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Cranial growth in normal and low-protein-fed Saimiri. An environmental heterochrony.

Protein malnutrition has a significant and measurable effect on the rate and timing of growth. Heterochrony is generally viewed as the study of evolutionary changes in the relative rates and timing of growth and development. Although changes in growth commonly result from experimental manipulations of diet, nobody has previously attempted to explain such changes from a heterochronic perspective. We use a heterochronic perspective to compare a group of squirrel monkeys fed a low-protein diet to individuals on a high-protein diet, but, in contrast to previous works, we focus particularly on the effects of environmental and not genetic factors. In the present study, Gould's (1977) and Godfrey and Sutherland's (1996) methodologies for studying heterochrony, as well as geometric morphometrics, are used to compare two groups of Saimiri sciureus boliviensis. Two groups of Saimiri were constructed on the basis of the protein content in their diets: a high-protein group (HP) (N=12) and a low-protein group (LP) (N=12). All individuals are males born in captivity. Two major functional components of the skull, the neurocranium and the face, were analysed. Four minor components were studied in each major component. Comparison of craniofacial ontogeny patterns based on major and minor components suggests that changes in the skull of LP animals can be explained by heterochrony. The skull of LP animals exhibits isomorphism produced by proportioned dwarfism. Our results suggest that heterochrony can be environmentally, rather than exclusively genetically, induced. The study of genetic assimilation (Waddington, 1953, 1956; see Scharloo, 1991; Hallgrimsson et al., 2002) has demonstrated that environmentally induced phenotypes often have a genetic basis, and thus parallel changes can be easily induced genetically. It is possible that proportioned dwarfism is far more common than currently appreciated.

Animals↗

Shape patterns of genital papillae in pinworms (Enterobiinae, Oxyurida, Nematoda) parasite of primates: a landmark analysis.

The Enterobiinae includes 47 species of pinworms parasite of primates. A previous cladistic analysis of this subfamily supported its monophyly and its subdivision into three genera. Based on morphological characters, this cladistic analysis excluded characters describing the shape of the genital papillae of male pinworms, because the corresponding patterns could not be described using discrete characters. In this study, the shape of the genital papillae of the males of 35 within the 47 species is analyzed using geometric morphometric approaches. The aims of this study are to investigate: (i) the relationships between the phylogeny and the shape patterns of the caudal bursa, (ii) the shape differences between and within monophyletic groups, and (iii) the functional implications of the shape patterns observed within the subfamily. Results demonstrate that different patterns of evolution of the caudal bursa, each one characterized by a particular spatial distribution of the phasmids and genital papillae may be recognized, which are consistent with the classification of the Enterobiinae into three groups. On the whole, these patterns may be related to particular mating behavior of the pinworms. When incongruence is observed between shape patterns distribution and species distribution into monophyletic groups, they are found to correspond to homoplasic events. This suggests that convergent selective pressures are involved in the evolution of the shape of the genital papillae. This analysis also confirms that morphometric shape patterns cannot be interpreted unequivocally without the support of a pre-existing phylogenetic framework.

Animals↗

Studies of morphological and molecular phylogenetic divergence in spiders (Araneae: Homalonychus) from the American southwest, including divergence along the Baja California Peninsula.

Comparative phylogenetic and phylogeographic analyses have revealed a pervasive midpeninsular divergence in the mitochondrial genealogies of numerous vertebrate taxa distributed on the Baja California Peninsula. In this study, we extend the investigation of regional vicariance in Baja California to an arthropod taxon by examining patterns of phylogenetic and morphological divergence in the spider genus Homalonychus (Araneae, Homalonychidae). We analyzed data from two mtDNA genes (16S rRNA and NADH dehydrogenase subunit (1) and a nuclear gene (28S rRNA) using maximum parsimony and Bayesian phylogenetic analyses, and also conducted geometric morphometric analyses employing landmark data on male and female genitalia. Genes and morphology both reveal a deep split across the Colorado River and Gulf of California, separating Homalonychus selenopoides on the east side of river from its congener Homalonychus theologus on the west side of the river, including the Baja California Peninsula. Along the north-south axis of the Baja Peninsula, an apparently more recent midpeninsular phylogenetic break is evident within H. theologus in the mitochondrial genome and in female genitalia. However, there is no measurable divergence between northern and southern populations in either nuclear DNA or male genitalia. We suggest that this discordance between datasets reflects either a difference in rates of evolution between male versus female systems, or that male-based nuclear gene flow is obscuring a phylogenetic split that is fixed in the female-based systems. Our findings provide additional support for a midpeninsular Baja divergence event, although the timing and geological evidence for such an event remain elusive.

Animals↗

Nuclear markers reveal that inter-lake cichlids' similar morphologies do not reflect similar genealogy.

The apparent inter-lake morphological similarity among East African Great Lakes' cichlid species/genera has left evolutionary biologists asking whether such similarity is due to sharing of common ancestor or mere convergent evolution. In order to answer such question, we first used Geometric Morphometrics, GM, to quantify morphological similarity and then subsequently used Amplified Fragment Length Polymorphism, AFLP, to determine if similar morphologies imply shared ancestry or convergent evolution. GM revealed that not all presumed morphological similar pairs were indeed similar, and the dendrogram generated from AFLP data indicated distinct clusters corresponding to each lake and not inter-lake morphological similar pairs. Such results imply that the morphological similarity is due to convergent evolution and not shared ancestry. The congruency of GM and AFLP generated dendrograms imply that GM is capable of picking up phylogenetic signal, and thus GM can be potential tool in phylogenetic systematics.

Africa, Eastern↗

The Petrolisthes galathinus complex: species boundaries based on color pattern, morphology and molecules, and evolutionary interrelationships between this complex and other Porcellanidae (Crustacea: Decapoda: Anomura).

While the amphi-American porcellanid crab Petrolistes galathinus has been traditionally viewed as a highly variable species containing several different color forms, we consider it to be a complex of at least 6 morphologically similar species with similar ecological requirements, but diagnosable through coloration. Here we surveyed sequence variation of the mitochondrial 16S rRNA gene, compared the morphology of adults and of the first larval stage (Zoea I), and explored shape variation of the sternal plate using geometric morphometric methods, to investigate boundaries among the species in the complex, and to confirm the validity of color and color pattern for distinguishing them. Sequences and larval morphological characters of other porcellanids were included to investigate the correspondence between genetic divergence and morphology of adults and larvae. The molecular and morphometric results support the validity of the species in the complex, and of color pattern for their distinction. The close relationship between the complex and the putative ancenstral porcellanid Parapetrolisthes tortugensis was indicated by the molecular and larval-morphology results. The adult morphology of this species is interpreted as a result of convergent evolution driven by a relatively rapid ecological adaptation to conditions in deeper waters. The nesting position in the phylogenetic trees of Petrocheles australiensis outside the Porcellanidae clade questions the monophyly of this family.

Animals↗

The Neanderthal taxonomic position: models of intra- and inter-specific craniofacial variation.

The Neanderthal taxonomic position is a matter of wide disagreement among paleoanthropologists. Some workers consider this fossil human group to represent a different species, Homo neanderthalensis, while others see it as a subspecies of Homo sapiens. This study developed two models of morphological variation to be applied to a comparison between Neanderthals and modern humans: modern human populations provided a measure of intra-specific variation, while the species and subspecies of Pan provided measures of both intra- and inter-specific morphological differences. Although such an approach has been advocated strongly, it has not been systematically undertaken until recently. The techniques of geometric morphometrics were used to collect data in the form of three-dimensional coordinates of craniofacial landmarks. The data were processed using generalized procrustes analysis, and analyzed by an array of multivariate statistical methods, including principal components analysis, canonical variates analysis and Mahalanobis D(2). The morphological distances between Neanderthals and modern humans, and between Neanderthals and Late Paleolithic/early anatomically modern specimens, are consistently greater than the distances among recent human populations, and greater than the distances between the two chimpanzee species. Furthermore, no strong morphological similarities were found between Neanderthals and Late Paleolithic Europeans. This study does not find evidence for Neanderthal contribution to the evolution of modern Europeans. Results are consistent with the recognition of Neanderthals as a distinct species.

Anatomy, Comparative↗

Virtual reality and anthropology.

Since the discovery of the Tyrolean Iceman in 1991 advanced imaging and post processing techniques were successfully applied in anthropology. Specific techniques include spiral computed tomography and 3-dimensional reconstructions including stereolithographic and fused deposition modeling of volume data sets. The Iceman's skull was the first to be reproduced using stereolithography, before this method was successfully applied in preoperative planning. With the advent of high-end graphics workstations and biomedical image processing software packages, 3-dimensional reconstructions were established as a routine tool for analyzing volume data sets. These techniques opened totally new insights in the field of physical anthropology. Computed tomography became the ideal research tool to access the internal structures of various precious fossils without damaging or even touching them. Many of the most precious specimens from the species Autralopithecus (1.8-3.5 Myears), Homo heidelbergensis (200-600 kyears) or Homo neanderthalensis (40-100 kyears) were scanned during the last 5 years. Often the fossils are filled with a stone matrix or other materials. During the postprocessing routines highly advanced algorithms were used to remove virtually these incrustations. Thus it was possible to visualize the morphological structures that lie beneath the matrix. Some specimen were partially destroyed, so the missing parts were reconstructed on computer screen in order to get estimations of the brain volume and endocranial morphology, both major fields of interest in physical anthropology. Moreover the computerized form of the data allows new descriptions of morphologic structures by the means of 'geometric morphometrics'. Some of the results may change aspects and interpretations in human evolution. The introduction of new imaging and post processing techniques created a new field of research: Virtual Anthropology.

Algorithms↗

[Cranial and mandibular morphology of the Indrinae. Contribution of Procrustes methods and Fourier analysis].

Although it is universally accepted that the Indridae family is monophyletic, there is no such unanimity about how the extant species of the Indrinae sub-family are related. Cranium and mandible disparity among Indri indri, Propithecus diadema, Propithecus verreauxi and Avahi laniger is analysed by geometrical morphometric methods and interpreted in adaptive terms. We compare results obtained by two techniques: Procrustes superimpositions for skulls and elliptical Fourier analysis for jawbones. In both studies, the three genera are clearly isolated. Avahi laniger is the species with the most paedomorphic cranium while Indri indri has the most 'juvenile' mandible. Cranial morphology is governed principally by orbit volume and body size, while jaw shape is related to diet (enlargement of the gonial region).

Animals↗

Inter- and intra-specific variation in the ontogeny of the hominoid facial skeleton: testing assumptions of ontogenetic variability.

In this paper we use geometric morphometric techniques to test two assumptions that are commonly made about variations in facial ontogeny: closely related species, or members of the same species, will share a common early post-natal ontogeny; and closely related species, or members of the same species, will share a common ontogenetic scaling trajectory. To test these assumptions we use four species of hominines: Homo sapiens, Gorilla gorilla, Pan troglodytes and Pan paniscus. The first assumption is falsified, both inter- and intra-specifically, using discriminant analysis with crossvalidation of subadults prior to the onset of the eruption of the permanent dentition. The second assumption only holds true for inter-specific comparisons of ontogenetic scaling trajectories, while assumptions of variation in intra-specific scaling trajectories are falsified with these data.

Adolescent↗

Regional dissociated heterochrony in multivariate analysis.

Heterochrony, the classic framework to study ontogeny and phylogeny, in essence relies on a univariate concept of shape. Though principal component plots of multivariate shape data seem to resemble classical bivariate allometric plots, the language of heterochrony cannot be translated directly into general multivariate methodology. We simulate idealized multivariate ontogenetic trajectories and demonstrate their behavior in principal component plots in shape space and in size-shape space. The concept of "dissociation", which is conventionally regarded as a change in the relationship between shape change and size change, appears to be algebraically the same as regional dissociation - the variation of apparent heterochrony by region. Only if the trajectories of two related species lie along exactly the same path in shape space can the classic terminology of heterochrony apply so that pure dissociation of size change against shape change can be detected. We demonstrate a geometric morphometric approach to these issues using adult and subadult crania of 48 Pan paniscus and 47 P. troglodytes. On each specimen we digitized 47 landmarks and 144 semilandmarks on ridge curves and the external neurocranial surface. The relation between these two species' growth trajectories is too complex for a simple summary in terms of global heterochrony.

Aging↗

Craniofacial sexual dimorphism patterns and allometry among extant hominids.

Craniofacial sexual dimorphism in primates varies in both magnitude and pattern among species. In the past two decades, there has been an increasing emphasis in exploring the correlations of these patterns with taxonomy and the variation in patterns within and among the craniofacial regions. Scrutinising these relationships for hominids, we decompose the craniofacial morphology in five taxa: Homo sapiens, Pan paniscus, Pan troglodytes, Gorilla gorilla and Pongo pygmaeus. 3D coordinates of 35 traditional landmarks and 61 semilandmarks, covering five ridge curves, are measured for each of 268 adult and sub-adult specimens and analysed using geometric morphometric methods. A multivariate analysis in size-shape space shows that ontogenetic scaling contributes to the development of sexual dimorphism in all five taxa, but to a varying extent. In absolute as well as in relative terms P. pygmaeus shows the greatest allometric component, followed by G. gorilla. Homo is intermediate, while in Pan the non-allometric constituent part contributes a large fraction to the actual sexual dimorphism, most markedly in the pygmy chimpanzee. An eigendecomposition of the five vectors of sexual dimorphism reveals two dimensions independent of allometry. One separates orang-utan sexual dimorphism from the African apes and Homo, and the other differentiates between the great apes and Homo with Pan mediating. We discuss these patterns and speculate on their use as characters for taxonomic analysis in the fossil record.

Animals↗

Quantification of dentine shape in anthropoid primates.

The external shape and thickness of the enamel component of primate molars have been employed extensively in phylogenetic studies of primate relationships. The dentine component of the molar crown also has been suggested to be indicative of phylogenetic relationships, but few studies have quantified dentine morphology in order to evaluate this possibility. To explore the utility of dentine shape as an indicator of phylogenetic affinity, a two-dimensional geometric morphometric analysis (EDMA-II) was performed using nine homologous landmarks on a sample of sectioned maxillary molars of extant ceboid, cercopithecoid, and hominoid primates. Results indicate that dentine shape (the configuration of the enamel-dentine junction, or EDJ) can distinguish taxa at every taxonomic level examined, including superfamilies, subfamilies, and closely related genera and species. This supports the idea that dentine morphology may be useful for phylogenetic studies. It is further suggested that the morphology of the EDJ may be more conservative than enamel morphology, and perhaps better-suited to phylogenetic studies. Among the samples studied, cercopithecoid primates have a unique dentine shape, and it is suggested that the development of bilophodont molars may be related to the distinctive EDJ configuration in cercopithecoids.

Animals↗

Functional adaptations in the craniofacial morphology of Malagasy primates: shape variations associated with gummivory in the family Cheirogaleidae.

The infraorder Lemuriformes is characterized by a high level of homoplasy that clouds the evolutionary signal. The analysis of the morphological disparity of the Malagasy primates' crania and mandibles demonstrates the high determinism of functional specializations and developmental constraints, regardless of the phylogeny. In the present work, the weight of functional constraints linked to diet--a putative source of homoplasy--is analyzed first at the level of the infraorder Lemuriformes as a whole, and secondly at the level of a single family, the Cheirogaleidae, chosen because it contains taxa with two different diets (omnivory and gummivory). Malagasy primates are characterized by a great variety of dietary habits: some of them are omnivores, folivores, frugivores, gummivores, insectivores or even specialized hard-object feeders. All cheirogaleids feed on tree exudates, but while gum consumption is occasional or limited for Microcebus, Cheirogaleus and Mirza, gums are the dominant food source for Phaner and Allocebus. Craniofacial shape variations are analyzed using geometric morphometrics: methods based on landmark identification (Procrustes superimpositions) are chosen for cranium shape analysis, and methods based on outline decomposition (elliptical Fourier functions) for study of mandible shape. The morphospaces obtained at the level of the infraorder appear to be highly constrained by dietary habits, especially in the case of the mandibles. At the finer level of the family Cheirogaleidae, the analyses permit (1) separation of craniomandibular shape variation associated with the two dietary categories and (2) among the omnivorous category, to distinguish variation associated with the percentage of gum consumption.

Adaptation, Biological↗

Comparative ontogeny in humans and chimpanzees: similarities, differences and paradoxes in postnatal growth and development of the skull.

The hypothesis of retarded development is a classic and controversial issue in human evolution. It depends directly on the understanding of ontogenetic trajectories and their basic constituents: timing, rate and associated patterns of maturation. In the present study, we applied geometric morphometrics to investigate postnatal ontogeny in human and chimpanzee skulls (N = 302). We evaluated postnatal ontogenetic rates, based on comparisons of properties of size and shape in adults. At different dental ages the percentage of the adult mean size (growth) and adult mean shape (development) was used to quantify patterns of maturation. We found significantly higher levels of ontogenetic maturity in humans than chimpanzees during pre-M1 and M1 eruption. However, during this ontogenetic period the human increments were lower than those of chimpanzees suggesting lower rates. During and after M2-eruption species did not differ in their ontogenetic trajectories. The results indicate that higher prenatal and lower peri- and postnatal maturation rates characterize human ontogeny when compared with chimpanzees. If mandibular ontogeny is considered alone, a paradox was found. Whereas growth maturation proceeded in an expected trajectory continuously approximating 100% adult mean size, developmental maturity was different. After M1-eruption in both species the morphological distance, which had increased before, became reduced again, and reached adult mean shape in a second developmental peak. Such a tendency was found in humans and chimpanzees. This indicates that both size and shape maturation must be considered to understand the complexity of postnatal mandibular ontogeny.

Adolescent↗

Cranial-base morphology in children with class III malocclusion.

The association between cranial-base morphology and Class III malocclusion is not fully understood. The purpose of this study was to investigate the morphologic characteristics of the cranial base in children with Class III malocclusion. Lateral cephalograms from 100 children with Class III malocclusion were compared with those from 100 subjects with normal occlusion. Ten landmarks on the cranial base were identified and digitized. Cephalometric assessment using seven angular and 18 linear measurements was performed by univariate and multivariate analyses. The results revealed that the greatest between-group differences occurred in the posterior cranial-base region. It was concluded that shortening and angular bending of the cranial base, and a diminished angle between the cranial base and mandibular ramus, may lead to Class III malocclusion associated with Class III facial morphology. The association between cranial-base morphology and other types of malocclusion needs clarification. Further study of regional changes in the cranial base, with geometric morphometric analysis, is warranted.

Cephalometry↗

Application of relative warp analysis to the evaluation of two-dimensional gels in proteomics: studying isoelectric point and relative molecular mass variation.

We propose a geometric-morphometrics method (relative warp analysis) to be used in proteomic comparisons. This approach was applied to a dataset from a comparison between 5 controls and 5 patients with colorectal cancer disease published elsewhere. The spots in the 2-D maps were used as landmarks in a morphometric study, and the differences in shape (spot distribution) among them were obtained. The shape variables were used to compare controls and patients. These components mostly ignore random or experimental effects affecting all the proteins in any of the two dimensions studied. Furthermore, the method allows the researcher to find those proteins which contributed the most to the local shape component detected. Applying this approach, we detected variations in the position (isoelectric point and/or relative molecular mass) of some spots that may reflect differences in the amino acidic sequence or post-translational modifications.

Electrophoresis, Gel, Two-Dimensional↗

Neanderthal cranial ontogeny and its implications for late hominid diversity.

Homo neanderthalensis has a unique combination of craniofacial features that are distinct from fossil and extant 'anatomically modern' Homo sapiens (modern humans). Morphological evidence, direct isotopic dates and fossil mitochondrial DNA from three Neanderthals indicate that the Neanderthals were a separate evolutionary lineage for at least 500,000 yr. However, it is unknown when and how Neanderthal craniofacial autapomorphies (unique, derived characters) emerged during ontogeny. Here we use computerized fossil reconstruction and geometric morphometrics to show that characteristic differences in cranial and mandibular shape between Neanderthals and modern humans arose very early during development, possibly prenatally, and were maintained throughout postnatal ontogeny. Postnatal differences in cranial ontogeny between the two taxa are characterized primarily by heterochronic modifications of a common spatial pattern of development. Evidence for early ontogenetic divergence together with evolutionary stasis of taxon-specific patterns of ontogeny is consistent with separation of Neanderthals and modern humans at the species level.

Adolescent↗

Ontogeny and homoplasy in the papionin monkey face.

Recent molecular research has provided a consistent estimate of phylogeny for the living papionin monkeys (Cercocebus, Lophocebus, Macaca, Mandrillus, Papio, and Theropithecus). This phylogeny differs from morphological phylogenies regarding the relationships of the mangabeys (Cercocebus and Lophocebus) and baboons (Mandrillus, Papio, and Theropithecus). Under the likely assumption that the molecular estimate is correct, the incongruence between the molecular and morphological data sets indicates that the latter include numerous homoplasies. Knowledge of how these homoplasies emerge through development is important for understanding the morphological evolution of the living papionins, and also for reconstructing the phylogenetic relationships and adaptations of their fossil relatives. Accordingly, we have used geometric morphometric techniques and the molecular phylogeny to investigate the ontogeny of a key area of morphological homoplasy in papionins, the face. Two analyses were carried out. The first compared allometric vectors of Cercocebus, Lophocebus, Macaca, Mandrillus, and Papioto determine which of the facial resemblances among the genera are homoplasic and which are plesiomorphic. The second analysis focused on early post-natal facial form in order to establish whether the facial homoplasies exhibited by the adult papionins are to some degree present early in the post-natal period or whether they develop only later in ontogeny. The results of our analyses go some way to resolving the debate over which papionin genera display homoplasic facial similarities. They strongly suggest that the homoplasic facial similarities are exhibited by Mandrillus and Papio and not by Cercocebus and Lophocebus, which share the putative primitive state with Macaca. Our results also indicate that Mandrillus and Papio achieve their homoplasic similarities in facial form not through simple extension of the ancestral allometric trajectory but through a combination of an extension of allometry into larger size ranges and a change in direction of allometry away from the ancestral trajectory. Thus, the face of Mandrillus is not simply a hypermorphic version of the face of its sister taxon, Cercocebus, and the face of Papio is not merely a scaled-up version of the face of its sister taxon, Lophocebus. Lastly, our results show that facial homoplasy is not restricted to adult papionins; it is also manifest in infant and juvenile papionins. This suggests that the homoplasic facial similarities between Mandrillus and Papio are unlikely to be a result of sexual selection.

Animals↗