Functional and historical determinants of shape in the scapula of Xenarthran mammals: Evolution of a complex morphological structure

The mammalian scapula is a complex morphological structure, composed of two ossification plates that fuse into a single structure. Most studies on morphological differentiation in the scapula have considered it to be a simple, spatially integrated structure, primarily influenced by the important locomotor function presented by this element. We used recently developed geometric morphometric techniques to test and quantify functional and phylogenetic influences on scapular shape variation in fossil and extant xenarthran mammals. The order Xenarthra is well represented in the fossil record and presents a stable phylogenetic hypothesis for its genealogical history. In addition, its species present a large variety of locomotor habits. Our results show that approximately half of the shape variation in the scapula is due to phylogenetic heritage. This is contrary to the view that the scapula is influenced only by functional demands. There are large‐scale shape transformations that provide biomechanical adaptation for the several habits (arboreality, terrestriality, and digging), and small scale‐shape transformations (mostly related to the coracoid process) that are not influenced by function. A nonlinear relationship between morphometric and phylogenetic distances indicates the presence of a complex mixture of evolutionary processes acting on shape differentiation of the scapula. J. Morphol. 241:251–263, 1999. © 1999 Wiley‐Liss, Inc.     

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.     

Facial heights: evolutionary relevance of postnatal ontogeny for facial orientation and skull morphology in humans and chimpanzees

Facial heights, i.e. the vertical distances between the superior and inferior limits of facial compartments, contribute to the orientation of the viscerocranium in the primate skull. In humans, vertical facial variation is among the main sources of diversity and frequently associated with an integrated suite of other cranio-mandibular traits. Facial heights and kyphosis are also important factors in interspecific variation and models of hominoid evolution. The ontogenetic determination of adult facial orientation and its relation to phylogenetic variation are unclear, but crucial in all previously mentioned respects. We addressed these issues in a sample of 175 humans and chimpanzees with Procrustes based geometric morphometrics, testing hypotheses of interspecific similarity in postnatal ontogenetic trajectories, early versus later ontogenetic facial pattern determination, and a developmental model of morphological integration. We analyzed the contribution of postnatal morphogenesis to adult vertical facial variation by partitioning morphological variation into a portion of pure growth allometry and a non-allometric fraction. A statistically significant difference of growth-allometries revealed that in both species growth established the adult skull proportions by vertical facial expansion, but while in chimpanzees the complete viscerocranium showed reorientation, in humans only the lower face was modified. In both species the results support a hypothesis of early facial pattern determination. A coincident emergence of morphological traits favors a hypothesis of developmental integration of the face, excluding traits of the basi- and neurocranium. Interspecific differences in integration may have implications for evolutionary studies. The present findings indicate that growth establishes the adult skull proportions and integrates principal facial orientation patterns, already there in early postnatal ontogeny.     

Constraints on the morphological evolution of marsupial shoulder girdles

Throughout their evolutionary histories, marsupial mammals have been taxonomically and morphologically less diverse than their sister taxa the placentals. Because of this, it has been proposed that the evolution of marsupials has been constrained by the functional requirements of their mode of reproduction. Marsupials give birth after short gestation times to immature neonates that immediately crawl, under the power of their precociously developed shoulder girdles, to the teat where they attach and complete their early development. Using a novel approach incorporating adult and embryological morphological data, this study is the first to both: (1) statistically support adult patterns of morphological divergence consistent with the constraint hypothesis, and (2) identify ontogenetic patterns of morphological change that demonstrate that the constraint was responsible, at least in part, for their formation. As predicted by the marsupial constraint, the shoulder girdles of adult marsupials are less diverse than those of adult placentals, and adult marsupial scapulae are less morphologically diverse than adult marsupial pelves. Furthermore, marsupials that complete an extensive crawl to the teat are restricted to a common pattern of ontogenetic scapular shape change, strongly supporting the hypothesis that the morphological development of the marsupial scapula has been limited evolutionarily by its obligate role in the crawl to the teat. Because this study establishes that ontogenetic and evolutionary morphological change is correlated within mammalian scapulae, it is probable that the marsupial constraint also restricted the morphological divergence of the scapula over evolutionary time by limiting ontogenetic change in the scapula. These findings, coupled with the importance of the shoulder girdle in mammalian locomotor specialization, support the conclusion that the low morphological diversity of marsupial forms over evolutionary time could be directly due to the constraint on marsupial morphological evolution caused by the functional requirements of the crawl to the teat.     

Ontogenesis of the scapula in marsupial mammals, with special emphasis on perinatal stages of didelphids and remarks on the origin of the therian scapula

The development of the scapula was studied in embryonic and postnatal specimens of Monodelphis domestica and perinatal specimens of Philander opossum, Caluromys philander, and Sminthopsis virginiae using histological sections and 3D reconstructions. Additionally, macerated skeletons of postnatal M. domestica were examined. This study focused on the detachment of the scapulocoracoid from the sternum and on the acquisition of a supraspinous fossa, a supraspinatus muscle, and a scapular spine, all these events associated with the origin of the therian shoulder girdle. In none of the specimens is there a continuity of the cartilaginous scapulocoracoid with the sternum, even though the structures are in close proximity, especially in S. virginiae. At birth, the first rib laterally presents a pronounced boss that probably contacts the humerus during certain movements. Only the acromial portion of the scapular spine, which originates from the anterior margin of the scapular blade, is preformed in cartilage. The other portion is formed by appositional bone ("Zuwachsknochen"), which expands from the perichondral ossification of the scapula into an intermuscular aponeurosis between the supra- and infraspinous muscles. This intermuscular aponeurosis inserts more or less in the middle of the lateral surface of the developing scapula. Thus, the floor of the supraspinous fossa is present from the beginning of scapular development, simultaneously with the infraspinous fossa. The homology of the therian spine with the anterior border of the sauropsid and monotreme scapula is questioned. We consider the dorsal portion (as opposed to the ventral or acromial portion) of the scapular spine a neomorphic structure of therian mammals.     

Ontogeny,function, and scaling of the mandibular symphysis in papionin primates

In vivo study of mastication in adult cercopithecine primates demonstrates a link between mandibular symphyseal form and resistance to “wishboning,” or lateral transverse bending. Mechanical consideration of wishboning at the symphysis indicates exponentially higher stresses along the lingual surface with increasing symphyseal curvature. Lengthening the anteroposterior width of the symphysis acts to resist these higher loads. Interspecific adult cercopithecine allometries show that both symphyseal curvature and symphyseal width exhibit positive allometry relative to body mass. The experimental and allometric data support an hypothesis that the cercopithecine mandibular symphysis is designed to maintain functional equivalence—in this case dynamic strain similarity—in wishboning stress and strain magnitudes across adult cercopithecines. We test the hypothesis that functional equivalence during masticatory wishboning is maintained throughout ontogeny by calculating relative stress estimates from morphometric dimensions of the mandibular symphysis in two cercopithecine primates, Macaca fascicularis and M. nemestrina. Results indicate no significant differences in relative stress estimates among the two macaque ontogenies and an interspecific sample of adult papionin primates. Further, relative stress estimates do not change significantly throughout ontogeny in either species. These results offer the first evidence for the maintenance of functional equivalence in stress and strain levels during postnatal growth in a habitually loaded cranial structure. Scaling analyses demonstrate significant slope differences for both symphyseal curvature and width between the ontogenetic and interspecific samples. The distinct interspecific cercopithecine slopes are realized by a series of ontogenetic transpositions in both symphyseal curvature and width. Throughout papionin ontogeny, symphyseal curvature increases with less negative allometry, while symphysis width increases with less positive allometry versus the interspecific pattern. As symphyseal curvature and width are inversely proportional to one another in estimating relative stresses, functionally equivalent stress levels are maintained both ontogenetically and interspecifically, because the relatively slower rate of allometric increase in symphyseal curvature during growth is compensated for by a slower rate of allometric increase in symphyseal width. These results indicate the primacy of maintaining functional equivalence during growth and the need for ontogenetic data in understanding the evolutionary processes that affect form–function relations as well as the interspecific patterning of adult form across a clade. J. Morphol. 235:157–175, 1998. © 1998 Wiley-Liss, Inc.     

3D reconstructions of quail–chick chimeras provide a new fate map of the avian scapula

Limbed vertebrates have functionally integrated postcranial axial and appendicular systems derived from two distinct populations of embryonic mesoderm. The axial skeletal elements arise from the paraxial somites, the appendicular skeleton and sternum arise from the somatic lateral plate mesoderm, and all of the muscles for both systems arise from the somites. Recent studies in amniotes demonstrate that the scapula has a mixed mesodermal origin. Here we determine the relative contribution of somitic and lateral plate mesoderm to the avian scapula from quail-chick chimeras. We generate 3D reconstructions of the grafted tissue in the host revealing a very different distribution of somitic cells in the scapula than previously reported. This novel 3D visualization of the cryptic border between somitic and lateral plate populations reveals the dynamics of musculoskeletal morphogenesis and demonstrates the importance of 3D visualization of chimera data. Reconstructions of chimeras make clear three significant contrasts with existing models of scapular development. First, the majority of the avian scapula is lateral plate derived and the somitic contribution to the scapular blade is significantly smaller than in previous models. Second, the segmentation of the somitic component of the blade is partially lost; and third, there are striking differences in growth rates between different tissues derived from the same somites that contribute to the structures of the cervical thoracic transition, including the scapula. These data call for the reassessment of theories on the development, homology, and evolution of the vertebrate scapula.     

Artificial selection sheds light on developmental mechanisms of limb elongation

Species diversity in limb lengths and proportions is thought to have evolved adaptively in the context of locomotor and habitat specialization, but the heritable cellular processes that drove this evolution within species are poorly understood. In this study, we take a novel “micro‐evo‐devo” approach, using artificial selection on relative limb length to amplify phenotypic variation in a population of mice, known as Longshanks, to examine the cellular mechanisms of postnatal limb development that contribute to intraspecific limb length variation. Cross‐sectional growth data indicate that differences in bone length between Longshanks and random‐bred controls are not due to prolonged growth, but to accelerated growth rates. Histomorphometric and cell proliferation assays on proximal tibial growth plates show that Longshanks’ increased limb bone length is associated with an increased number of proliferative chondrocytes. In contrast, we find no differences in other growth plate cellular features known to underlie interspecific differences in limb bone size and shape, such as the rates of chondrocyte proliferation or the size and number of hypertrophic cells in the growth plate. These data suggest that small differences among individuals in the number of proliferating chondrocytes are a potentially important determinant of selectable intraspecific variation in individual limb bone lengths, independent of body size.     

Functional trait differences influence neighbourhood interactions in a hyperdiverse Amazonian forest

As distinct community assembly processes can produce similar community patterns, assessing the ecological mechanisms promoting coexistence in hyperdiverse rainforests remains a considerable challenge. We use spatially explicit neighbourhood models of tree growth to quantify how functional trait and phylogenetic similarities predict variation in growth and crowding effects for the 315 most abundant tree species in a 25‐ha lowland rainforest plot in Ecuador. We find that functional trait differences reflect variation in (1) species maximum potential growth, (2) the intensity of interspecific interactions for some species, and (3) species sensitivity to neighbours. We find that neighbours influenced tree growth in 28% of the 315 focal tree species. Neighbourhood effects are not detected in the remaining 72%, which may reflect the low statistical power to model rare taxa and/or species insensitivity to neighbours. Our results highlight the spectrum of ways in which functional trait differences can shape community dynamics in highly diverse rainforests.     

Allometry and heterochrony in the African apes

In this work allometry and heterochrony are integrated in an analysis of ontogenic and interspecific morphological patterns in the African apes. The relationship between the interspecific differences in adult morphology and the differences in underlying patterns of growth allometries, body weight growth rates, and developmental chronologies is investigated. Results indicate that rate hypermorphosis, or the extension of ancestral allometries into new size/shape ranges with no increase in the duration of ontogeny, underlies many of the interspecific differences in form among the African apes. In addition, the need for further clarification of the processes of heterochrony is stressed by distinguishing between rate and timing differences. These distinctions and processes are illustrated and discussed using the morphological data on the African apes.     

Phylogenetic effects on functional traits and life history strategies of Australian freshwater fish

Understanding the biogeographic and phylogenetic basis to interspecific differences in species’ functional traits is a central goal of evolutionary biology and community ecology. We quantify the extent of phylogenetic influence on functional traits and life‐history strategies of Australian freshwater fish to highlight intercontinental differences as a result of Australia's unique biogeographic and evolutionary history. We assembled data on life history, morphological and ecological traits from published sources for 194 Australian freshwater species. Interspecific variation among species could be described by a specialist–generalist gradient of variation in life‐history strategies associated with spawning frequency, fecundity and spawning migration. In general, Australian fish showed an affinity for life‐history strategies that maximise fitness in hydrologically unpredictable environments. We also observed differences in trait lability between and within life history, morphological and ecological traits where in general morphological and ecological traits were more labile. Our results showed that life‐history strategies are relatively evolutionarily labile and species have potentially evolved or colonised in freshwaters frequently and independently allowing them to maximise population performance in a range of environments. In addition, reproductive guild membership showed strong phylogenetic constraint indicating that evolutionary history is an important component influencing the range and distribution of reproductive strategies in extant species assemblages. For Australian freshwater fish, biogeographic and phylogenetic history contribute to broad taxonomic differences in species functional traits, while finer scale ecological processes contribute to interspecific differences in smaller taxonomic units. These results suggest that the lability or phylogenetic relatedness of different functional traits affects their suitability for testing hypothesis surrounding community level responses to environmental change.     

Phylogenetic and environmental components of morphological variation: skull, mandible, and molar shape in marmots (Marmota, Rodentia)

The phenotype is a product of its phylogenetic history and its recent adaptation to local environments, but the relative importance of the two factors is controversial. We assessed the effects of diet, habitat, elevation, temperature, precipitation, body size, and mtDNA genetic divergence on shape variation in skulls, mandibles, and molars, structures that differ in their genetic and functional control. We asked whether these structures have adapted to environment to the same extent and whether they retain the same amount of phylogenetic signal. We studied these traits in intra- and interspecific populations of Eurasian marmots whose last common ancestor lived 2-5 million years ago. Path Analysis revealed that body size explained 10% of variation in skulls, 7% in mandibles, and 15% in molars. Local vegetation explained 7% of variation in skulls, 11% in mandibles, and 12% in molars. Dietary category explained 25% of variation in skulls, 11% in mandibles, and 9% in molars. Cyt b mtDNA divergence (phylogeny) explained 15% of variation in skulls, 7% in mandibles, and 5% in molars. Despite the percentages of phylogenetic variance, maximum-likelihood trees based on molar and skull shape recovered most phylogenetic groupings correctly, but mandible shape did not. The good performance of molars and skulls was probably due to different factors. Skulls are genetically and functionally more complicated than teeth, and they had more mathematically independent components of variation (5-6-in skulls compared to 3-in molars). The high proportion of diet-related variance was not enough to mask the phylogenetic signal. Molars had fewer independent components, but they also have less ecophenotypic variation and evolve more slowly, giving each component a proportionally stronger phylogenetic signal. Molars require larger samples for each operational taxonomic unit than the other structures because the proportion of within-taxon to between-taxon variation was higher. Good phylogenetic signal in quantitative skeletal morphology is likely to be found only when the taxa have a common ancestry no older than hundreds of thousands or millions of years (1% to 10% mtDNA divergence)--under these conditions skulls and molars provide stronger signal than mandibles.     

Assessment of scapular morphology and bone quality with statistical models

The design of total shoulder arthroplasty implants are guided by anatomy. The objective of this study was to develop statistical models to quantify shape and material property variation in the scapula. Material-mapped models were reconstructed from CT scans for a training set of subjects. Statistical shape (SSM) and intensity (SIM) models were created; SSM modes described scaling, changes in the medial border and acromial process, and elongation of the scapular blade. SIM modes captured bone quality changes in the anterior and inferior glenoid. Bone quality was independent of scapular morphology. Variation described by the statistical representations can inform implant design and sizing.     

Arm joint articulations in the ophiuran brittlestars (Echinodermata: Ophiuroidea): a morphometric analysis of ontogenetic, serial, and interspecific variation

The ophiuroid arm contains a series of vertebral ossicles that form an articulated internal skeleton. Ontogenetic, serial, and interspecific variation in these skeletal elements are investigated using morphometric data from 35 species of brittle-stars (Order Ophiurae). Multiple ossicles were sampled from each individual and several individuals were sampled from each species to reconstruct serial and ontogenetic changes in vertebral morphology. Within species, ontogenetic and serial allometries are not statistically different. These data support 'Jackson's law of localized stages' (Jackson, 1899; Clark, 1914), which proposes that serial variation along the arm reflects ontogenetic stages of ossicle growth.
A multivariate analysis of interspecific variation shows two major vertebral forms: ossicles with a proximal depression and distal keel, and ossicles lacking these features. Variation within these groups is largely continuous, but individual species show distinct shape differences and unique allometric patterns of serial variation. These results suggest that vertebral ossicle variation among species can be described by: 1) variation in initial shape; and 2) variation in the allometric trajectory along the proximal-distal axis.
In all species, the most proximal ossicles within the disk show a non-keeled morphology. In species with keeled arm ossicles, however, there is an abrupt transition within the disk between non-keeled and keeled vertebral forms. A single ossicle, having features of both vertebral types, occurs at this site. The taxonomic distribution of the two vertebral forms and the anatomical transition between forms is discussed with reference to current classification systems and recent phylogenetic schemes for the Ophiuroidea.     

Cats and Dogs Down the Tree: The Tempo and Mode of Evolution in the Lower Carnassial of Fossil and Living Carnivora

Teeth are usually considered the primer to understand mammalian evolution. Their morphology is the result of the complex interplay between adaptation to food processing and somewhat fixed developmental programs. We analyse the morphometry of the first lower molar (m1 = lower carnassial) in 199 carnivore species (64 extant and 135 extinct) in order to clarify the tempo and mode of evolution of two different and possibly related traits, tooth size and tooth angular height. We applied a set of comparative methods and produced disparity through time plots by using four alternative phylogenetic trees. Three of them include fossil species, and were used in order to estimate what an effect the inclusion of fossil species has on the patterns we found for extant species. Our analyses on living species show that m1 size exhibits a weak phylogenetic signal, and that its variance occurs more within than among clades. The opposite applies to m1 angular height, which evolved in an adaptive radiation-like fashion, showing very strong phylogenetic signal and great among-clade variation. These results are thoroughly confirmed after the inclusion of fossil data. Major differences in m1 shape in Carnivora were clearly established early in their evolutionary history, probably as a result of rapid morphospace occupation after the clade radiation. Successive variation in tooth size allowed species to avoid potential overlap in feeding morphologies as a mechanism to limit interspecific competitive interaction within subclades.     

Exploring patterns of interspecific variation in quantitative traits using sequential phylogenetic eigenvector regressions

A number of metrics have been developed for estimating phylogenetic signal in data and to evaluate correlated evolution, inferring broad-scale evolutionary and ecological processes. Here, we proposed an approach called phylogenetic signal-representation (PSR) curve, built upon phylogenetic eigenvector regression (PVR). In PVR, selected eigenvectors extracted from a phylogenetic distance matrix are used to model interspecific variation. In the PSR curve, sequential PVR models are fitted after successively increasing the number of eigenvectors and plotting their R(2) against the accumulated eigenvalues. We used simulations to show that a linear PSR curve is expected under Brownian motion and that its shape changes under alternative evolutionary models. The PSR area, expressing deviations from Brownian motion, is strongly correlated (r= 0.873; P < 0.01) with Blomberg's K-statistics, so nonlinear PSR curves reveal if traits are evolving at a slower or higher rate than expected by Brownian motion. The PSR area is also correlated with phylogenetic half-life under an Ornstein-Uhlenbeck process, suggesting how both methods describe the shape of the relationship between interspecific variation and time since divergence among species. The PSR curve provides an elegant exploratory method to understand deviations from Brownian motion, in terms of acceleration or deceleration of evolutionary rates occurring at large or small phylogenetic distances.     

Phylogenetic signal,function and integration in the subunits of the carnivoran mandible

Complex phenotypes could be interpreted as the result of functional integration between identifiable subunits. Common developmental or ecological factors may favour macroevolutionary morphological integration so that functional subunits also covary above the species level. We investigate shape variation and functional integration in two subunits of the mammalian mandible: the corpus and the ramus in a subset of extant terrestrial Carnivora using geometric morphometric and comparative methods. More specifically, we test if corpus and ramus shape exhibit similar degree of homoplasy and if these traits covary above species level. Additionally, broad functional categorisations (predaceous and non predaceous) are investigated to test if differences in morphological variation and integration at macroevolutionary scale occur. Principal components of shape data show a significant phylogenetic signal in both mandibular subunits, with the ramus exhibiting a higher degree of homoplasy than the corpus. Functional groups (predators and non-predators) are significantly distinct in corpus shape, while in the ramus significance emerges only after removing the phylogenetic signal. Partial Least Square shows that mandibular corpus and ramus region covaries above species level even if this trend is not supported when employing comparative methods. Only in a subset of predaceous species covariation still hold. We conclude that mandibular subunits of Carnivora differ considerably in shape among predaceous and non-predaceous species because of the adaptive selection pressure imposed by catching and hold of live prey. This selective process also favoured macroevolutionary integration in predaceous carnivorans.     

Evolution of a complex phenotype with biphasic ontogeny: Contribution of development versus function and climatic variation to skull modularity in toads

The theory of morphological integration and modularity predicts that if functional correlations among traits are relevant to mean population fitness, the genetic basis of development will be molded by stabilizing selection to match functional patterns. Yet, how much functional interactions actually shape the fitness landscape is still an open question. We used the anuran skull as a model of a complex phenotype for which we can separate developmental and functional modularity. We hypothesized that functional modularity associated to functional demands of the adult skull would overcome developmental modularity associated to bone origin at the larval phase because metamorphosis would erase the developmental signal. We tested this hypothesis in toad species of the Rhinella granulosa complex using species phenotypic correlation pattern (P‐matrices). Given that the toad species are distributed in very distinct habitats and the skull has important functions related to climatic conditions, we also hypothesized that differences in skull trait covariance pattern are associated to differences in climatic variables among species. Functional and hormonal‐regulated modules are more conspicuous than developmental modules only when size variation is retained on species P‐matrices. Without size variation, there is a clear modularity signal of developmental units, but most species have the functional model as the best supported by empirical data without allometric size variation. Closely related toad species have more similar climatic niches and P‐matrices than distantly related species, suggesting phylogenetic niche conservatism. We infer that the modularity signal due to embryonic origin of bones, which happens early in ontogeny, is blurred by the process of growth that occurs later in ontogeny. We suggest that the species differing in the preferred modularity model have different demands on the orbital functional unit and that species contrasting in climate are subjected to divergent patterns of natural selection associated to neurocranial allometry and T3 hormone regulation.     

Chewing on the trees: Constraints and adaptation in the evolution of the primate mandible

Chewing on different food types is a demanding biological function. The classic assumption in studying the shape of feeding apparatuses is that animals are what they eat, meaning that adaptation to different food items accounts for most of their interspecific variation. Yet, a growing body of evidence points against this concept. We use the primate mandible as a model structure to investigate the complex interplay among shape, size, diet, and phylogeny. We find a weak but significant impact of diet on mandible shape variation in primates as a whole but not in anthropoids and catarrhines as tested in isolation. These clades mainly exhibit allometric shape changes, which are unrelated to diet. Diet is an important factor in the diversification of strepsirrhines and platyrrhines and a phylogenetic signal is detected in all primate clades. Peaks in morphological disparity occur during the Oligocene (between 37 and 25 Ma) supporting the notion that an adaptive radiation characterized the evolution of South American monkeys. In all primate clades, the evolution of mandible size is faster than its shape pointing to a strong effect of allometry on ecomorphological diversification in this group.