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.     

AN ALMOST COMPLETE JUVENILE SPECIMEN OF THE CHELONIID TURTLE CTENOCHELYS STENOPORUS (HAY, 1905) FROM THE UPPER CRETACEOUS NIOBRARA FORMATION OF KANSAS,USA

Abstract: A new, unusually well‐preserved juvenile specimen of Ctenochelys stenoporus from the Niobrara Formation is described. The skull has come apart at its sutures and all bones of the braincase and ear region are preserved three‐dimensionally. This allows a detailed reconstruction of the important brain structures of a basal juvenile cheloniid turtle. It is compared with adult Ctenochelys specimens, and the major ontogenetic changes in the skull and postcranial skeleton are described. Furthermore, the specimen is compared with other fossil and extant cheloniids with well‐known braincases and the differences between basal and advanced cheloniids turtles are specified.     

Turtle carotid circulation: a character analysis case study

The bony canals permeating the turtle skull associated with the cranial circulation have long been considered integral to an understanding of extinct and extant turtle systematics. Recent phylogenetic analyses, employing a variety of data sets, suggest alternatives to the traditional arrangement of crown turtles. Of particular note is the recent failure of investigations employing molecular techniques to retrieve a monophyletic Trionychoidea, a clade supported largely by shared circulatory features. These alternative phylogenies may also have implications for extinct forms. The turtle cranial arterial circulation therefore represents an ideal system upon which to conduct a detailed, multipronged analysis of a systematically influential character. In the present study, the theoretical underpinnings of character analysis are critically evaluated, and a new interpretation of circulatory variation in turtles is offered, including a revised phylogenetic character suite. This assessment indicates an autapomorphic circulatory pattern in Trionychia, whereas Trionychoidea is not supported.  © 2008 The Linnean Society of London, Biological Journal of the Linnean Society , 2008, 93 , 239–256.     

A quantitative approach to the cranial ontogeny of the puma

The cranial ontogeny of specialized mammals is relevant to the understanding of the connection of form and function in a developmental, ecological, and evolutionary context. As highly specialized carnivores, felids are of especial interest. We studied the postnatal ontogeny of the skull in Puma concolor (Mammalia: Carnivora: Felidae) using a quantitative approach. We interpreted our results in the light of a previous qualitative assessment of ontogenetic changes in the species. This represents one of the few integrative studies of skull development in any extant species of wild felids. We report patterns of multivariate allometry of 19 linear skull dimensions measured in 48 Argentine specimens. We examined the (jackknife resampled) departures from isometry as well as the interplay of isometric and allometric trends in shaping the puma skull. Both the qualitative and quantitative results indicate that the major ontogenetic changes are directly linked to cranial structures that support a developing masticatory apparatus and its associated jaw and neck musculature, which are essential for the action of canines and carnassials during the killing bite and slicing flesh. Sexual differences suggest allometric scaling (hypo- or hyper-morphosis) as key processes in the development of the puma skull.     

The cranial morphology of Kayentachelys,an Early Jurassic cryptodire,and the early history of turtles

Gaffney, E.S. and Jenkins, F.A., Jr. 2010. The cranial morphology of Kayentachelys, an Early Jurassic cryptodire, and the early history of turtles. — Acta Zoologica (Stockholm) 91 : 335–368 The skull morphology of Kayentachelys aprix Gaffney et al., 1987 , a turtle from the Early Jurassic Kayenta Fm of northern Arizona, demonstrates the presence of cryptodiran synapomorphies in agreement with Gaffney et al. (1987, 1991, 2007) , and contrary to the conclusions of Sterli and Joyce (2007) , Joyce (2007) , Sterli (2008) , and Anquetin et al. (2008) . Specific characters found in Kayentachelys and diagnostic of cryptodires include the processus trochlearis oticum, the curved processus pterygoideus externus with a vertical plate, and the prefrontal–vomer contact, which are confirmed as absent in the outgroups, specifically the Late Triassic Proganochelys. The Joyce (2007) analysis suffers from the reduction of the signal from skull characters, with a consequently greater reliance on shell characters, resulting in pleurodires being resolved at various positions within the cryptodires. Kayentachelys reveals what a primitive cryptodire would be expected to look like: a combination of primitive and derived characters, with the fewer derived characters providing the best test of its relationships to other turtles. Although incompletely known, the Mid‐Late Jurassic Condorchelys, Heckeremys, and Eileanchelys may be early cryptodires close to Kayentachelys. We confirm the Late Triassic Proterochersis as a pleurodire, dating the pleurodire–cryptodire split as Late Triassic or earlier.     

Interspecific variation of ontogeny and skull shape among porpoises (Phocoenidae)

All extant members of Phocoenidae (porpoises) have been characterized as pedomorphic based on skeletal characters. To investigate the ontogenetic background for pedomorphosis and assess interspecific differences in ontogeny among phocoenids, samples of the six extant species were compared in terms of development of both epiphyseal and cranial suture fusion. Across all species, full maturity of the vertebral column was rare. Vertebral epiphyseal development did not progress so far in most Phocoena phocoena as in Phocoenoides dalli and Phocoena dioptrica. P. phocoena, Phocoena spinipinnis, Ph. dalli, and P. dioptrica, for which large series were available, were further compared in terms of ontogeny of cranial shape by three‐dimensional geometric morphometrics. Ph. dalli and P. dioptrica generally showed further development of cranial sutures than the other species. Postnatal skull shape development was similar for all species studied; the majority of interspecific shape differences are present at parturition. Smaller species had a higher rate of shape development relative to growth in size than Ph. dalli and P. dioptrica, but they still showed less allometric development due to less postnatal growth. Interspecific shape differences indicate phylogenetic relationships similar to that proposed based on morphology or convergent evolution of the two pelagic species, Ph. dalli and P. dioptrica, under the scenarios suggested by recent molecular studies. A shape trend coinciding with habitat preference was detected; in species with pelagic preference the position and orientation of the foramen magnum aligned the skull with the vertebral column; the rostrum showed less ventral inclination, and the facial region was larger and more concave in lateral aspect. J. Morphol., 2011. © 2010 Wiley‐Liss, Inc.     

Ontogeny of skull size and shape changes within a framework of biphasic lifestyle: a case study in six <Emphasis Type="Italic">Triturus</Emphasis> species (Amphibia,Salamandridae)

As with many other amphibians, Triturus species are characterized by a biphasic life cycle with abrupt changes in the cranial skeleton during metamorphosis. The post-metamorphic shape changes of the cranial skeleton were investigated using geometric morphometric techniques in six species: Triturus alpestris, T. vulgaris, T. dobrogicus, T. cristatus, T. carnifex, and T. karelinii. The comparative analysis of ontogenetic trajectories revealed that these species have a conserved developmental rate with divergent ontogenetic trajectories of the ventral skull shape that mainly reflect phylogenetic relatedness. A striking exception in the ontogenetic pattern was possibly found in T. dobrogicus, characterized by a marked increase in the developmental rate compared to the other newt species. The size-related shape changes explained a large proportion of shape change during post-metamorphic growth within each species, with marked positive allometric growth of skull elements related to foraging.     

An exploration of differences in the scaling of life history traits with body mass within reptiles and between amniotes

Allometric relationships linking species characteristics to body size or mass (scaling) are important in biology. However, studies on the scaling of life history traits in the reptiles (the nonavian Reptilia) are rather scarce, especially for the clades Crocodilia, Testudines, and Rhynchocephalia (single extant species, the tuatara). Previous studies on the scaling of reptilian life history traits indicated that they differ from those seen in the other amniotes (mammals and birds), but so far most comparative studies used small species samples and also not phylogenetically informed analyses. Here, we analyzed the scaling of nine life history traits with adult body mass for crocodiles (n = 22), squamates (n = 294), turtles (n = 52), and reptiles (n = 369). We used for the first time a phylogenetically informed approach for crocodiles, turtles, and the whole group of reptiles. We explored differences in scaling relationships between the reptilian clades Crocodilia, Squamata, and Testudines as well as differences between reptiles, mammals, and birds. Finally, we applied our scaling relationships, in order to gain new insights into the degree of the exceptionality of the tuatara's life history within reptiles. We observed for none of the life history traits studied any difference in their scaling with body mass between squamates, crocodiles, and turtles, except for clutch size and egg weight showing small differences between these groups. Compared to birds and mammals, scaling relationships of reptiles were similar for time‐related traits, but they differed for reproductive traits. The tuatara's life history is more similar to that of a similar‐sized turtle or crocodile than to a squamate.     

Cranial anatomy and systematics of Hypacrosaurus altispinus,and a comparative analysis of skull growth in lambeosaurine hadrosaurids (Dinosauria: Ornithischia)

The cranial anatomy of the helmet‐crested lambeosaurine Hypacrosaurus altispinus (Ornithischia: Hadrosauridae) is described, with a focus on ontogenetic and individual variation in phylogenetically significant characters of the cranial crest, braincase, and facial skeleton. Cranial material of H. altispinus represents a relatively complete growth series that includes crestless juveniles of less than half the size of large individuals with fully developed crests. Cranial ontogeny is compared with other lambeosaurines using bivariate morphometrics and through qualitative comparison of a size‐standardized cranial growth series. Bivariate analyses reveal that the relative growth of the skull and cranial crest of H. altispinus and H. stebingeri are similar, and that Hypacrosaurus more closely resembles Corythosaurus than Lambeosaurus. Hypacrosaurus altispinus is systematically revised. The taxon is characterized by five autapomorphies, most of which are concentrated in the skull, as well as an enlarged terminal ischial foot. Maximum parsimony and Bayesian likelihood (Mk+gamma) phylogenetic analyses were conducted to test the monophyly of the genus. Hypacrosaurus monophyly is corroborated in light of new anatomical data. Although H. stebingeri and H. altispinus share few derived characters of the skull, the hypothesis that H. stebingeri is a metaspecies that represents the ancestor of H. altispinus cannot be rejected. © 2010 The Linnean Society of London, Zoological Journal of the Linnean Society, 2010, 159 , 398–434.     

Influence of precipitation pulses on long-term <Emphasis Type="Italic">Prosopis ferox</Emphasis> dynamics in the Argentinean intermontane subtropics

Biological processes in arid communities are associated with episodic precipitation pulses. We postulate that annual to decadal-scale precipitation pulses modulate the dynamics of the intermontane Prepuna woodlands. To study this hypothesis, we have assessed the influence of precipitation pulses on the rates of growth and survival of Prosopis ferox in the Prepuna woodlands during the past century. Tree ages from several P. ferox stands were used to reconstruct the establishment patterns at each sampling site. Ring-width chronologies provided the basis to assess the influence of annual versus multiannual precipitation pulses on radial growth and establishment over time. Both the radial growth and the stand dynamics of P. ferox at the regional scale were found to be largely modulated by climate, with precipitation the dominant factor influencing interannual variations in P. ferox ring-widths. Our analysis of dendrochronological dating data on 885 individuals of P. ferox revealed a period of abundant establishment from the mid-1970s to beginning of 1990s, which is coincident with an interval of remarkable above-average precipitation. However, tree-growth and establishment patterns at the local scale in the Prepuna also reflected land-use changes, particularly long-term variations in livestock intensity. The P. ferox dynamics documented here substantiates the hierarchical concept of “resource-pulse” in dry ecosystems, with precipitation pulses of different lengths modulating distinct dynamic processes in the P. ferox woodlands. Interannual variations in precipitation influence year-to-year patterns of P. ferox radial growth, whereas multiannual oscillations in rainfall influence episodic events of tree establishment. The long-term interval considered in this study enabled us to disentangle the roles of natural versus human controls on P. ferox dynamics in the region.     

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.     

Evolution of ontogeny in the hippopotamus skull: using allometry to dissect developmental change

Allometry describes the effect of size change on aspects of an organism's form and can be used to summarize the developmental history of growing parts of an animal. By comparing how allometric growth differs between species, it is possible to reveal differences in their pathways of development. The ability to compare and categorize developmental change between species is demonstrated here using morphometric methods. This involves the interspecific statistical comparison of a large number of bivariate relationships that summarize ontogenetic trajectories. These linear ontogenetic trajectories can be modified as they evolve in any of three ways: ontogenetic scaling indicative of change in the duration of growth, lateral shifts indicative of changes in prenatal development, and directional change indicative of novel modes of postnatal growth. I apply this analysis to skulls of the common hippopotamus ( Hippopotamus amphibius ) and the pygmy hippopotamus ( Hexaprotodon liberiensis ). The number of allometric changes falling into each category was statistically determined and Jolicoeur's multivariate generalization of simple allometry was used to provide an overview of cranial variation. For these skulls, directional change was not found to be statistically significant, but ontogenetic scaling and lateral shifts were both common. This indicates that conserved patterns of growth covariance (ontogenetic scaling) can be separated from novel or derived patterns (directional change and/or lateral shifts). This study demonstrates that He. liberiensis is not simply an ontogenetically scaled version of its larger relative. The evolutionary implications of allometric growth variation are discussed in the light of these findings and those of other studies.  © 2003 The Linnean Society of London, Biological Journal of the Linnean Society , 2003, 80 , 625–638.     

The ontogeny of feeding kinematics in a giant salamander Cryptobranchus alleganiensis: Does current function or phylogenetic relatedness predict the scaling patterns of movement?

Studies of the scaling of feeding movements in vertebrates have included three species that display both near-geometric growth and isometry of kinematic variables. These scaling characteristics allow one to examine the “pure” relationship of growth and movement. Despite similar growth patterns, the feeding movements of toads (Bufo) slow down more with increasing body size than those of bass (Micropterus), and sharks (Ginglymostoma). This variation might be due to major differences in the mechanism of prey capture; the bass and sharks use suction to capture prey in water, while the toad uses tongue prehension to capture prey on land. To investigate whether or not these different scaling patterns are correlated with differences in feeding mechanics, we examined the ontogenetic scaling of prey capture movements in the hellbender salamander (Cryptobranchus alleganiensis), which also has near-geometric growth. The hellbender suction feeds in the same general manner as the teleosts and shark, but is much more closely related to the toad. The feeding movements of the hellbender scale more similarly to the feeding movements of toads than to those of fishes or sharks, indicating that phylogenetic relatedness rather than biomechanical similarity predicts ontogenetic scaling patterns of movement.     

Comparative ontogenetic shape changes in the skull of Caiman species (Crocodylia,Alligatoridae)

Ontogenetic shape changes in the skull of three species of the genus Caiman (C. latirostris, C. sclerops, and C. yacare) are compared by geometric morphometrics for three-dimensional configurations (the least-squares analysis). The technique for obtaining the landmark coordinates is a simplification of the algorithm for multidimensional scaling. The ontogenetic nonlinear shape changes are similar in the three species but occur in a lesser extent in C. latirostris. These seem to be correlated with functional changes in the skull. The uniform shape change corresponds to an elongation of the skull, dorsoventral flattening, and lateral compression in C. sclerops and C. yacare. There is some lateral broadening in C. latirostris. Differences in the ontogenetic processes probably cause the differences in diet observed between C. latirostris and the other two species. Neotenic evolution seems to have acted in the skull of C. latirostris, and a posterior amplification of the early divergence led to a repatterning of the shape ontogenetic trajectory in this species. J. Morphol. 231:53–62, 1997. © 1997 Wiley-Liss, Inc.     

Postnatal temporal bone ontogeny in Pan,Gorilla, and Homo,and the implications for temporal bone ontogeny in Australopithecus afarensis

Assessments of temporal bone morphology have played an important role in taxonomic and phylogenetic evaluations of fossil taxa, and recent three‐dimensional analyses of this region have supported the utility of the temporal bone for testing taxonomic and phylogenetic hypotheses. But while clinical analyses have examined aspects of temporal bone ontogeny in humans, the ontogeny of the temporal bone in non‐human taxa is less well documented. This study examines ontogenetic allometry of the temporal bone in order to address several research questions related to the pattern and trajectory of temporal bone shape change during ontogeny in the African apes and humans. We further apply these data to a preliminary analysis of temporal bone ontogeny in Australopithecus afarensis. Three‐dimensional landmarks were digitized on an ontogenetic series of specimens of Homo sapiens, Pan troglodytes, Pan paniscus, and Gorilla gorilla. Data were analyzed using geometric morphometric methods, and shape changes throughout ontogeny in relation to size were compared. Results of these analyses indicate that, despite broadly similar patterns, African apes and humans show marked differences in development of the mandibular fossa and tympanic portions of the temporal bone. These findings indicate divergent, rather than parallel, postnatal ontogenetic allometric trajectories for temporal bone shape in these taxa. The pattern of temporal bone shape change with size exhibited by A. afarensis showed some affinities to that of humans, but was most similar to extant African apes, particularly Gorilla. Am J Phys Anthropol 151:630–642, 2013. © 2013 Wiley Periodicals, Inc.     

The origin of the turtle body plan: evidence from fossils and embryos

The origin of the unique body plan of turtles has long been one of the most intriguing mysteries in evolutionary morphology. Discoveries of several new stem-turtles, together with insights from recent studies on the development of the shell in extant turtles, have provided crucial new information concerning this subject. It is now possible to develop a comprehensive scenario for the sequence of evolutionary changes leading to the formation of the turtle body plan within a phylogenetic framework and evaluate it in light of the ontogenetic development of the shell in extant turtles. The fossil record demonstrates that the evolution of the turtle shell took place over millions of years and involved a number of steps.     

A new turtle from the La Colonia Formation (Campanian–Maastrichtian), Patagonia,Argentina, with remarks on the evolution of the vertebral column in turtles

Abstract: Patagoniaemys gasparinae gen. et sp. nov. is a new stem turtle found in central Patagonia, Chubut Province, Argentina, in outcrops of the La Colonia Formation (Campanian–Maastrichtian). This is a turtle of relatively large size (carapace length c. 70 cm), and the preserved remains of the holotype consist of skull fragments and several postcranial elements including a nearly complete vertebral column. A phylogenetic analysis shows Patagoniaemys gasparinae gen. et sp. nov. forming a monophyletic group with Otwayemys cunicularius and Mongolochelys efremovi, as a sister group to Meiolaniidae. A comprehensive review confirms that formed cervical vertebrae appeared independently several times during turtle evolution: in the clade that includes Patagoniaemys gasparinae gen. et sp. nov. and Meiolaniidae, in some baenids, in the total group Pleurodira and in crown group Cryptodira. Likewise, formed caudal vertebrae appeared several times in turtle evolution.