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.     

Ontogenies in mice selected for high voluntary wheel-running activity. I. Mean ontogenies

The evolutionary importance of postnatal ontogenies has long been recognized, but most studies of ontogenetic trajectories have focused exclusively on morphological traits. For animals, this represents a major omission because behavioral traits and their ontogenies often have relatively direct relationships to fitness. Here four replicate lines of house mice artificially selected for high early-age wheel running and their four replicate control lines were used to evaluate the effects of early-age directional selection, genetic drift, and activity environment (presence or absence of a running wheel) on variation in the ontogenies of three traits known to be genetically correlated: voluntary wheel running, body mass, and food consumption. Early-age selection significantly changed both the shape and position of the wheel-running and food-consumption ontogenies while influencing the position, but not the shape, of the body mass ontogeny. Genetic drift (as indicated by variation among replicate lines) produced significant changes in both the position and shape of all three ontogenies; however, its effect differed between the selection and control groups. For wheel running and food consumption, genetic drift only influenced the control ontogenies, whereas for body mass, genetic drift had a significant effect in both selection groups. Both body-mass and food-consumption ontogenies were significantly altered by activity environment, with the environment causing significant changes in the shape and position of both ontogenies. Overall the results demonstrate strong effects of early-age selection, genetic drift, and environmental variation on the evolution and expression of behavioral and morphological ontogenies, with selection changing only the position of the morphological ontogeny but both the position and shape of the behavioral ontogenies.     

Spatiotemporal reorganization of growth rates in the evolution of ontogeny

Abstract. Heterochrony, evolutionary changes in rate or timing of development producing parallelism between ontogeny and phylogeny, is viewed as the most common type of evolutionary change in development. Alternative hypotheses such as heterotopy, evolutionary change in the spatial patterning of development, are rarely entertained. We examine the evidence for heterochrony and heterotopy in the evolution of body shape in two clades of piranhas. One of these is the sole case of heterochrony previously reported in the group; the others were previously interpreted as cases of heterotopy. To compare ontogenies of shape, we computed ontogenetic trajectories of shape by multivariate regression of geometric shape variables (i.e., partial warp scores and shape coordinates) on centroid size. Rates of development relative to developmental age and angles between the trajectories were compared statistically. We found a significant difference in developmental rate between species of Serrasalmus , suggesting that heterochrony is a partial explanation for the evolution of body shape, but we also found a significant difference between their ontogenetic transformations; the direction of the difference between them suggests that heterotopy also plays a role in this group. In Pygocentrus we found no difference in developmental rate among species, but we did find a difference in the ontogenies, suggesting that heterotopy, but not heterochrony, is the developmental basis for shape diversification in this group. The prevalence of heterotopy as a source of evolutionary novelty remains largely unexplored and will not become clear until the search for developmental explanations looks beyond heterochrony.     

COMPARATIVE ONTOGENY OF A WILD CUCURBIT AND ITS DERIVED CULTIVAR

Most previous studies of evolutionary modification of form in plants have focused primarily on individual organs or flowers. Few have investigated the role of evolutionary changes in timing or position at the level of whole plant ontogeny. This study compares ontogenies of the primary shoots of two subspecies of Cucurbita argyrosperma, one a cultivar and the other its wild progenitor. Differences in flowering times between these subspecies suggested that the cultivar may have evolved from the wild subspecies via heterochronic processes leading to paedomorphosis. Analyses showed that both subspecies are similar in vegetative architecture and rates of leaf production. Earlier flowering in the cultivar, both in terms of position and absolute time, appears to have arisen through progenesis. Initial observations of leaf blade morphology led to the hypothesis that paedomorphosis and gigantism also may have been involved in the evolution of leaf blade shape in the cultivar: all leaves of the cultivar are larger and visually similar in shape to early leaves of the wild subspecies. However, quantitative analysis revealed that leaves of the cultivar are neither geometrically, nor solely allometrically larger versions of early leaves of the progenitor. Leaf shape in the cultivar exhibits novel features as well as effects of allometry shared with the progenitor, hence a simple hypothesis of paedomorphic evolution of leaf shape is not supported.     

Comparison of cranial ontogenetic trajectories among great apes and humans

Molecular data suggest that humans are more closely related to chimpanzees than either is to the gorillas, yet one finds the closest similarity in craniofacial morphology to be among the great apes to the exclusion of humans. To clarify how and when these differences arise in ontogeny, we studied ontogenetic trajectories for Homo sapiens, Pan paniscus, Pan troglodytes, Gorilla gorilla and Pongo pygmaeus. A total of 96 traditional three-dimensional landmarks and semilandmarks on the face and cranial base were collected on 268 adult and sub-adult crania for a geometric morphometric analysis. The ontogenetic trajectories are compared by various techniques, including a new method, relative warps in size-shape space. We find that adult Homo sapiens specimens are clearly separated from the great apes in shape space and size-shape space. Around birth, Homo sapiens infants are already markedly different from the great apes, which overlap at this age but diverge among themselves postnatally. The results suggest that the small genetic differences between Homo and Pan affect early human ontogeny to induce the distinct adult human craniofacial morphology. Pure heterochrony does not sufficiently explain the human craniofacial morphology nor the differences among the African apes.     

A Shared Pattern of Postnatal Endocranial Development in Extant Hominoids

By comparing species-specific developmental patterns, we can approach the question of how development shapes adult morphology and contributes to the evolution of novel forms. Studies of evolutionary changes to brain development in primates can provide important clues about the emergence of human cognition, but are hindered by the lack of preserved neural tissue in the fossil record. As a proxy, we study the shape of endocasts, virtual imprints of the endocranial cavity, using 3D geometric morphometrics. We have previously demonstrated that the pattern of endocranial shape development is shared by modern humans, chimpanzees and Neanderthals after the first year of life until adulthood. However, whether this represents a common hominoid mode of development is unknown. Here, we present the first characterization and comparison of ontogenetic endocranial shape changes in a cross-sectional sample of modern humans, chimpanzees, gorillas, orangutans and gibbons. Using developmental simulations, we demonstrate that from late infancy to adulthood ontogenetic trajectories are similar among all hominoid species, but differ in the amount of shape change. Furthermore, we show that during early ontogeny gorillas undergo more pronounced shape changes along this shared trajectory than do chimpanzees, indicative of a dissociation of size and shape change. As shape differences between species are apparent in even our youngest samples, our results indicate that the ontogenetic trajectories of extant hominoids diverged at an earlier stage of ontogeny but subsequently converge following the eruption of the deciduous dentition.     

Different cranial ontogeny in Europeans and Southern Africans

Modern human populations differ in developmental processes and in several phenotypic traits. However, the link between ontogenetic variation and human diversification has not been frequently addressed. Here, we analysed craniofacial ontogenies by means of geometric-morphometrics of Europeans and Southern Africans, according to dental and chronological ages. Results suggest that different adult cranial morphologies between Southern Africans and Europeans arise by a combination of processes that involve traits modified during the prenatal life and others that diverge during early postnatal ontogeny. Main craniofacial changes indicate that Europeans differ from Southern Africans by increasing facial developmental rates and extending the attainment of adult size and shape. Since other studies have suggested that native subsaharan populations attain adulthood earlier than Europeans, it is probable that facial ontogeny is linked with other developmental mechanisms that control the timing of maturation in other variables. Southern Africans appear as retaining young features in adulthood. Facial ontogeny in Europeans produces taller and narrower noses, which seems as an adaptation to colder environments. The lack of these morphological traits in Neanderthals, who lived in cold environments, seems a paradox, but it is probably the consequence of a warm-adapted faces together with precocious maturation. When modern Homo sapiens migrated into Asia and Europe, colder environments might establish pressures that constrained facial growth and development in order to depart from the warm-adapted morphology. Our results provide some answers about how cranial growth and development occur in two human populations and when developmental shifts take place providing a better adaptation to environmental constraints.     

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.     

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.     

Evolution of human growth prolongation

This investigation evaluates hypotheses that seek to explain temporal retardation or prolongation of human ontogeny. Current hypotheses that address this issue are poorly defined and conflate several distinct theoretical positions. A model that predicts homogeneity in the extension of human growth periods is evaluated. This model is contrasted with two alternatives. The first alternative predicts heterogeneity in the extension of human growth periods. The second anticipates that human growth prolongation is the result of the uniquely derived “insertion” of a human childhood period into an ancestral ontogenetic trajectory. Allometric analyses of body mass growth data from 21 species of anthropoid primates suggest that human female and male ontogenies often depart from patterns established by other primates, but these departures are not uniformly exceptional. Comparisons imply that derived changes in human growth are heterogeneous. Relative to interspecific expectations, early growth periods are much prolonged, but later growth periods are actually reduced. Moreover, the attributes of early growth periods, including growth rates, timing of growth events, and size-for-age, are highly variable across primates. Low correlations among growth periods suggest independence among growth phases. These analyses highlight minimal distinctions between competing models (heterogeneous extension and insertion hypotheses) that attempt to explain human growth prolongation. More important, the present study facilitates refinements of causal models that have been proposed to explain human growth prolongation. Specifically, human growth prolongation may be related to derived changes in patterns of brain development. Alternatively, metabolic factors may have exerted influences on human ontogeny. However, models that predict long growth periods as a byproduct of metabolic factors do not adequately explain temporal retardation of human ontogeny. Am J Phys Anthropol 107:331–350, 1998. © 1998 Wiley-Liss, Inc.     

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.     

The ontogeny of cranial base angulation in humans and chimpanzees and its implications for reconstructing pharyngeal dimensions

This paper examines differences in the processes by which the cranial base flexes in humans and extends in chimpanzees. In addition, we test the extent to which one can use comparisons of cranial base angles in humans and non-human primates to predict vocal tract dimensions. Four internal cranial base angles and one external cranial base angle were measured in a longitudinal sample of Homo sapiens and a cross-sectional sample of Pan troglodytes. These data show that the processes of cranial base angulation differ substantially in these species. While the human cranial base flexes postnatally in a rapid growth trajectory that is complete by two years, the cranial base in P. troglodytes extends postnatally in a more prolonged skeletal growth trajectory. These comparisons also demonstrate that the rate of cranial base angulation is comparable for different measures, but that angles which incorporate different anterior cranial base measurements correlate poorly. We also examined ontogenetic relationships between internal and external cranial base angles and vocal tract growth in humans to test the hypothesis that cranial base angulation influences pharyngeal dimensions and can, therefore, be used to estimate vocal tract proportions in fossil hominids. Our results indicate that internal and external cranial base angles are independent of the horizontal and vertical dimensions of the vocal tract. Instead, a combination of mandibular and palatal landmarks can be used to predict dimensions of the vocal tract in H. sapiens. The developmental contrasts in cranial base angulation between humans and non-human primates may have important implications for testing hypotheses about the relationship between cranial base flexion and other craniofacial dimensions in hominid evolution.     

Ontogeny and phylogeny of the pelvis in Gorilla, Pongo, Pan, Australopithecus and Homo

To examine the evolutionary differences between hominoid locomotor systems, a number of observations concerning the growth of the pelvis among the great apes as compared to modern and fossil hominids are reported. We are interested in the size and shape of the coxal bones at different developmental stages across species that may elucidate the relationship between ontogeny and phylogeny (i.e., heterochrony) in the hominoid pelvis. Our hypotheses are: (1) do rates of absolute growth differ?, (2) do rates of relative growth differ?, and (3) does heterochrony explain these differences? Bivariate and multivariate analyses of pelvic dimensions demonstrate both the diversity of species-specific ontogenetic patterns among hominoids, and an unequivocal separation of hominids and the great apes. Heterochrony alone fails to account for the ontogenetic differences between hominids and the great apes. Compared to recent Homo,Australopithecus can be described as 'hyper-human' from the relative size of the ischium, and short but broad ilium. Australopithecus afarensis differs from Australopithecus africanus by its relatively long pubis. In multivariate analyses of ilium shape, the most complete coxal bone attributed to Homo erectus, KNM-ER 3228, falls within the range of juvenile and adult Australopithecus, whereas Broken Hill falls within the range of modern Homo, suggesting that the modern human ilium shape arose rather recently. Among the great apes, patterns of pelvic ontogeny do not exclusively separate the African apes from Pongo.     

Iterative ontogenetic development of ammonoid conch shapes from the Devonian through to the Jurassic

We measured longitudinal growth in conch cross‐sections of 177 Devonian to Jurassic ammonoid species to test whether conch ontogenetic development parallels the iterative evolution of pachyconic or globular conch shapes. Ontogenetic trajectories of two cardinal conch parameters, conch width index and umbilical width index, show a few common recurring ontogenetic pathways in terms of the number of ontogenetic phases. The most common, with three phases in the conch width index (decrease–increase–decrease) and umbilical width index (increase–decrease–increase), is termed here C‐mode ontogeny (after the Carboniferous genus Cravenoceras). Many of the studied globular Palaeozoic and Triassic species (of the latter, particularly the arcestid ammonoids) share principal patterns in the triphasic C‐mode conch ontogeny in closely related groups but also between unrelated groups as well. The repetition of conch growth patterns is an example of convergent evolution of the entire life history of globular ammonoids. The studied Jurassic globular shaped ammonoids deviate from the growth patterns seen in earlier groups showing less pronounced ontogenetic trajectories with nearly isometric or weakly asymmetric growth without distinct phases. This trajectory is termed here M‐mode ontogeny (after the Jurassic genus Macrocephalites). No major change in the ontogenetic modes of pachyconic and globular ammonoids occurred moving from the Palaeozoic into the Mesozoic; the survivors of the end‐Permian extinction event iteratively developed conch ontogenies similar to those of Palaeozoic forms. In contrast, the Triassic–Jurassic boundary marks the major event with the evolution of some cardinal conch parameters relating to globular ammonoid ontogeny.     

Size and shape regulation during larval growth in the lepidopteran Pieris brassicae

By adopting a longitudinal study design and through geometric morphometrics methods, we investigated size and shape regulation in the head capsule during the larval development of the cabbage butterfly Pieris brassicae under laboratory conditions. We found evidence of size regulation by compensatory growth, although not equally effective in all larval stages. Size compensation is not attained through the regulation of developmental timing, but rather through the modulation of per‐time growth rate. As for the shape, neither the variance of the symmetric component of shape, nor the level of fluctuating asymmetry show any evidence of increase across stages, either at the population or individual level, which is interpreted as a mark of ontogenetic shape regulation. In addition, also the geometry of individual asymmetry is basically conserved across stages. While providing specific documentation on the ontogeny of size and shape variation in this insect, this study may contribute to a more general understanding of developmental regulation and its influence on phenotypic evolution.     

The ontogeny of sexual dimorphism in the cranium of Bornean orang-utans (Pongo pygmaeus pygmaeus) as detected by principal-components analysis

The ontogeny of cranial sexual dimorphism in the Bornean orang-utan (Pongo pygmaeus pygmaeus) is examined by means of principal-components analysis (PCA). Normalized first components are called allometry vectors or vectors of relative growth and show that sexual dimorphism is present at all stages of growth. Two patterns of sexual dimorphism are present: (1) sexual differences at age groups 2 and 3 are the result primarily of differences in principal component II scores, reflecting mainly shape-related differences, and (2) age groups 5, 6, and 7 show a trend of stronger size-related shape differences with increasing age in the allometry vector along with decreasing differences in principal component II scores, reflecting an increase in size-related shape differences between the sexes. Age group 4 shows a combination of both patterns. Our results support Shea's hypothesis (1985a) that when using multigroup PCAs in closely related taxa, the allometry vector will generally estimate the shape variation resulting from the extension of common growth allometry patterns (ontogenetic scaling). The second and subsequent components summarize shape variation from slope and intercept differences between the groups, provided that ontogenetic scaling is not solely responsible for all the shape differences present. Subanalyses of those dimensions previously found to show ontogenetic scaling and acceleration follow this pattern well. The total sample provides a pattern whereby ontogenetically scaled dimensions possess a stronger influence over accelerated dimensions but still generally follow Shea's hypothesis. Finally, variously derived coefficients provided several interesting findings: (1) strong evidence was found against multivariate isometry for both the pooled and the separate samples, (2) multivariate allometric coefficients for both sexes follow the general growth pattern of negative scaling in neurocranial dimensions and positive scaling in the viscerocranium, and (3) multivariate slopes have a very high correlation with bivariate slopes relative to the same independent X variable, thereby lending further support to Jolicoeur's (1963a, b) allometry generalization.     

PASOS: a method for the phylogenetic analysis of shape ontogenies

We present a novel phylogenetic approach to infer ancestral ontogenies of shape characters described as landmark configurations. The method is rooted in previously published theoretical developments to analyse landmark data in a phylogenetic context with parsimony as the optimality criterion, in this case using the minimization of differences in landmark position to define not only ancestral shapes but also the changes in developmental timing between ancestor–descendant shape ontogenies. Evolutionary changes along the tree represent changes in relative developmental timing between ontogenetic trajectories (possible heterochronic events) and changes in shape within each stage. The method requires the user to determine the shape of the specimens between two standard events, for instance birth and onset of sexual maturity. Once the ontogenetic trajectory is discretized into a series of consecutive stages, the method enables the user to identify changes in developmental timing associated with changes in the offset and/or onset of the shape ontogenetic trajectories. The method is implemented in a C language program called SPASOS. The analysis of two empirical examples (anurans and felids) using this novel method yielded results in agreement with previous hypotheses about shape evolution in these groups based on non-phylogenetic analyses.     

Morphological evolution in Ceratophryinae frogs (Anura,Neobatrachia): the effects of heterochronic changes during larval development and metamorphosis

Heterochrony produces morphological change with effects in shape, size, and/or timing of developmental events of a trait related to an ancestral ontogeny. This paper analyzes heterochrony during the ontogeny of Ceratophryinae (Ceratophrys, Chacophrys, and Lepidobatrachus), a monophyletic group of South American frogs with larval development, and uses different approaches to explore their morphological evolution: (1) inferences of ancestral ontogenies and heterochronic variation from a cladistic analysis based on 102 morphological larval and adult characters recorded in ten anuran taxa; (2) comparisons of size, morphological variation, and timing (age) of developmental events based on a study of ontogenetic series of ceratophryines, Telmatobius atacamensis, and Pseudis platensis. We found Chacophrys as the basal taxon. Ceratophrys and Lepidobatrachus share most derived larval features resulting from heterochrony. Ceratophryines share high rates of larval development, but differ in rates of postmetamorphic growth. The ontogeny of Lepidobatrachus exhibits peramorphic traits produced by the early onset of metamorphic transformations that are integrated in an unusual larval morphology. This study represents an integrative examination of shape, size, and age variation, and discusses evolutionary patterns of metamorphosis. © 2008 The Linnean Society of London, Zoological Journal of the Linnean Society, 2008, 154 , 752–780.     

Historical Patterns of Developmental Integration in Piranhas

TO test the hypothesis that developmental integration coordinatesevolutionary change through history, we dissect the spatialand temporal integration of ontogenetic allometries of piranhabody form and examine the evolutionary coordination among ontogeneticfeatures by a phylogenetic analysis. Few of our characters provideevidence in support of the hypothesis. In general, we find thatdevelopmental integration is historically labile, being modifiedat virtually every speciation event. Most of the ontogeneticfeatures are dissociated in their phylogenetic changes and evolvein a mosaic fashion. Indeed, developmental integration is solabile that primitively integrated features of ontogeny usuallyevolve subsequently as independent characters. Evolutionarychanges in developmental integration can result in increasedor decreased integration on the ontogenetic time scale. Whenlocalized features are deleted from ontogeny, or when spatiallyintegrated features are gained, the derived ontogenies may bemore integrated in a spatial sense. The end result of phylogeneticdissociations may be a more highly developmentally integratedontogeny. Thus, in the piranhas we studied, we find a historicallycoupled increase in developmental integration caudally and adecrease indevelopmental integration cranially.     

Heterochrony and allometry: the analysis of evolutionary change in ontogeny

The connection between development and evolution has become the focus of an increasing amount of research in recent years, and heterochrony has long been a key concept in this relation. Heterochrony is defined as evolutionary change in rates and timing of developmental processes; the dimension of time is therefore an essential part in studies of heterochrony. Over the past two decades, evolutionary biologists have used several methodological frameworks to analyse heterochrony, which differ substantially in the way they characterize evolutionary changes in ontogenies and in the resulting classification, although they mostly use the same terms. This review examines how these methods compare ancestral and descendant ontogenies, emphasizing their differences and the potential for contradictory results from analyses using different frameworks. One of the two principal methods uses a clock as a graphical display for comparisons of size, shape and age at a particular ontogenic stage, whereas the other characterizes a developmental process by its time of onset, rate, and time of cessation. The literature on human heterochrony provides particularly clear examples of how these differences produce apparent contradictions when applied to the same problem. Developmental biologists recently have extended the concept of heterochrony to the earliest stages of development and have applied it at the cellular and molecular scale. This extension brought considerations of developmental mechanisms and genetics into the study of heterochrony, which previously was based primarily on phenomenological characterizations of morphological change in ontogeny. Allometry is the pattern of covariation among several morphological traits or between measures of size and shape; unlike heterochrony, allometry does not deal with time explicitly. Two main approaches to the study of allometry are distinguished, which differ in the way they characterize organismal form. One approach defines shape as proportions among measurements, based on considerations of geometric similarity, whereas the other focuses on the covariation among measurements in ontogeny and evolution. Both are related conceptually and through the use of similar algebra. In addition, there are close connections between heterochrony and changes in allometric growth trajectories, although there is no one-to-one correspondence. These relationships and outline links between different analytical frameworks are discussed.