Allometry and evolution in the galago skull

To probe the ontogenetic bases of morphological diversity across galagos, we performed the first clade-wide analyses of growth allometries in 564 adult and non-adult crania from 12 galagid taxa. In addition to evaluating if variation in galago skull form results from the differential extension/truncation of common ontogenetic patterns, scaling trajectories were employed as a criterion of subtraction to identify putative morphological adaptations in the feeding complex. A pervasive pattern of ontogenetic scaling is observed for facial dimensions across galagids, with 2 genera also sharing relative growth trajectories for masticatory proportions (Galago, Galagoides). As the facial growth series and adult data are largely coincidental, interspecific variation may result from character displacement and consequent selection for size differentiation among sister taxa. Derived configurations of the jaw joint and jaw muscle mechanical advantage in Otolemur and Euoticus appear to facilitate increased gape during scraping behaviors. Differences in aspects of masticatory growth and form characterizing these 2 genera highlight selection to uncouple shared ontogenetic patterns, which occurred via transpositions that retained ancestral scaling patterns. Due to the lack of increased robusticity of load-resisting mandibular elements in Otolemur and Euoticus, there is little evidence to suggest that exudativory in galagos results in correspondingly higher masticatory stresses.     

Patterns of intraspecific variation through ontogeny: a case study of the Cretaceous nautilid Eutrephoceras dekayi and modern Nautilus pompilius

The magnitude and ontogenetic patterns of intraspecific variation can provide important insights into the evolution and development of organisms. Understanding the intraspecific variation of organisms is also a key to correctly pursuing studies in major fields of palaeontology. However, intraspecific variation has been largely overlooked in ectocochleate cephalopods, particularly nautilids. Furthermore, little is known regarding the evolutionary pattern. Here, we present morphological data for the Cretaceous nautilid Eutrephoceras dekayi (Morton) and the modern nautilid Nautilus pompilius Linnaeus through ontogeny. The data are used to describe conch morphology and to elucidate the evolutionary patterns of intraspecific variation. We discovered a similar overall pattern of growth trajectories and the presence of morphological changes at hatching and maturity in both taxa. We also found that intraspecific variation is higher in earlier ontogeny than in later ontogeny in both taxa. The high variation in earlier ontogeny may imply increased flexibility in changing the timing of developmental events, which probably played an important role in nautilid evolution. We assume that the decrease in variation in later ontogeny reflects developmental constraints. Lastly, we compared the similarity/dissimilarity of ontogenetic patterns of variation between taxa. Results reveal that the similarity/dissimilarity of the ontogenetic pattern differs between E. dekayi and N. pompilius. We conclude that this shift in the ontogenetic pattern of variation may be rooted in changes in the developmental programme of nautilids through time. We propose that studying ontogenetic patterns of intraspecific variation can provide new insights into the evolution and development of organisms.     

Ontogeny and phyletic size change in living and fossil lemurs

Lemurs are notable for encompassing the range of body‐size variation for all primates past and present—close to four orders of magnitude. Benefiting from the phylogenetic proximity of subfossil lemurs to smaller‐bodied living forms, we employ allometric data from the skull to probe the ontogenetic bases of size differentiation and morphological diversity across these clades. Building upon prior pairwise comparisons between sister taxa, we performed the first clade‐wide analyses of craniomandibular growth allometries in 359 specimens from 10 lemuroids and 176 specimens from 8 indrioids. Ontogenetic trajectories for extant forms were used as a criterion of subtraction to evaluate morphological variation, and putative adaptations among sister taxa. In other words, do species‐level differences in skull form result from the differential extension of common patterns of relative growth? In lemuroids, a pervasive pattern of ontogenetic scaling is observed for facial dimensions in all genera, with three genera also sharing relative growth trajectories for jaw proportions (Lemur, Eulemur, Varecia). Differences in masticatory growth and form characterizing Hapalemur and fossil Pachylemur likely reflect dietary factors. Pervasive ontogenetic scaling characterizes the facial skull in extant Indri, Avahi, and Propithecus, as well as their larger, extinct sister taxa Mesopropithecus and Babakotia. Significant interspecific differences are observed in the allometry of indrioid masticatory proportions, with variation in the mechanical advantage of the jaw adductors and stress‐resisting elements correlated with diet. As the growth series and adult data are largely coincidental in each clade, interspecific variation in facial form may result from selection for body‐size differentiation among sister taxa. Those cases where trajectories are discordant identify potential dietary adaptations linked to variation in masticatory forces during chewing and biting. Although such dissociations highlight selection to uncouple shared ancestral growth patterns, they occur largely via transpositions and retention of primitive size‐shape covariation patterns or relative growth coefficients. Am. J. Primatol. 72:161–172, 2010. © 2009 Wiley‐Liss, Inc.     

Limb morphology of domestic and wild canids: the influence of development on morphologic change

Biomechanical hypotheses are often invoked to explain the characteristic scaling of limb proportions. Patterns of static allometry and morphologic diversity, however, may also reflect the developmental mechanisms underlying morphologic change. In this study I document the importance of such developmental influences on the evolution of limb morphology in the extremely polymorphic domestic dog and in wild canid species. I use bivariate and discriminant function analyses to compare the limb morphology of adult dogs and wild canid species. I then compare ontogenetic allometry of four dog breeds with static allometry of domestic and wild canids. Results reveal, first, that there is considerable similarity between dogs and wild canid species; many wolf-like canids cannot be distinguished from domestic dogs of equivalent size. However, all dogs are consistently separated from fox-sized, wild canids by subtle but evolutionarily significant differences in olecranon, metapodial, and scapula morphology. Second, in domestic dogs the pattern of static allometry is nearly identical to that of ontogenetic allometry. This finding can be attributed to simple heterochronic alterations of postnatal growth rates. Apparently the diversity of limb proportions among adult domestic dogs and the observed difference between dogs and wild canids are somewhat predetermined, as they directly reflect the diversity of limb proportions evident during development of the domestic dog.     

HETEROCHRONY WITHIN SPECIES: CRANIOFACIAL GROWTH IN GIANT,STANDARD, AND DWARF RABBITS

Change in developmental timing is one source of heritable variation upon which selection can act. However, the amount of variation possible in ontogenetic trajectories is often unknown. We used three different-sized conspecific breeds of domestic rabbits to investigate the extent of variation in growth trajectories of craniofacial morphology. The growth and adult morphology of several structures (one soft tissue and 15 skeletal) were quantified and analyzed. We took two views of radiographs at close time intervals throughout ontogeny, from one week of age through adult size. Measurements from the radiographs were analyzed using a Gompertz growth model. Between-breed differences in model parameters were tested using one-way ANOVA. Few significant differences existed between the white and giant rabbits, but several differences were found between the white and dwarf breeds. Similarly, comparisons of adult morphology showed that white and giant rabbits are the same shape, while dwarf rabbits have shorter and broader snouts than white rabbits. The variation in size among breeds appeared to be due to differences in the length of time spent growing at rates near the maximum growth rate. While no one parameter of this model quantifies this pattern, differences in duration of maximum growth rate can be seen in the first derivative of the growth trajectory. Small changes in the model's parameters that measure rate and timing of growth have large morphological consequences, indicating that heterochronic changes are important sources of variation.     

In vivo bone strain and ontogenetic growth patterns in relation to life-history strategies and performance in two vertebrate taxa: goats and emu

This study examined ontogenetic patterns of limb loading, bone strains, and relative changes in bone geometry to explore the relationship between in vivo mechanics and size-related changes in the limb skeleton of two vertebrate taxa. Despite maintaining similar relative limb loads during ontogeny, bone strain magnitudes in the goat radius and emu tibiotarsus generally increased. However, while the strain increases in the emu tibiotarsus were mostly insignificant, strains within the radii of adult goats were two to four times greater than in young goats. The disparity between ontogenetic strain increases in these taxa resulted from differences in ontogenetic scaling patterns of the cross-sectional bone geometry. While the cross-sectional and second moments of area scaled with negative allometry in the goat radius, these measures were not significantly different from isometry in the emu tibiotarsus. Although the juveniles of both taxa exhibited lower strains and higher safety factors than the adults, the radii of the young goats were more robust relative to the adult goats than were the tibiotarsi of the young compared with adult emu. Differences in ontogenetic growth and strain patterns in the limb bones examined likely result from different threat avoidance strategies and selection pressures in the juveniles of these two taxa.     

Relative growth of the limbs and trunk in the African apes

Examination of relative growth and allometry is important for our understanding of the African apes, as they represent a closely related group of species of increasing body size. This study presents a comparison of ontogenetic relative growth patterns of some postcranial dimensions in Pan paniscus, Pantroglodytes, and Gorilla gorilla. Interspecific proportion differences among the three species are also analyzed. It is stressed that reliable ontogenetic information can only be obtained if subadults are examined-growth data cannot be inferred from static adult scaling. Results indicate that some postcranial relative growth patterns are very similar in the three species, suggesting differential extrapolation of a common growth pattern, whereas for other proportion comparisons the growth trends differ markedly among the species, producing distinct shape differences in the adults Interspecific shape changes among the three species are characterized by positive allometry of chest girth and negative allometry of body height and leg length. It is suggested that relative decrease of leg length with increasing body size among the African pongids might be expected on biomechanical grounds, in order to maintain similar locomotor abilities of climbing arborealism and quadrupedal terrestrialism. Relative to body weight or trunk length, the limbs of the bonobo (Pan paniscus) are longer than in the common chimpanzee or the gorilla, with a lower intermembral index. This may most closely resemble the primitive condition for the African apes.     

滇金丝猴,藏酋猴和毛耳猴下颌骨的异速生长

本文对滇金丝猴(Rhinopithecus bieti)、藏酋猴(Macaca thibetana)和毛耳猴(Macacamulatta lasiota)下颌骨的33项指标进行了测量.经分析,下颌骨的生长存在有部位间、左右间及类群间的差异。表明这些动物下颌骨形态因适应某种生态环境而可能存在某些相似性,但因其食物性质、取食行为、系统及个体发育过程中存在差异而出现不同的生长模式。     

Craniofacial sexual dimorphism in Alouatta palliata, the mantled howling monkey

Ontogenetic scaling has been hailed as an explanation of the differences in craniofacial morphology between adult males and females of a number of non human primate species. This inference has implications for the evolutionary processes underlying patterns of sexual variation, as several heterochronic processes (rate and time hypo- and hypermorphosis) predict ontogenetic scaling. Primary among species for which ontogenetic scaling of craniofacial dimensions has been claimed is Alouatta palliata , the mantled howling monkey. This study uses a variety of analytical tools to explore the efficacy of ontogenetic scaling as an explanatory paradigm for this classic example. Multivariate analysis captures shape far better than does bivariate analysis. However, multivariate analysis does not support the traditional inference of ontogenetic scaling. Explanations for contradictory results are considered.     

An ontogenetic perspective on the study of sexual dimorphism, phylogenetic variability, and allometry of the skull of European ground squirrel, Spermophilus citellus (Linnaeus, 1766)

Most studies of morphological variability in or among species are performed on adult specimens. However, it has been proven that knowledge of the patterns of size and shape changes and their covariation during ontogeny is of great value for the understanding of the processes that produce morphological variation. In this study, we investigated the patterns of sexual dimorphism, phylogenetic variability, and ontogenetic allometry in the Spermophilus citellus with geometric morphometrics applied to cross-sectional ontogenetic data of 189 skulls from three populations (originating from Burgenland, Banat, and Dojran) belonging to two phylogenetic lineages (the Northern and Southern). Our results indicate that sexual dimorphism in the ventral cranium of S. citellus is expressed only in skull size and becomes apparent just before or after the first hibernation because of accelerated growth in juvenile males. Sexes had the same pattern of ontogenetic allometry. Populations from Banat and Dojran, belonging to different phylogroups, were the most different in size but had the most similar adult skull shape. Phylogenetic relations among populations, therefore, did not reflect skull morphology, which is probably under a significant influence of ecological factors. Populations had parallel allometric trajectories, indicating that alterations in development probably occur prenatally. The species’ allometric relations during cranial growth showed characteristic nonlinear trajectories in the two northern populations, with accelerated shape changes in juveniles and continued but almost isometric growth in adults. The adult cranial shape was reached before sexual maturity of both sexes and adult size after sexual maturity. The majority of shape changes during growth are probably correlated with the shift from a liquid to a solid diet and to a lesser degree due to allometric scaling, which explained only 20 % of total shape variation. As expected, viscerocranial components grew with positive and neurocranial with negative allometry.     

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.     

Relationships among ontogenetic,static, and evolutionary allometry

The relationship between ontogenetic, static, and evolutionary levels of allometry is investigated. Extrapolation from relative size relationships in adults to relative growth in ontogeny depends on the variability of slopes and intercepts of ontogenetic vectors relative to variability in length of the vector. If variability in slopes and intercepts is low relative to variability in length, ontogenetic and static allometries will be similar. The similarity of ontogenetic and static allometries was tested by comparing the first principal component, or size vector, for correlations among 48 cranial traits in a cross-sectional ontogenetic sample of rhesus macaques from Cayo Santiago with a static sample from which all age- and sex-related variation had been removed. The vector correlation between the components is high but significantly less than one while two of three allometric patterns apparent in the ontogenetic component are not discernable in the static component. This indicates that there are important differences in size and shape relationships among adults and within ontogenies. Extrapolation from intra- or interspecific phenotypic allometry to evolutionary allometry is shown to depend on the similarity of genetic and phenotypic allometry patterns. Similarity of patterns was tested by comparing the first principal components of the phenotypic, genetic, and environmental correlation matrices calculated using standard quantitative genetic methods. The patterns of phenotypic, genetic, and environmental allometry are dissimilar; only the environmental allometries show ontogenetic allometric patterns. This indicates that phenotypic allometry may not be an accurate guide to patterns of evolutionary change in size and shape.     

Fossil evidence of evolutionary convergence in juvenile dental morphology and upper canine replacement in sabertooth carnivores

The convergent suite of morphological traits characterizing the mammalian sabertooth ecomorphology is well documented, including modifications of the dental and osteological portions of the masticatory apparatus from a less‐specialized carnivore condition. Equally important is how those specialized adult morphologies developed through ontogeny because previous studies have shown that growing such specialized craniodental traits may require evolutionary modification of growth patterns and tooth replacement mechanisms. Despite the understanding of convergent morphological specialization in adult sabertooth carnivores, the possibility of a convergent ontogenetic trajectory toward those adult morphologies has not been rigorously examined. The present study examines numerous previously undescribed juvenile nimravid specimens. The results provide insights about nimravid ontogeny and show, for the first time, that the nimravid sabertooth lineage included species in which the permanent upper canine erupted within a lingual concavity of the deciduous upper canine until it reached comparable crown height beyond the alveolar border. Furthermore, this investigation assesses the juvenile morphology and upper canine replacement of felid and barbourofelid sabertooth taxa. The results provide evidence of convergence in deciduous upper canine morphology of three sabertooth carnivore lineages (i.e., nimravid, felid, and barbourofelid), as well as preliminary evidence of convergence in the upper canine replacement process. It might be beneficial for studies of extreme morphological specialization to simultaneously consider convergence in adult morphologies and how morphologies change through ontogeny.     

Scapula form and locomotion in chimpanzee evolution

A number of primatologists have followed Coolidge (Am. J. Phys. Anthropol. 18:1–57, 1933) in suggesting that 1) there are significant shape differences in scapula form between pygmy and common chimpanzees, 2) scapulae of P. paniscus resemble those of hylobatids more than do those of P. troglodytes, and 3) therefore pygmy chimpanzees may exhibit a greater component of arm-swinging and other arboreal behaviors than common chimpanzees. In this paper I utilize a comparative analysis of ontogenetic allometries of linear dimensions to determine shape differences in the scapulae of adult pygmy and common chimpanzees and to clarify size-related changes in shape resulting from ontogenetic scaling, i.e., the differential extension of common patterns of growth allometry. Results demonstrate that the scapulae of adult P. paniscus are relatively narrower (in a direction approximately perpendicular to the scapula spine) than those of P. troglodytes, supporting Coolidge's original claim. The allometric analysis further demonstrates, however, that the two chimpanzee species exhibit ontogenetic scaling for all proportions of the scapula examined. Thus, adult pygmy chimpanzees have the scapula proportions observed in small adult and subadult P. troglodytes of comparable scapula size. The implications of this finding for past claims concerning differences in locomotor behavior between the species are discussed. This work lends additional support to previous studies that have demonstrated a high frequency of ontogenetic scaling within the genus Pan and a pedomorphic or juvenilized morphology in the pygmy chimpanzee.     

Comparative growth in the postnatal skull of the extant North American turtle Pseudemys texana (Testudinoidea: Emydidae)

Bever, G.S. 2007. Comparative growth in the postnatal skull of the extant North American turtle Pseudemys texana (Testudinoidea: Emydidae). —Acta Zoologica (Stockholm) 88 : 000–000 Postnatal growth is one of the many aspects of developmental morphology that remains distinctly understudied in reptiles. Variation and ontogenetic scaling within the skull of the extant emydid turtle, Pseudemys texana is described based on 25 continuous characters. Results indicate that skull shape in this species changes little during postnatal growth relative to the only cryptodire taxa for which comparable datasets are available (Apalone ferox and Sternotherus odoratus). This relative lack of change results in the paedomorphic retention of a largely juvenile appearance in the adult form of P. texana. The skulls of males and females, despite the presence of distinct sexual dimorphism in size, grow with similar scaling patterns, and the few observed differences appear to reflect alteration of the male growth trajectory. Comparisons with A. ferox and S. odoratus reveal a number of similarities and differences that are here interpreted within a phylogenetic context. These preliminary hypotheses constitute predictive statements that phylogenetically bracket the majority of extant cryptodire species and provide baseline comparative data that are necessary for the future recognition of apomorphic transformations. Plasticity of ontogenetic scaling as a response to the homeostatic needs and behaviour of individuals commonly is evoked as a limitation of ontogenetic scaling as a means to inform phylogenetic studies. These evocations are largely unfounded considering that variability itself can evolve and thus be phylogenetically informative.     

Ontogeny, phylogeny, and morphology in anuran larvae: morphometric analysis of cranial development and evolution in Rana tadpoles (Anura: Ranidae)

Comparative studies of chondrocranial morphology in larval anurans are typically qualitative in nature, focusing primarily on discrete variation or gross differences in the size or shape of individual structures. Detailed data on chondrocranial allometry are currently limited to only two species, Rana sylvatica and Bufo americanus. This study uses geometric morphometric and multivariate statistical analyses to examine interspecific variation in both larval chondrocranial shape and patterns of ontogenetic allometry among six species of Rana. Variation is interpreted within the context of hypothesized phylogenetic relationships among these species. Canonical variates analyses of geometric morphometric datasets indicate that species can be clearly discriminated based on chondrocranial shape, even when whole ontogenies are included in the analysis. Ordinations and cluster analyses based on chondrocranial shape data indicate the presence of three primary groupings (R. sylvatica; R. catesbeiana + R. clamitans; and R. palustris + R. pipiens + R. sphenocephala), and patterns of similarity closely reflect phylogenetic relationships. Analysis of chondrocranial allometry reveals that some patterns are conserved across all species (e.g., most measurements scale with negative allometry, those associated with the posterior palatoquadrate tend to scale with isometry or positive allometry). Ontogenetic scaling along similar allometric trajectories, lateral transpositions of individual trajectories, and variable allometric relationships all contribute to shape differences among species. Overall patterns of similarity among ontogenetic trajectories also strongly reflect phylogenetic relationships. Thus, this study demonstrates a tight link between ontogeny, phylogeny, and morphology, and highlights the importance of including both ontogenetic and phylogenetic data in studies of chondrocranial evolution in larval anurans.     

CRANIAL MORPHOLOGY OF DOMESTIC AND WILD CANIDS: THE INFLUENCE OF DEVELOPMENT ON MORPHOLOGICAL CHANGE

The domestic dog varies remarkably in cranial morphology. In fact, the differences in size and proportion between some dog breeds are as great as those between many genera of wild canids. In this study, I compare patterns of intracranial allometry and morphologic diversity between the domestic dog and wild canid species. The results demonstrate that the domestic dog is morphologically distinct from all other canids except its close relatives, the wolf-like canids. Following this, I compare patterns of static and ontogenetic scaling. Data on growth of domestic dogs are presented and used to investigate the developmental mechanisms underlying breed evolution. Apparently, most small breeds are paedomorphic with respect to certain morphologic characters. In dogs and other domestic animals, morphologic diversity among adults seems to depend on that expressed during development.     

Allometric relations in three species of finches (Aves: Fringillidae)

Static nestling, adult and ontogenetic allometry were analysed in three species of finches. Static nestling allometry was very similar across age in early ontogeny and among species and could be approximated by a single matrix of phenotypic variances and covariances. The first eigenvector of this matrix showed negative allometry of bill and tarsus to mass, but positive for wing length to mass. Adult static allometry was also very similar among species, but differed from nestling pattern. In adults the bill had a positive allometry in relation to tarsus and wing, but negative to mass, while tarsus and wing were unrelated to mass. The ontogenetic allometry in each species was very similar to nestling static allometry. Viewed in relation to final size, bill characters grew more slowly than body characters, but for a longer time, which created the difference between adult and nestling allometric patterns. There were differences among species both with regard to elevation and slope of allometric coefficients, suggesting that the differences among species came about by changes in the three fundamental ontogenetic parameters namely growth rate, onset of growth and offset of growth.     

The effects of hybridization on growth allometry and craniofacial form in Sulawesi macaques

The present research investigates the effects of hybridization between Macaca maurus and M. tonkeana on adult male form and patterns of growth allometry. Comparisons of adult hybrid mean phenotypic values with the adult averages of the parental species indicate a condition of heterosis for cranial vault length and crown-rump length. Negative heterosis is indicated for body mass. Regression parameters describing growth allometry are generated for four craniofacial measurement variables and one body measurement using both least squares and reduced major axis regression. Comparisons of hybrid and parental regression slopes and intercepts using analysis of covariance and t-tests suggest that there is a hybrid pattern of growth allometry characterized by an increase in regression slope values coupled with lower intercept values compared to those of the parental species and the parental averages for most regression parameters. Multivariate analyses of the adult and ontogenetic morphometric data indicate significant differences across species taxa in form and shape during development and adulthood. Our finding of significant differences between hybrids and their parental taxa in growth allometry and craniofacial form and shape during development challenges the assumption often made regarding the reproductive and taxonomic significance of observed ontogenetic divergence between Neandertals and modern humans. We propose that anthropological primatology, with its goal of developing nonhuman primate models for investigating human evolution, can provide a biologically relevant means by which to empirically estimate the taxonomic significance of morphological and ontogenetic divergence observed in the hominid fossil record.