Geometric morphometrics of the scapula of South American caviomorph rodents (Rodentia: Hystricognathi): Form, function and phylogeny

The scapula of the ecomorphologically diverse South American caviomorph rodents was studied through geometric morphometric techniques, using landmarks and semilandmarks to capture the shape of this complex morphological structure. Representatives of 33 species from all caviomorph superfamilies, as well as Hystrix cristata for comparisons, were analyzed. Marked differences in scapular shape were found among the major caviomorph lineages analyzed, particularly in the shape and length of the scapular spine and development of the great scapular notch. Shape differences were not influenced by body size, and only partially influenced by locomotor mode. Thus, at this scale of analysis, phylogenetic history seems to be the strongest factor influencing scapular shape. The scapular shape of erethizontids, chinchillids and Cuniculus paca could represent the less specialized state with respect to the highly differentiated scapula of octodontoids and most cavioids. In this sense, the characteristic scapular morphologies of octodontoids and cavioids could reflect particular functional capabilities and constraints associated with the evolution of prevalent locomotor modes within each lineage.     

A comparison of the ontogeny of shape variation in the anthropoid scapula: functional and phylogenetic signal

This article compares ontogenetic shape variation in the scapula of 17 anthropoid species using three-dimensional landmark-based geometric morphometrics. These data are used to investigate functional and phylogenetic signal in the major components of scapular variation and to evaluate the degree to which postnatal growth contributes to interspecific differences in shape. Results indicate that the shape of the infant and adult scapula is primarily associated with positional behavior (e.g., orthograde suspensory nonquadrupeds versus pronograde quadrupeds), but within this functional structure there is phylogenetic signal, particularly at infant stages. Growth most closely correlates with infant/adult shape and locomotor function. These results suggest that the shape of the infant scapula drives the pattern of postnatal scapular growth and adult morphology. As such, variation in postnatal growth is not the primary source of interspecific variation in adult shape. Instead, interspecific differences in scapular morphology are hypothesized to be the result of selection for variation in embryonic developmental processes that affect shape.     

Locomotion in some small to medium-sized mammals: a geometric morphometric analysis of the penultimate lumbar vertebra,pelvis and hindlimbs

We assessed the influence of a variety of aspects of locomotion and ecology including gait and locomotor types, maximal running speed, home range, and body size on postcranial shape variation in small to medium-sized mammals, employing geometric morphometric analysis and phylogenetic comparative methods. The four views analyzed, i.e., dorsal view of the penultimate lumbar vertebra, lateral view of the pelvis, posterior view of the proximal femur and proximal view of the tibia, showed clear phylogenetic signal and interesting patterns of association with movement. Variation in home range size was related to some tibia shape changes, while speed was associated with lumbar vertebra, pelvis and tibia shape changes. Femur shape was not related to any locomotor variables. In both locomotor type and high-speed gait analyses, locomotor groups were distinguished in both pelvis and tibia shape analyses. These results suggest that adaptations to both typical and high-speed gaits could explain a considerable portion of the shape of those elements. In addition, lumbar vertebra and tibia showed non-significant relationships with body mass, which suggests that they might be used in morpho-functional analyses and locomotor inferences on fossil taxa, with little or no bias for body size. Lastly, we observed morpho-functional convergences among several mammalian taxa and detected some taxa that achieve similar locomotor features following different morphological paths.     

Evolutionary patterns of shape and functional diversification in the skull and jaw musculature of triggerfishes (Teleostei: Balistidae)

The robust skull and highly subdivided adductor mandibulae muscles of triggerfishes provide an excellent system within which to analyze the evolutionary processes underlying phenotypic diversification. We surveyed the anatomical diversity of balistid jaws using Procrustes‐based geometric morphometric analyses and a phylomorphospace approach to quantifying morphological transformation through evolution. We hypothesized that metrics of interspecific cranial shape would reveal patterns of phylogenetic diversification that are congruent with functional and ecological transformation. Morphological landmarks outlining skull and adductor mandibulae muscle shape were collected from 27 triggerfish species. Procrustes‐transformed skull shape configurations revealed significant phylogenetic and size‐influenced structure. Phylomorphospace plots of cranial shape diversity reveal groupings of shape between different species of triggerfish that are mostly consistent with phylogenetic relatedness. Repeated instances of convergence upon similar cranial shape by genetically disparate taxa are likely due to the functional demands of shared specialized dietary habits. This study shows that the diversification of triggerfish skulls occurs via modifications of cranial silhouette and the positioning of subdivided jaw adductor muscles. Using the morphometric data collected here as input to a biomechanical model of triggerfish jaw function, we find that subdivided jaw adductors, in conjunction with a unique cranial skeleton, have direct biomechanical consequences that are not always congruent with phylomorphospace patterns in the triggerfish lineage. The integration of geometric morphometrics with biomechanical modeling in a phylogenetic context provides novel insight into the evolutionary patterns and ecological role of muscle subdivisions in triggerfishes. J. Morphol. 277:737–752, 2016. © 2016 Wiley Periodicals, Inc.     

Reconciling the convergence of supraspinous fossa shape among hominoids in light of locomotor differences

Differences in scapular morphology between modern humans and the African and lesser apes are associated with the distinct locomotor habits of these groups. However, several traits, particularly aspects of the supraspinous fossa, are convergent between Homo and Pongo—an unexpected result given their divergent locomotor habits. Many morphological assessments of the scapula rely on the limited number of static landmarks available, and traditional approaches like these tend to oversimplify scapular shape. Here, we present the results of two geometric morphometric (GM) analyses of hominoid supraspinous fossa shape—one employing five homologous landmarks and another with 83 sliding semilandmarks—alongside those of traditional methods to evaluate if three-dimensional considerations of fossa shape afford more comprehensive insights into scapular shape and functional morphology. Traditional measures aligned Pongo and Homo with narrow and transversely oriented supraspinous fossae, whereas African ape and Hylobates fossae are broader and more obliquely situated. However, our GM results highlight that much of the convergence between Homo and Pongo is reflective of their more medially positioned superior angles. These approaches offered a more complete assessment of supraspinous shape and revealed that the Homo fossa, with an intermediate superior angle position and moderate superoinferior expansion, is actually reminiscent of the African ape shape. Additionally, both Pongo and Hylobates were shown to have more compressed fossae, something that has not previously been identified through traditional analyses. Thus, the total morphological pattern of the Pongo supraspinous fossa is unique among hominoids, and possibly indicative of its distinctive locomotor habits. Am J Phys Anthropol 156:498–510, 2015. © 2015 Wiley Periodicals, Inc.     

Ecomorphology of the cervid intermediate phalanx and its implications for palaeoenvironmental reconstruction

This paper reports on newly developed ecomorphological models for the cervid intermediate phalanx. Using a geometric morphometric approach, we quantitatively assess the overall gracility of the bone, the depth and concavity of the proximal articulation and the roundness and symmetry of the distal articulation in the intermediate phalanx, to establish relationships between morphology, locomotor behavior and environment. The morphology of the phalanx was found to vary along a gradient from gracile phalanges with shallow proximal articulations in forms adapted to yielding substrate, to robust phalanges with deeper proximal articulations in taxa adapted to firm substrate. Phylogeny and allometry are accounted for using regressions and phylogenetic comparative methods. Although the results indicate phylogeny explains part of the morphological variation, overall the shape of the intermediate phalanx appears mainly driven by differences in function. Consequently, this element promises to be a useful palaeoenvironmental proxy that can be applied on fossil assemblages with cervid remains.     

The utility of cranial ontogeny for phylogenetic inference: a case study in crocodylians using geometric morphometrics

The degree to which the ontogeny of organisms could facilitate our understanding of phylogenetic relationships has long been a subject of contention in evolutionary biology. The famed notion that ‘ontogeny recapitulates phylogeny’ has been largely discredited, but there remains an expectation that closely related organisms undergo similar morphological transformations throughout ontogeny. To test this assumption, we used three‐dimensional geometric morphometric methods to characterize the cranial morphology of 10 extant crocodylian species and construct allometric trajectories that model the post‐natal ontogenetic shape changes. Using time‐calibrated molecular and morphological trees, we employed a suite of comparative phylogenetic methods to assess the extent of phylogenetic signal in these trajectories. All analyses largely demonstrated a lack of significant phylogenetic signal, indicating that ontogenetic shape changes contain little phylogenetic information. Notably, some Mantel tests yielded marginally significant results when analysed with the morphological tree, which suggest that the underlying signal in these trajectories is correlated with similarities in the adult cranial morphology. However, despite these instances, all other analyses, including more powerful tests for phylogenetic signal, recovered statistical and visual evidence against the assumption that similarities in ontogenetic shape changes are commensurate with phylogenetic relatedness and thus bring into question the efficacy of using allometric trajectories for phylogenetic inference.     

Modular diversification of the locomotor system in damselfishes (Pomacentridae)

As fish move and interact with their aquatic environment by swimming, small morphological variations of the locomotor system can have profound implications on fitness. Damselfishes (Pomacentridae) have inhabited coral reef ecosystems for more than 50 million years. As such, habitat preferences and behavior could significantly constrain the morphology and evolvability of the locomotor system. To test this hypothesis, we used phylogenetic comparative methods on morphometric, ecological and behavioral data. While body elongation represented the primary source of variation in the locomotor system of damselfishes, results also showed a diverse suite of morphological combinations between extreme morphologies. Results show clear associations between behavior, habitat preferences, and morphology, suggesting ecological constraints on shape diversification of the locomotor system. In addition, results indicate that the three modules of the locomotor system are weakly correlated, resulting in versatile and independent characters. These results suggest that Pomacentridae is shape may result from the interaction between (1) integrated parts of morphological variation that maintain overall swimming ability and (2) relatively independent parts of the morphology that facilitate adaptation and diversification. J. Morphol. 277:603–614, 2016. © 2016 Wiley Periodicals, Inc.     

New characters for the functional interpretation of primate scapulae and proximal humeri

The study of muscle function in nonhuman primates through the technique of electromyography (EMG) has facilitated the identification of specific functional roles for muscles in particular behaviors. This has led to a more complete understanding of the biomechanics of certain regions of the musculoskeletal system, and should facilitate our ability to identify morphological features useful in the functional interpretation of fossil material. The current paper represents one such investigation of a new set of morphometric characters of the scapula and proximal humerus suggested by EMG analyses of shoulder muscle function. A set of new metric variables were examined on the scapulae and proximal humeri of 25 species of extant anthropoid primates, as well as on casts of scapulae and humeri of three fossil primate taxa. The variables are primarily related to the line of action and attachments of the rotator cuff muscles. The position of the scapular spine, the degree of lateral expansion of the subscapular fossa, the size and shape of the subscapularis insertion facet on the lesser tubercle, and the orientation of the infraspinatus insertion facet on the greater tubercle all appear to successfully sort the extant taxa into locomotor groups. Their appearance on the fossil specimens generally supports previous functional interpretations of each taxon's locomotor abilities based on a variety of other characters, suggesting that these traits are equally applicable to fossil material. © Wiley-Liss, Inc.     

Ontogeny of the hominoid scapula: The influence of locomotion on morphology

Primate shoulder morphology has been linked with locomotor habits, oftentimes irrespective of phylogenetic heritage. Among hominoids, juvenile African apes are known to climb more frequently than adults, while orangutans and gibbons maintain an arboreal lifestyle throughout ontogeny. This study examined if these ontogenetic locomotor differences carry a morphological signal, which should be evident in the scapulae of chimpanzees and gorillas but absent in taxa that do not display ontogenetic behavioral shifts. The scapular morphology of five hominoid primates and one catarrhine outgroup was examined throughout ontogeny to evaluate if scapular traits linked with arboreal activities are modified in response to ontogenetic behavioral shifts away from climbing. Specifically, the following questions were addressed: 1) which scapular characteristics distinguish taxa with different locomotor habits; and 2) do these traits show associated changes during development in taxa known to modify their behavioral patterns? Several traits characterized suspensory taxa from nonsuspensory forms, such as cranially oriented glenohumeral joints, obliquely oriented scapular spines, relatively narrow infraspinous fossae, and inferolaterally expanded subscapularis fossae. The relative shape of the dorsal scapular fossae changed in Pan, Gorilla, and also Macaca in line with predictions based on reported ontogenetic changes in locomotor behavior. These morphological changes were mostly distinct from those seen in Pongo, Hylobates, and Homo and imply a unique developmental pattern, possibly related to ontogenetic locomotor shifts. Accordingly, features that sorted taxa by locomotor habits and changed in concert with ontogenetic behavioral patterns should be particularly useful for reconstructing the locomotor habits of fossil forms. Am J Phys Anthropol 152:239–260, 2013. © 2013 Wiley Periodicals, Inc.     

Microevolutionary patterns in the common caiman predict macroevolutionary trends across extant crocodilians

Both extinct and extant crocodilians have repeatedly diversified in skull shape along a continuum, from narrow‐snouted to broad‐snouted phenotypes. These patterns occur with striking regularity, although it is currently unknown whether these trends also apply to microevolutionary divergence during population differentiation or the early stages of speciation. Assessing patterns of intraspecific variation within a single taxon can potentially provide insight into the processes of macroevolutionary differentiation. For example, high levels of intraspecific variation along a narrow‐broad axis would be consistent with the view that cranial shapes can show predictable patterns of differentiation on relatively short timescales, and potentially scale up to explain broader macroevolutionary patterns. In the present study, we use geometric morphometric methods to characterize intraspecific cranial shape variation among groups within a single, widely distributed clade, Caiman crocodilus. We show that C. crocodilus skulls vary along a narrow/broad‐snouted continuum, with different subspecies strongly clustered at distinct ends of the continuum. We quantitatively compare these microevolutionary trends with patterns of diversity at macroevolutionary scales (among all extant crocodilians). We find that morphological differences among the subspecies of C. crocodilus parallel the patterns of morphological differentiation across extant crocodilians, with the primary axes of morphological diversity being highly correlated across the two scales. We find intraspecific cranial shape variation within C. crocodilus to span variation characterized by more than half of living species. We show the main axis of intraspecific phenotypic variation to align with the principal direction of macroevolutionary diversification in crocodilian cranial shape, suggesting that mechanisms of microevolutionary divergence within species may also explain broader patterns of diversification at higher taxonomic levels.     

Patterns of cranial shape variation in the Papionini (Primates: Cercopithecinae)

Traditional classifications of the Old World monkey tribe Papionini (Primates: Cercopithecinae) recognized the mangabey genera Cercocebus and Lophocebus as sister taxa. However, molecular studies have consistently found the mangabeys to be diphyletic, with Cercocebus and Mandrillus forming a clade to the exclusion of all other papionins. Recent studies have identified cranial and postcranial features which distinguish the Cercocebus-Mandrillus clade, however the detailed similarities in cranial shape between the mangabey genera are more difficult to reconcile with the molecular evidence. Given the large size differential between members of the papionin molecular clades, it has frequently been suggested that allometric effects account for homoplasy in papionin cranial form. A combination of geometric morphometric, bivariate, and multivariate methods was used to evaluate the hypothesis that allometric scaling contributes to craniofacial similarities between like-sized papionin taxa. Patterns of allometric and size-independent cranial shape variation were subsequently described and related to known papionin phylogenetic relationships and patterns of development.Results confirm that allometric scaling of craniofacial shape characterized by positive facial allometry and negative neurocranial allometry is present across adult papionins. Pairwise comparisons of regression lines among genera revealed considerable homogeneity of scaling within the Papionini, however statistically significant differences in regression lines also were noted. In particular, Cercocebus and Lophocebus exhibit a shared slope and significant vertical displacement of their allometric lines relative to other papionins. These findings give no support to narrowly construed hypotheses of uniquely shared patterns of allometric scaling, either between sister taxa or across all papionins. However, more general allometric trends do appear to account for a substantial proportion of papionin cranial shape variation, most notably in those features which have influenced traditional morphological phylogenies. Examination of size-uncorrelated shape variation gives no clear support to molecular phylogenies, but underscores the absence of morphometric similarities between the mangabey genera when size effects are controlled. Patterns of allometric and size-uncorrelated shape variation indicate conservatism of cranial form in non- Theropithecus papionins, and suggest that Papio represents the primitive morphometric pattern for the African papionins. Lophocebus exhibits a divergent morphometric pattern, clearly distinguishable from other papionins, most notably Cercocebus. These results clarify patterns of cranial shape variation among the extant Papionini and lay the groundwork for studies of related fossil taxa.     

Head shape evolution in monitor lizards (Varanus): interactions between extreme size disparity,phylogeny and ecology

Characterizing patterns of observed current variation, and testing hypotheses concerning the potential drivers of this variation, is fundamental to understanding how morphology evolves. Phylogenetic history, size and ecology are all central components driving the evolution of morphological variation, but only recently have methods become available to tease these aspects apart for particular body structures. Extant monitor lizards (Varanus) have radiated into an incredible range of habitats and display the largest body size range of any terrestrial vertebrate genus. Although their body morphology remains remarkably conservative, they have obvious head shape variation. We use two‐dimensional geometric morphometric techniques to characterize the patterns of dorsal head shape variation in 36 species (375 specimens) of varanid, and test how this variation relates to size, phylogenetic history and ecology as represented by habitat. Interspecific head shape disparity is strongly allometric. Once size effects are removed, principal component analysis shows that most shape variation relates to changes in the snout and head width. Size‐corrected head shape variation has strong phylogenetic signal at a broad level, but habitat use is predictive of shape disparity within phylogenetic lineages. Size often explains shape disparity among organisms; however, the ability to separate size and shape variation using geometric morphometrics has enabled the identification of phylogenetic history and habitat as additional key factors contributing to the evolution of head shape disparity among varanid lizards.     

EVOLUTION OF SCAPULA SIZE AND SHAPE IN DIDELPHID MARSUPIALS (DIDELPHIMORPHIA: DIDELPHIDAE)

The New World family Didelphidae, the basal lineage within marsupials, is commonly viewed as morphologically conservative, yet includes aquatic, terrestrial, scansorial, and arboreal species. Here, I quantitatively estimated the existing variability in size and shape of the Didelphidae scapula (1076 specimens from 56 species) using geometric morphometrics, and compared size and shape differences to evolutionary and ecologic distances. I found considerable variation in the scapula morphology, most of it related to size differences between species. This results in morphologic divergence between different locomotor habits in larger species (resulting from increased mechanical loads), but most smaller species present similarly shaped scapulae. The only exceptions are the water opossum and the short-tailed opossums, and the functional explanations for these differences remain unclear. Scapula size and shape were mapped onto a molecular phylogeny for 32 selected taxa and ancestral size and shapes were reconstructed using squared-changed parsimony. Results indicate that the Didelphidae evolved from a medium- to small-sized ancestor with a generalized scapula, slightly more similar to arboreal ones, but strikingly different from big-bodied present arboreal species, suggesting that the ancestral Didelphidae was a small scansorial animal with no particular adaptations for arboreal or terrestrial habits, and these specializations evolved only in larger-bodied clades.     

Lower molar shape and size in prosimian and platyrrhine primates

The goal of this research is to evaluate the relative strength of the influences of diet, size, and phylogenetic signal on dental geometric shape. Accurate comprehension of these factors and their interaction is important for reconstructing diet and deriving characters for a cladistic analysis in fossil primates. Geometric morphometric analysis is used to identify axes of shape variation in the lower second molars of (a) prosimian primates and (b) platyrrhines. Landmarks were placed on µCT‐generated surface renderings. Landmark configurations were aligned using generalized Procrustes analysis. Principal components analysis and phylogenetic principal components analysis (pPCA) were performed on species average landmark co‐ordinates. pPCs were examined with phylogenetic generalized least squares analysis for association with size and with diet. PCs from both phylogenetic and non‐phylogenetic analyses were sufficient to separate species by broad dietary categories, including insectivores and folivores. In neither analysis was pPC1 correlated with tooth size, but some other pPCs were significantly correlated with size. The pattern of association between pPCs and size altered when centroid size and dietary variables were combined in the model; effects of diet factors typically exceeded effects of size. These results indicate a dominant phylogenetic and dietary signal in molar shape but also show some shape change correlated with size in the absence of obvious dietary associations. Geometric morphometric analysis appears to be useful for tracking functional traits in molars, particularly in tracking differences between folivorous and insectivorous species.     

Differentiation at a microgeographical scale within two species of ground beetle, Carabus auronitens and C. nemoralis (Coleoptera, Carabidae): a geometrical morphometric approach

New morphometric methods, the geometrical morphometrics, offer promising perspectives to appraise morphological variation among organisms and open up, to a large extent, the field of morphometrics for the study of systematics and evolution. Until now, however, few studies have explored the potential of these methods at a microgeographical scale. In the present work, we applied them to quantify morphological (size and shape) differentiation among populations of two forest species of ground beetles: Carabus auronitens and C. nemoralis . We found a significant shape variation among sites, as well as among sexes, for both species. Additionally, for C. auronitens , we found significant positive correlations in both sexes between morphological (shape) and geographical distances between populations. In contrast, significant size differences were found between sexes, but not between sites. We conclude that geometrical morphometric methods provide valuable tools for the study of morphological variation among populations and therefore offer, on the whole, interesting perspectives for the study of biodiversity patterns.     

TESTING FOR ANCIENT ADAPTIVE RADIATIONS IN NEOTROPICAL CICHLID FISHES

Most contemporary studies of adaptive radiation focus on relatively recent and geographically restricted clades. It is less clear whether diversification of ancient clades spanning entire continents is consistent with adaptive radiation. We used novel fossil calibrations to generate a chronogram of Neotropical cichlid fishes and to test whether patterns of lineage and morphological diversification are congruent with hypothesized adaptive radiations in South and Central America. We found that diversification in the Neotropical cichlid clade and the highly diverse tribe Geophagini was consistent with diversity‐dependent, early bursts of divergence followed by decreased rates of lineage accumulation. South American Geophagini underwent early rapid differentiation in body shape, expanding into novel morphological space characterized by elongate‐bodied predators. Divergence in head shape attributes associated with trophic specialization evolved under strong adaptive constraints in all Neotropical cichlid clades. The South American Cichlasomatini followed patterns consistent with constant rates of morphological divergence. Although morphological diversification in South American Heroini was limited, Eocene invasion of Central American habitats was followed by convergent diversification mirroring variation observed in Geophagini. Diversification in Neotropical cichlids was influenced by the early adaptive radiation of Geophagini, which potentially limited differentiation in other cichlid clades.     

Ontogeny of the Massospondylus labyrinth: implications for locomotory shifts in a basal sauropodomorph dinosaur

Ontogeny is a vital aspect of life history sometimes overlooked in palaeontological studies. However, the changing geometry of anatomical structures during growth can be informative regarding ecological and functional reconstructions. The inner ear, or labyrinth, is an ideal ontogenetic study system because it has a strong functional signal in its morphology that is linked to locomotor mode. Yet almost nothing is known about labyrinth development in dinosaurs. We quantified labyrinth scale and geometry through ontogeny in the Early Jurassic dinosaur Massospondylus carinatus, which has an exceptional fossil record and is hypothesized to have undergone a gait change, from quadrupedal juvenile to bipedal adult. To test whether this putative locomotor shift is reflected in labyrinth morphology, computed microtomography (μCT) and propagation phase‐contrast synchrotron radiation microtomography (PPC‐SRμCT) were used to obtain labyrinths from eight specimens, ranging from near‐hatchling to adult. Labyrinths grow substantially but scale with slight negative allometry compared to skull length throughout ontogeny, the first time this has been documented in dinosaurs. Geometric morphometric analysis of the labyrinth using a sliding semilandmark approach shows some morphological change through ontogeny, but little evidence supporting a locomotor shift. These results have implications for our understanding of sauropodomorph development and provide a better understanding of dinosaur locomotory evolution.     

Ontogeny of robusticity of craniofacial traits in modern humans: A study of South American populations

To date, differences in craniofacial robusticity among modern and fossil humans have been primarily addressed by analyzing adult individuals; thus, the developmental basis of such differentiation remains poorly understood. This article aims to analyze the ontogenetic development of craniofacial robusticity in human populations from South America. Geometric morphometric methods were used to describe cranial traits in lateral view by using landmarks and semilandmarks. We compare the patterns of variation among populations obtained with subadults and adults to determine whether population‐specific differences are evident at early postnatal ontogeny, compare ontogenetic allometric trajectories to ascertain whether changes in the ontogeny of shape contribute to the differentiation of adult morphologies, and estimate the amount of size change that occurs during growth along each population‐specific trajectory. The results obtained indicate that the pattern of interpopulation variation in shape and size is already established at the age of 5 years, meaning that processes acting early during ontogeny contribute to the adult variation. The ontogenetic allometric trajectories are not parallel among all samples, suggesting the divergence in the size‐related shape changes. Finally, the extension of ontogenetic trajectories also seems to contribute to shape variation observed among adults. Am J Phys Anthropol 2010. © 2009 Wiley‐Liss, Inc.