Eurasians carried ~2-3% Neanderthal ancestry in their genomes, originating from admixture with Neanderthals that took place sometime between 50,000 and 60,000 years ago, probably in the Middle East. In Europe, the modern human expansion preceded the disappearance of Neanderthals from the fossil record by 3,000-5,000 years. The genetic makeup of the first Europeans who colonized the continent more than 40,000 years ago remains poorly understood since few specimens have been studied. Here, we analyse a genome generated from the skull of a female individual from Zlatý kun, Czechia. We found that she belonged to a population that appears to have contributed genetically neither to later Europeans nor to Asians. Her genome carries ~3% Neanderthal ancestry, similar to those of other Upper Palaeolithic hunter-gatherers. However, the lengths of the Neanderthal segments are longer than those observed in the currently oldest modern human genome of the ~45,000-year-old Ust'-Ishim individual from Siberia, suggesting that this individual from Zlatý kun is one of the earliest Eurasian inhabitants following the expansion out of Africa.

Comparative micromechanics of bushcricket ears with and without a specialized auditory fovea region in the crista acustica.

In some insects and vertebrate species, the specific enlargement of sensory cell epithelium facilitates the perception of particular behaviourally relevant signals. The insect auditory fovea in the ear of the bushcricket Ancylecha fenestrata (Tettigoniidae: Phaneropterinae) is an example of such an expansion of sensory epithelium. Bushcricket ears developed in convergent evolution anatomical and functional similarities to mammal ears, such as travelling waves and auditory foveae, to process information by sound. As in vertebrate ears, sound induces a motion of this insect hearing organ (crista acustica), which can be characterized by its amplitude and phase response. However, detailed micromechanics in this bushcricket ear with an auditory fovea are yet unknown. Here, we fill this gap in knowledge for bushcricket, by analysing and comparing the ear micromechanics in Ancylecha fenestrata and a bushcricket species without auditory fovea (Mecopoda elongata, Tettigoniidae: Mecopodinae) using laser-Doppler vibrometry. We found that the increased size of the crista acustica, expanded by a foveal region in A. fenestrata, leads to higher mechanical amplitudes and longer phase delays in A. fenestrata male ears. Furthermore, area under curve analyses of the organ oscillations reveal that more sensory units are activated by the same stimuli in the males of the auditory fovea-possessing species A. fenestrata. The measured increase of phase delay in the region of the auditory fovea supports the conclusion that tilting of the transduction site is important for the effective opening of the involved transduction channels. Our detailed analysis of sound-induced micromechanics in this bushcricket ear demonstrates that an increase of sensory epithelium with foveal characteristics can enhance signal detection and may also improve the neuronal encoding.

Response to Garcia and Dunn.

Garcia and Dunn [1] raise some interesting and valuable points regarding our recent paper in Current Biology[2]. As Garcia and Dunn [1] point out, cross-species variation in vocal and anatomical relations allows for the identification of relevant outliers from the body size - fundamental frequency (f0) regression. However, this depends on the premise that the chosen or available f0 and body size values are typical of the species. A motivation for our study [2] was in part to improve the accuracy of such estimates by providing more data per species compared to previous studies. We address each point of their critique by controlling for cross-species body size variation using body weights for chimpanzees (Pan troglodytes) and bonobos (Pan paniscus), addressing potential call variation in different subspecies of Pan troglodytes, measuring minimum f0 as well as maximum f0 and possible effects caused by different larynx fixation methods.

Higher fundamental frequency in bonobos is explained by larynx morphology.

Acoustic signals, shaped by natural and sexual selection, reveal ecological and social selection pressures [1]. Examining acoustic signals together with morphology can be particularly revealing. But this approach has rarely been applied to primates, where clues to the evolutionary trajectory of human communication may be found. Across vertebrate species, there is a close relationship between body size and acoustic parameters, such as formant dispersion and fundamental frequency (f0). Deviations from this acoustic allometry usually produce calls with a lower f0 than expected for a given body size, often due to morphological adaptations in the larynx or vocal tract [2]. An unusual example of an obvious mismatch between fundamental frequency and body size is found in the two closest living relatives of humans, bonobos (Pan paniscus) and chimpanzees (Pan troglodytes). Although these two ape species overlap in body size [3], bonobo calls have a strikingly higher f0 than corresponding calls from chimpanzees [4]. Here, we compare acoustic structures of calls from bonobos and chimpanzees in relation to their larynx morphology. We found that shorter vocal fold length in bonobos compared to chimpanzees accounted for species differences in f0, showing a rare case of positive selection for signal diminution in both bonobo sexes.

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.

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.

Morphological integration versus ecological plasticity in the avian pelvic limb skeleton.

Understanding patterns and distributions of morphological traits is essential for discerning underpinning processes of morphological variation. We report on the variation in the avian pelvic limb skeleton. Length and width variables were measured in the skeletons of 236 avian species in order to examine the importance of body mass, ecological factors, phylogeny and integration in the formation of specific hindlimb morphology. Scaling relationships with body mass were analyzed across Aves and in individual avian subclades. Principal component analysis and multiple regressions were performed to examine the relationship between morphology, ecology, and phylogeny. Finally, the occurrence of within-limb morphological integration was tested by partial correlation analysis of the residuals from element lengths vs. body mass and correlation analysis of avian hindlimb proportions. Body mass is the greatest contributor to variation, and it strongly influences variation in avian skeletal lengths. Lengthening of the leg typically comes from disproportionate increases in tibiotarsal and tarsometatarsal length. Partial correlation analysis showed that only these two elements are distinctly integrated consistently across all bird taxa, whereas relation of femur and third toe to other limb elements displays no clear pattern. Hence, morphological integration of all elements is not a prerequisite for limb design, and variation between taxa is mainly to be found in femoral and digital length. Furthermore, variation in tibiotarsal relative length is much lower than in other elements likely due to geometric constrains. Clear ecological adaptations are obscured by multifunctionality of the avian hindlimb, and phylogeny significantly constrains the morphology. Finally, when looking at relative lengths segmented limbs meet the requirements of many-to-one-mapping of phenotype to functional property, in line with a common concept of evolvability of function and morphology.

Comparative intralimb coordination in avian bipedal locomotion.

Analyses of how intralimb coordination during locomotion varies within and across different taxa are necessary for understanding the morphological and neurological basis for locomotion in general. Previous findings suggest that intralimb proportions are the major source of kinematic variation that governs intralimb coordination across taxa. Also, independence of kinematics from habitat preference and phylogenetic position has been suggested for mammals. This leads to the hypothesis that among equally sized bird species exhibiting equal limb proportions, similar kinematics can be observed. To test this hypothesis, the bipedal locomotion of two distantly related ground-dwelling bird species (Eudromia elegans and Coturnix coturnix) and of a less terrestrial species (Corvus monedula) was investigated by means of a biplanar high-speed X-ray videographic analysis. Birds exhibited similar intralimb proportions and were filmed over a broad range of speed while moving on a treadmill. Joint and limb element angles, as well as pelvic rotations, were quantified. Regarding fore-aft motions of the limb joints and elements, a congruent pattern of intralimb coordination was observed among all experimental species. The sample of species suggests that this is largely independent of their habitat preference and systematic position and seems to be related to demands for coping with an irregular terrain with a minimum of necessary control. Hence, the initial hypothesis was confirmed. However, this congruence is not found when looking at medio-lateral limb motions and pelvic rotations, showing distinct differences between ground-dwellers (e.g. largely restricted to a parasagittal plane) and C. monedula (e.g. increased mobility of the hip joint).