Convergent evolution in Afrotheria and non-afrotherians demonstrates high evolvability of the mammalian inner ear.

Evolutionary convergence in distantly related species is among the most convincing evidence of adaptive evolution. The mammalian ear, responsible for balance and hearing, is not only characterised by its spectacular evolutionary incorporation of several bones of the jaw, it also varies considerably in shape across modern mammals. Using a multivariate approach, we show that in Afrotheria, a monophyletic clade with morphologically and ecologically highly disparate species, inner ear shape has evolved similar adaptations as in non-afrotherian mammals. We identify four eco-morphological trait combinations that underlie this convergence. The high evolvability of the mammalian ear is surprising: Nowhere else in the skeleton are different functional units so close together; it includes the smallest bones of the skeleton, encapsulated within the densest bone. We suggest that this evolvability is a direct consequence of the increased genetic and developmental complexity of the mammalian ear compared to other vertebrates.

Morphology of the Bony Labyrinth Supports the Affinities of Paradolichopithecus with the Papionina.

Discoveries in recent decades indicate that the large papionin monkeys Paradolipopithecus and Procynocephalus are key members of the Late Pliocene - Early Pleistocene mammalian faunas of Eurasia. However, their taxonomical status, phylogenetic relationships, and ecological profile remain unclear. Here we investigate the two latter aspects through the study of the inner ear anatomy, as revealed by applying micro-CT scan imaging techniques on the cranium LGPUT DFN3-150 of Paradolichopithecus from the lower Pleistocene (2.3 Ma) fossil site Dafnero-3 in Northwestern Greece. Using geometric morphometric methods, we quantified shape variation and the allometric and phylogenetic signals in extant cercopithecines (n = 80), and explored the morphological affinities of the fossil specimen with extant taxa. LGPUT DFN3-150 has a large centroid size similar to that of baboons and their relatives. It shares several shape features with Macacina and Cercopithecini, which we interpret as probable retention of a primitive morphology. Overall, its inner ear morphology is more consistent with a stem Papionini more closely related to Papionina than Macacina, or to a basal crown Papionina. Our results, along with morphometrical and ecological features from previous studies, call into question the traditional hypothesis of a Paradolichopithecus-Macacina clade, and provide alternative perspectives in the study of Eurasian primate evolution during the late Neogene-Quaternary. Supplementary Information: The online version contains supplementary material available at 10.1007/s10764-022-00329-4.

Detecting Phylogenetic Signal and Adaptation in Papionin Cranial Shape by Decomposing Variation at Different Spatial Scales.

Phylogenetic reconstruction based on morphometric data is hampered by homoplasies. For example, many similarities in cranial form between primate taxa more strongly reflect ecological similarities rather than phylogenetic relatedness. However, the way in which the different cranial bones constitute cranial form is, if at all, of less functional relevance and thus largely hidden from selection. We propose that these "constructional details" are better indicators of phylogenetic history than any large-scale shape feature or raw form variable. Within a geometric morphometric context, we show how to analyze the relative extent of bones independently of differences in overall shape. We also show how to decompose total shape variation into small-scale and large-scale shape variation. We apply both methods to the midsagittal cranial morphology of papionin monkeys, which are well known for the discrepancy between morphological similarities and phylogenetic relationships. We study phylogenetic signal and functional adaptation using a molecular phylogeny and contextual data on feeding ecology and locomotor behavior. As expected, total cranial shape, bone outline shape, and large-scale shape features were only weakly associated with phylogenetic distance. But the relative bone contributions and small-scale shape features were both highly correlated with phylogenetic distances. By contrast, the association with ecological and behavioral variables was strongest for the outline shape and large-scale shape features. Studies of morphological adaptation and phylogenetic history thus profit from a decomposition of shape variation into different spatial scales. [Adaptation; canalization; cranial shape; geometric morphometrics; papionini; partial warps; phylogeny.].

Evolution of the Mammalian Ear: An Evolvability Hypothesis.

Encapsulated within the temporal bone and comprising the smallest elements of the vertebrate skeleton, the ear is key to multiple senses: balance, posture control, gaze stabilization, and hearing. The transformation of the primary jaw joint into the mammalian ear ossicles is one of the most iconic transitions in vertebrate evolution, but the drivers of this complex evolutionary trajectory are not fully understood. We propose a novel hypothesis: The incorporation of the bones of the primary jaw joint into the middle ear has considerably increased the genetic, regulatory, and developmental complexity of the mammalian ear. This increase in the number of genetic and developmental factors may, in turn, have increased the evolutionary degrees of freedom for independent adaptations of the different functional ear units. The simpler ear anatomy in birds and reptiles may be less susceptible to developmental instabilities and disorders than in mammals but also more constrained in its evolution. Despite the tight spatial entanglement of functional ear components, the increased "evolvability" of the mammalian ear may have contributed to the evolutionary success and adaptive diversification of mammals in the vast diversity of ecological and behavioral niches observable today. A brief literature review revealed supporting evidence for this hypothesis.

Morphometric Variation at Different Spatial Scales: Coordination and Compensation in the Emergence of Organismal Form.

It is a classic aim of quantitative and evolutionary biology to infer genetic architecture and potential evolutionary responses to selection from the variance-covariance structure of measured traits. But a meaningful genetic or developmental interpretation of raw covariances is difficult, and classic concepts of morphological integration do not directly apply to modern morphometric data. Here, we present a new morphometric strategy based on the comparison of morphological variation across different spatial scales. If anatomical elements vary completely independently, then their variance accumulates at larger scales or for structures composed of multiple elements: morphological variance would be a power function of spatial scale. Deviations from this pattern of "variational self-similarity" (serving as a null model of completely uncoordinated growth) indicate genetic or developmental coregulation of anatomical components. We present biometric strategies and R scripts for identifying patterns of coordination and compensation in the size and shape of composite anatomical structures. In an application to human cranial variation, we found that coordinated variation and positive correlations are prevalent for the size of cranial components, whereas their shape was dominated by compensatory variation, leading to strong canalization of cranial shape at larger scales. We propose that mechanically induced bone formation and remodeling are key mechanisms underlying compensatory variation in cranial shape. Such epigenetic coordination and compensation of growth are indispensable for stable, canalized development and may also foster the evolvability of complex anatomical structures by preserving spatial and functional integrity during genetic responses to selection.[Cranial shape; developmental canalization; evolvability; morphological integration; morphometrics; phenotypic variation; self-similarity.].

New Eocene primate from Myanmar shares dental characters with African Eocene crown anthropoids.

Recent discoveries of older and phylogenetically more primitive basal anthropoids in China and Myanmar, the eosimiiforms, support the hypothesis that Asia was the place of origins of anthropoids, rather than Africa. Similar taxa of eosimiiforms have been discovered in the late middle Eocene of Myanmar and North Africa, reflecting a colonization event that occurred during the middle Eocene. However, these eosimiiforms were probably not the closest ancestors of the African crown anthropoids. Here we describe a new primate from the middle Eocene of Myanmar that documents a new clade of Asian anthropoids. It possesses several dental characters found only among the African crown anthropoids and their nearest relatives, indicating that several of these characters have appeared within Asian clades before being recorded in Africa. This reinforces the hypothesis that the African colonization of anthropoids was the result of several dispersal events, and that it involved more derived taxa than eosimiiforms.

New data about semicircular canal morphology and locomotion in modern hominoids.

The labyrinth has two functional parts: the cochlea for audition and the vestibular system for equilibrioception. In the latter, the semicircular ducts and the otolithic organs are sensitive to rotational and linear accelerations of the head, respectively. The labyrinthine morphology influences perception accuracy, hence the adaptation to a specific locomotor pattern. The aim of this study is to determine the relationship between locomotion and semicircular canal morphology using geometric morphometrics, and to explain these links with existing functional models. The influence of factors other than functional constraints on labyrinthine morphology is discussed. The left bony labyrinth of 65 specimens was extracted virtually. Five extant hominoid species with various locomotion modes were sampled. A set of 13 landmarks was placed on the semicircular canals. After a Procrustes fit, their coordinates were analyzed using a principal component analysis. It was found that labyrinthine morphology is significantly distinct between species. More specifically, the differences involve a posterolateral projection of the lateral semicircular canal and the rotation of this canal relative to the vertical canals. This rotation occurs in the sagittal plane, which is consistent with previous studies based on traditional morphometrics. Among extant hominoids, the shape of the canals potentially discriminates species based on posture. This result could be used to reconstruct the locomotor pattern of fossil hominoids.