Ontogenetic study of the skull in modern humans and the common chimpanzees: neotenic hypothesis reconsidered with a tridimensional Procrustes analysis

Heterochronic studies compare ontogenetic trajectories of an organ in different species: here, the skulls of common chimpanzees and modern humans. A growth trajectory requires three parameters: size, shape, and ontogenetic age. One of the great advantages of the Procrustes method is the precise definition of size and shape for whole organs such as the skull. The estimated ontogenetic age (dental stages) is added to the plot to give a graphical representation to compare growth trajectories. We used the skulls of 41 Homo sapiens and 50 Pan troglodytes at various stages of growth. The Procrustes superimposition of all specimens was completed by statistical procedures (principal component analysis, multivariate regression, and discriminant function) to calculate separately size-related shape changes (allometry common to chimpanzees and humans), and interspecific shape differences (discriminant function). The results confirm the neotenic theory of the human skull (sensu Gould [1977] Ontogeny and Phylogeny, Cambridge: Harvard University Press; Alberch et al. [1979] Paleobiology 5:296-317), but modify it slightly. Human growth is clearly retarded in terms of both the magnitude of changes (size-shape covariation) and shape alone (size-shape dissociation) with respect to the chimpanzees. At the end of growth, the adult skull in humans reaches an allometric shape (size-related shape) which is equivalent to that of juvenile chimpanzees with no permanent teeth, and a size which is equivalent to that of adult chimpanzees. Our results show that human neoteny involves not only shape retardation (paedomorphosis), but also changes in relative growth velocity. Before the eruption of the first molar, human growth is accelerated, and then strongly decelerated, relative to the growth of the chimpanzee as a reference. This entails a complex process, which explains why these species reach the same overall (i.e., brain + face) size in adult stage. The neotenic traits seem to concern primarily the function of encephalization, but less so other parts of the skull. Our results, based on the discriminant function, reveal that additional structural traits (corresponding to the nonallometric part of the shape which is specific to humans) are rather situated in the other part of the skull. They mainly concern the equilibrium of the head related to bipedalism, and the respiratory and masticatory functions. Thus, the reduced prognathism, the flexed cranial base (forward position of the foramen magnum which is brought closer to the palate), the reduced anterior portion of the face, the reduced glabella, and the prominent nose mainly correspond to functional innovations which have nothing to do with a neotenic process in human evolution. The statistical analysis used here gives us the possibility to point out that some traits, which have been classically described as paedomorphic because they superficially resemble juvenile traits, are in reality independent of growth.     

Facultative paedomorphosis and the pattern of intra- and interspecific variation in cranial skeleton: lessons from European newts (Ichthyosaura alpestris and Lissotriton vulgaris)

Paedomorphosis, the presence of ancestral larval and juvenile traits that occur at the descendent adult stage, is an evolutionary phenomenon that shaped morphological evolution in many vertebrate lineages, including tailed amphibians. Among salamandrid species, paedomorphic and metamorphic phenotypes can be observed within single populations (facultative paedomorphosis). Despite wide interest in facultative paedomorphosis and polymorphism produced by heterochronic changes (heterochronic polymorphism), the studies that investigate intraspecific morphological variation in facultative paedomorphic species are largely missing. By quantifying the cranium size and development (bone development and remodeling), we investigated the variation at multiple levels (i.e., between sexes, populations and species) of two facultatively paedomorphic European newt species: the alpine and the smooth newt. The pattern of variation between paedomorphs (individuals keeping larval traits at the adult stage) and metamorphs (metamorphosed adult individuals) varied between species and among populations within a single species. The patterns of variation in size and skull formation appear to be more uniform in the alpine than in the smooth newt, indicating that developmental constraints differed between species (more pronounced in alpine than in smooth newt). Our study shows that the cranial skeleton provides detailed insight in the pattern of variation and divergence in heterochronic polymorphism within and between species and open new questions related to heterochronic polymorphism and evolution of cranial skeleton.     

Heterochronic differentiation of sexual dimorphs among Jurassic ammonite species

Ontogenetic and then heterochronic approaches are used here to analyze sexual differentiation within two well-known Jurassic dimorphic species. This analysis compares two ways of determining the relative biological age of ammonites, one using size (diameter) and the other the number of septa as a proxy of age. The shape standard is established from factor analysis of morphological and growth parameters. Size-age-shape relationships are analyzed on the basis of a new heterochronic representation. When diameter is used as a proxy of age, microconch morphs are globally considered to be progenetic compared with macroconch morphs. When size and age are determined separately and shape is included, (1) Ebrayiceras jactatum (microconch morph) has a shorter period of growth (progenesis) with acceleration of shape compared with its macroconch morph ( Morphoceras macrescens ), (2)( Cardioceras cordatum (microconch morph) has a shorter period of growth (progenesis) coupled with a slower rhythm of growth (dwarfism) compared with its macroconch morph. These findings emphasize the complex relationship between supposed sexual dimorphs in ammonites when size and age standards can be separated, as well as the need for an ontogenetic approach.     

Geometric morphometric analysis of Eysarcoris guttiger,E.annamita and E.ventralis (Hemiptera: Pentatomidae)

The genus Eysarcoris can be easily distinguished from other genera through the two spots in the basal angle of the scutellum.Nevertheless,Eysarcoris species show complex variances.Geometric morphometric methods have been increasingly applied to distinguish species and to define the boundary of genera among insects.In the present study,geometric morphometric approach was firstly employed to evaluate the shape variation of three characters (fore wing,hind wing and pygophore) of E.guttiger,E.annamita and E.ventralis using E.aeneus as outgroup to ascertain whether this approach is a reliable method for the taxonomy of Eysarcoris.Analysis was conducted on the landmarks of the three characters of these species.Multivariate regression of procrustes coordinates against centroid size was conducted to test the presence of allometry.Principal component analysis (PCA),canonical variate analysis (CVA)and cluster analysis were utilized to describe variations in shapes among the studied species.For all of the three characters,though PCA analysis showed some overlap among species,p-values for procrustes distance and mahalanobis distance were all less than 0.0001.The distribution of the three studied species corresponds with their species status.This study demonstrates that the geometric morphometrics of both the fore wing and the hind wing might represent a possible tool for the identification of species within this genus.     

Heterochrony during skeletal development of Pseudis platensis (anura,hylidae) and the early offset of skeleton development and growth

The aquatic frog Pseudis platensis has a giant tadpole, long developmental time, and dissociated metamorphic events that include later offset of larval somatic morphologies. Moreover, when the tadpole metamorphoses, the young frog is nearly the size of an adult, suggesting that this species has low rates of postmetamorphic growth. Herein, we study the development of the skeleton during larval development up to the end of metamorphosis, which is denoted by the complete lost of the tail in P. platensis. Our study revealed heterochronic differences in skeletal development compared with that of most anurans; these involve the complete differentiation of skull bones and the extensive ossification of the postcranial skeleton before completion of metamorphosis. The skull of metamorphosing P. platensis has an ossified sphenethmoid and a fully formed plectral apparatus, thus differing with regard to the pattern observed in most anurans in which both developmental events take place during the postmetamorphic life. Despite the fact that the iliosacral articulation and the urostyle are present at the end of metamorphosis as in most anurans, ossification/calcification of carpus, tarsus, and limb epihyses during metamorphosis of P. platensis suggests that the postcranial skeleton lacks postmetamorphic growth. This study also includes a discussion of the pattern of development of the plectral apparatus, which allows us to propose a new hypothesis regarding pars externa plectri homology. J. Morphol., 2009. © 2008 Wiley‐Liss, Inc.     

Geometric morphometrics of the skull of various murid rodents (Mammalia, Rodentia): relation of the skull shape to the trophic specialization

Presented is a brief overview of basic principles and notions of geometric morphometrics, a new approach to quantitative analysis of shape variations. This approach is applied to analysis of variation of the skull shape in the sample of 18 muroid genera belonging to the families Cricetidae, Arvicolidae and Gerbillidae. The skull shape is described by landmarks, and skulls are compared by resistant fit and superimposition methods. Under consideration is relation of skull shape to the trophic specialization, to family belonging, and to body size. Axial skull reveals more conspicuous relation to each of the factor analyzed as compared to mandible. Zygomatic region and tooth raw are most differentiable, while change of auditory bulla is of secondary effect. Transition from omnivorous through granivorous to grass-eating specialization involves the same trend in each of the family studied in the case of axial skull but not of mandible. Most dependent of trophic specialization appeared to be shape of axial skull rather then of mandible. Arvicolines are most specific in respect to the skull shape. Shape to size relation, although rather slight, also involves the same zygomatic-dental region. The results obtained indicate probably that geometric morphometrics does reveal variations in the skull shape that are free of the size effect.     

Testing heterochrony: Connecting skull shape ontogeny and evolution of feeding adaptations in baleen whales

Ontogeny plays a key role in the evolution of organisms, as changes during the complex processes of development can allow for new traits to arise. Identifying changes in ontogenetic allometry—the relationship between skull shape and size during growth—can reveal the processes underlying major evolutionary transformations. Baleen whales (Mysticeti, Cetacea) underwent major morphological changes in transitioning from their ancestral raptorial feeding mode to the three specialized filter-feeding modes observed in extant taxa. Heterochronic processes have been implicated in the evolution of these feeding modes, and their associated specialized cranial morphologies, but their role has never been tested with quantitative data. Here, we quantified skull shapes ontogeny and reconstructed ancestral allometric trajectories using 3D geometric morphometrics and phylogenetic comparative methods on sample representing modern mysticetes diversity. Our results demonstrate that Mysticeti, while having a common developmental trajectory, present distinct cranial shapes from early in their ontogeny corresponding to their different feeding ecologies. Size is the main driver of shape disparity across mysticetes. Disparate heterochronic processes are evident in the evolution of the group: skim feeders present accelerated growth relative to the ancestral nodes, while Balaenopteridae have overall slower growth, or pedomorphosis. Gray whales are the only taxon with a relatively faster rate of growth in this group, which might be connected to its unique benthic feeding strategy. Reconstructed ancestral allometries and related skull shapes indicate that extinct taxa used less specialized filter-feeding modes, a finding broadly in line with the available fossil evidence.     

Brachyspira asperella Yu et Zhang的个体发育

对Brachyspira asperella Yu et Zhang的40个个体的测量统计表明,此种在生长发育过程中可以区分出3个生长阶段:幼年期壳体生长速度缓慢,壳形卵圆形,胎壳乳突状,壳口圆形;成年期生长迅速,壳高显著大于壳宽的增长率,壳形卵圆形-长卵圆形,壳口卵圆形;老年期生长速度缓慢,壳形长卵圆形,壳饰强烈。这3个生长期代表了此种的个体发育过程。研究化石腹足类种的个体发育过程不仅能了解这一类群的系统发生史、生物演化过程及生物间的亲缘关系,而且能提高物种研究程度,避免分类上的错误。     

Heterochronic mechanisms of morphological diversification and evolutionary change in the neotropical salamander,Bolitoglossa occidentalis (Amphibia: Plethodontidae)

Bolitoglossa occidentalis, a lowland salamander of Mexico and Guatemala, has a highly derived morphology. The features that are derived with respect to the condition in generalized members of the genus include the following: (1) small body size; (2) short tail; (3) fully webbed hands and feet; (4) reduction and loss of certain phalangeal elements; (5) fusion of carpals and tarsals; (6) absence of prefrontal bones; and (7) reduced skull ossification. The ontogeny of this species was analyzed quantitatively and compared with the patterns of growth and differentiation encountered in two morphologically generalized members of the genus, B. rostrata and B. subpalmata. Most of the derived features can be explained by invoking a single heterochronic process: truncation of development at a small size (most likely the product of early maturation). Therefore, B. occidentalis is a paedomorphic species whose morphology has been attained through the process of progenesis. This result supports Alberch's ('80a) prediction, based on functional analysis, that the principle adaptation to arboreality in B. occidentalis is small size; other derived morphological features are associated with the organism's truncated development and may have no adaptive significance. However, patterns of dissociation are found within this overall progenetic process. Some of these include the following: (1) accelerated growth rates of the metatarsals and first phalanges, and retarded growth rates of the second and third phalangeal elements; (2) dissociation between rates of ossification of the skull and the autopodial elements; and (3) dissociation between the timing of termination of the process of shape change during the ontogeny of the foot (the product of differential growth between digital and interdigital areas) and termination of growth in overall foot size (foot surface area). This later result illustrates the independence of morphogenetic phenomena (shape change) from processes of growth (size increase).     

GENETIC ANALYSIS OF SKULL SHAPE VARIATION AND MORPHOLOGICAL INTEGRATION IN THE MOUSE USING INTERSPECIFIC RECOMBINANT CONGENIC STRAINS BETWEEN C57BL/6 AND MICE OF THE MUS SPRETUS SPECIES

To assess the genetic basis of the skull shape variation and morphological integration in mice, we have used a tool based on the cross between the distantly related mouse species Mus spretus (SEG/Pas strain) and the laboratory strain C57BL/6 called interspecific recombinant congenic strains (IRCSs). The genome of each IRCS consists on average of 1.3% of SEG/Pas derived sequences, located on multiple chromosomes as small-sized, DNA segments. Quantitative trait loci (QTL) on the skull shape, separated into dorsal and ventral sides, were analyzed in 17 IRCSs by a Procrustes superimposition method using 3D landmarks. The shapes of 16 strains differed significantly from C57BL/6. Discrepancy in the QTLs effects was found between the dorsal side and the anterior region of the ventral side due to a differential effect of the SEG/Pas alleles on the skull shape. A comprehensive analysis of all allelic combinations of the BCG-66H strain showed strong epistatic interactions between SEG/Pas segment acting on both skull sides. Epistatic pleiotropy and covariation between sides were dependent in SEG/Pas alleles direction and contributed to the strong morphological integration between sides. Introduction of Mus spretus alleles in a C57BL/6 background induced strong morphological changes mostly in SEG/Pas alleles direction and provided evidence for high level of morphological integration.     

Heterochrony, maternal effects, and phenotypic variation among sympatric pupfishes

Variation in ontogeny can produce phenotypic variation both within and among species. I investigated whether changes in timing and rate of growth were a source of phenotypic variation in a putative incipient species group of pupfish (Cyprinodon spp.). On San Salvador Island, Bahamas, sympatric forms of pupfish differ in morphology but show only partial reproductive isolation in the laboratory. Offspring from two forms and two geographical areas and their hybrids were bred in the laboratory, and ontogenetic trajectories of their feeding morphology were followed until maturity. In the Bahamian pupfish the two forms grow along similar size but not shape trajectories. Two heterochronic parameters, onset and rate of growth, alter shape trajectories in the Bahamian pupfish. Similar forms from different geographical areas (Florida and the Bahamas) grow along parallel shape trajectories, differing only in one heterochronic parameter, the onset shape. Hybrids within and between the pupfish forms produced intermediate feeding morphologies that were influenced by their maternal phenotype, suggesting that maternal effects may be a source of phenotypic variation in shape that can persist to maturity. In Cyprinodon, small changes in multiple heterochronic parameters translate into large phenotypic differences in feeding morphology.     

From Jumbo to Dumbo: Cranial Shape Changes in Elephants and Hippos During Phyletic Dwarfing

Members of the mammalian families Elephantidae and Hippopotamidae (extant and extinct elephants and hippos) include extinct dwarf species that display up to 98% decrease in body size compared to probable ancestral sources. In addition to differences in body mass, skulls of these species consistently display distinctive morphological changes, including major reduction of pneumatised areas in dwarf elephants and shortened muzzles in dwarf hippos. Here we build on previous studies of island dwarf species by conducting a geometric morphometric analysis of skull morphology and allometry in target taxa, living and extinct, and elaborate on the relation between skull size and body size. Our analysis indicates that skull size and body size within terrestrial placental mammals scale almost isometrically (PGLS major axis slope 0.906). Furthermore, skull shape in dwarf species differed from both their ancestors and the juveniles of extant species. In insular dwarf hippos, the skull was subject to considerable anatomical reorganisation in response to distinct selection pressures affecting early ontogeny (the “island syndrome”). By contrast, skull shape in adult insular dwarf elephants can be explained well by allometric effects; selection on size may thus have been the main driver of skull shape in dwarf elephants. We suggest that a tightly constrained growth trajectory, without major anatomical reorganization of the skull, allowed for flexible adaptations to changing environments and was one of the factors underlying the evolutionary success of insular dwarf elephants.     

Ontogenetic allometry, heterochrony, and interspecific differences in the skull of African apes, using tridimensional Procrustes analysis

Ontogenetic studies of African ape skulls lead to an analysis of morphological differences in terms of allometry, heterochrony, and sexual dimorphism. The use of geometric morphometrics allows us 1) to define size and shape variations as independent factors (an essential but seldom respected condition for heterochrony), and 2) to calculate in percentage of shape changes and to graphically represent the parts of shape variation which are related to various biological phenomena: common allometry, intraspecific allometry, and allometric and nonallometric shape discrimination. Three tridimensional Procrustes analyses and the calculation of multivariate allometries, discriminant functions, and statistical tests are used to compare the skulls of 50 Pan troglodytes, and 50 Gorilla gorilla of different dental stages. The results both complement and modify classical results obtained from similar material but with different methods. Size and Scaling in Primate Morphology, New York: Plenum, p. 175-205). As previously described by Shea, the common growth allometric pattern is very important (64% of total shape variation). It corresponds to a larger increase of facial volume than of neurocranial volume, a more obliquely oriented foramen magnum, and a noticeable reshaping of the nuchal region (higher inion). However, the heterochronic interpretation based on common allometry is rather different from Shea. Gorillas differ from chimpanzees not only with a larger magnitude of allometric change (rate peramorphosis), as is classically said, but also grow more in size than in shape (size acceleration). In other words, for a similar stage of growth, gorillas have the size and shape corresponding to older chimpanzees, and for a similar shape, gorillas have a larger size than chimpanzees. In contrast, sexual dimorphism actually corresponds to allometric changes only, as classically demonstrated (time hypermorphosis). Sexual dimorphism is here significant in adult gorillas alone, and solely in terms of allometry (size-related shape and size, given that sagittal and nuchal crests are not taken into account). The study also permits us to differentiate two different shape variations that are classically confused in ontogenetic studies: a very small part of allometric shape change which is specific to each species (1% of the total shape variation), and nonallometric species-specific traits independent of growth (8% of total shape change). When calculated in terms of intraspecific allometries (including common allometry and noncommon allometry), shape changes are more extensive in gorillas (36% of total shape change) than in chimpanzees (29% of total shape change). The allometric differences mainly concern the inion, which becomes higher; the position of the foramen magnum, more dorsally oriented; and the palate, more tilted in adult gorillas than in adult chimpanzees. In contrast, nonallometric species-specific traits in gorillas are the long and flat vault characterized by a prominent occipital region, the higher and displaced backward glabella, and the protrusive nose. Biomechanical schemes built from shape partition suggest that the increased out-of-plumb position of the head during growth is partially compensated in gorillas by a powerful nuchal musculature due to the peculiar shape of the occipital region.     

Characterization of the age-dependent shape of the pediatric thoracic spine and vertebrae using generalized procrustes analysis

Generalized Procrustes Analysis (GPA) is a superimposition method used to generate size-invariant distributions of homologous landmark points. Several studies have used GPA to assess the three-dimensional (3D) shapes of or to evaluate sex-related differences in the human brain, skull, rib cage, pelvis and lower limbs. Previous studies of the pediatric thoracic vertebrae suggest that they may undergo changes in shape as a result of normative growth. This study uses GPA and second order polynomial equations to model growth and age- and sex-related changes in shape of the pediatric thoracic spine. We present a thorough analysis of the normative 3D shape, size, and orientation of the pediatric thoracic spine and vertebrae as well as equations which can be used to generate models of the thoracic spine and vertebrae for any age between 1 and 19 years. Such models could be used to create more accurate 3D reconstructions of the thoracic spine, generate improved age-specific geometries for finite element models (FEMs) and used to assist clinicians with patient-specific planning and surgical interventions for spine deformity.     

The morphology and post-hatching development of the skull of Bolitoglossa nicefori (Caudata: Plethodontidae): developmental implications of recapitulation and repatterning

The cranial morphology of the direct-developing salamander Bolitoglossa nicefori and its post-hatching development are described and compared with that of other urodeles. Four stages of cranial development are defined on the basis of conspicuous events that occur during post-hatching ontogeny. The adult skull morphology of B. nicefori is similar to that of other plethodontids; however, some regions show interspecific variation. The post-hatching ontogeny of the skull and the stage of ossification observed in the hatchlings of B. nicefori show two important ontogenetic features: (1) a mosaic of early larval, metamorphic and post-metamorphic skull features in hatchlings, and (2) absence of characteristic larval elements in skull and hyoid apparatus. The distinctive stage of ossification in the hatchlings of B. nicefori could be caused by heterochronic changes in the ossification sequence, compared to the ontogeny of metamorphic salamanders. The possible heterochronic changes and the absence of larval traits are perhaps due to ontogenetic repatterning, yet without an obvious impact on the adult skull morphology (absence of morphological novelties). This might indicate a compartmentalized development. Further studies should be performed in order to establish the possible occurrence of recapitulatory patterns or ontogenetic repatterning in the skull morphogenesis of B. nicefori during its embryonic development.     

Evolutionary development of the neurocranium in Dissorophoidea (Tetrapoda: Temnospondyli), an integrative approach

SUMMARY Ontogenetic data can play a prominent role in addressing questions in tetrapod evolution, but such evidence from the fossil record is often incompletely considered because it is limited to initiation of ossification, or allometric changes with increasing size. In the present study, specimens of a new species of an archaic amphibian (280 Myr old), Acheloma n. sp., a member of the temnospondyl superfamily Dissorophoidea and the sister group to Amphibamidae, which is thought to include at least two of our modern amphibian clades, anurans and caudatans (Batrachia), provides us with new developmental data. We identify five ontogenetic events, enabling us to construct a partial ontogenetic trajectory (integration of developmental and transformation sequence data) related to the relative timing of completion of neurocranial structures. Comparison of the adult amphibamid morphology with this partial ontogeny identifies a heterochronic event that occurred within the neurocranium at some point in time between the two taxa, which is consistent with the predictions of miniaturization in amphibamids, providing the first insights into the influence of miniaturization on the neurocranium in a fossil tetrapod group. This study refines hypotheses of large‐scale evolutionary trends within Dissorophoidea that may have facilitated the radiation of amphibamids and, projected forward, the origin of the generalized batrachian skull. Most importantly, this study highlights the importance of integrating developmental and transformation sequence data, instead of onset of ossification alone, into investigations of major events in tetrapod evolution using evidence provided by the fossil record, and highlights the value of even highly incomplete growth series comprised of relatively late‐stage individuals.     

Cranial shape differentiation in three closely related delphinid cetacean species: insights into evolutionary history

The present study investigates the pattern of differentiation of cranial shape in three closely related delphinid cetacean species of the complex Delphinus-Stenella-Tursiops: Delphinus delphis, Stenella coeruleoalba and Tursiops truncatus. Dorsal and ventral aspects of the cranium were analysed using landmark-based geometric morphometric methods. While there was no evidence of sexual dimorphism for shape or size, multivariate statistical analyses showed that there were interspecific differences in skull morphology. Skull shape differences between the three studied species were related with cranial width and differences in the length of the rostrum relative to the cranial portion of the skull. D. delphis and S. coeruleoalba showed high cranial shape similarity, which is indicative of their evolutionary proximity when compared with T. truncatus. Phenetic clusters based on cranial shape similarities were found to be concordant with the molecular phylogenetic clades obtained from mitochondrial DNA genes. Geometric morphometric methods can thus be an exceptionally useful tool for the study of differentiation of delphinid cetacean species and therefore provide some insights into their evolutionary history.     

Skull reconstruction and ecology of <Emphasis Type="Italic">Urmiatherium polaki</Emphasis> (Bovidae,Mammalia) from the upper Miocene deposits of Maragheh,Iran

Study of a newly discovered cranial specimen of Urmiatherium polaki from Karaj Abad site in Maragheh, Iran, allows us to describe the complete skull and present a new diagnosis for this late Miocene mammal species. In the comparative study of the specimen we propose the relative position of the upper teeth as a reliable metrical method for discriminating bovids of similar size. Based on the available information, a skull reconstruction of Urmiatherium polaki is provided and its ecological profile is outlined. Both the cranial and dental features of U. polaki indicate a gregarious grazing bovid of medium size, adapted to uneven ground and exhibiting ramming as the predominant fighting behavior.     

Heterochronies in the cranial development of Asian tree frogs (Amphibia: Anura: Rhacophoridae) with different life histories

The development of bony skull was studied in four species of Asian tree frogs (Rhacophoridae) with different life histories: biphasic development with free larval stage and direct development. In biphasic rhacophorids the sequence of the appearance of cranial bones generally followed the generalized pattern of craniogenesis, which was described for most studied anurans. In contrast, direct-developing species displayed some heterochronies in the formation of skull bones, namely, the accelerated formation of the anlagen of jaw and suspensorium bones. The obtained results support that the embryonization in amphibians is regularly accompanied by a heterochronic repatterning of craniogenesis, rather similar in different phyletic groups.     

饶阳地区三种农田啮齿类头骨形态比较及性二型

关于动物头骨形态方面的研究报道曾受到了较多的关注（Cesani et al., 2003）.头骨形态是动物形态特征的一个重要方面,受遗传和环境因素的共同影响,存在着种间、性别和地理差异（张焱等,1999）.头骨的形态特征不仅是动物生理上的一个基本解剖指标,同时也是动物分类（李晓晨和王廷正,1992）和年龄鉴定（张洁,1989）的重要依据,是动物生态研究的重要指标.对头骨形态的研究,不仅对动物的种间、种内关系（Yom et al.,1999）和生态特征（Barlow et al.,1997）等方面的研究具有重要的参考价值,在动物的地理演化、发育生物学以及进化生态学的研究中也具有十分重要的意义.