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.     

中华蟾蜍蝌蚪颅骨发育的形态计量学分析

采用TPS(thin-plate spline)形态计量软件计量了中华蟾蜍Bufogargarizans幼体蝌蚪发育中软骨性颅骨的11项形态指标的变化,采用颅骨总长(TLC,the total length of chondrocranium)线性回归分析了各形态特征与颅骨总长的关系。通过对中华蟾蜍幼体蝌蚪颅骨的线性形态测量,结果表明喙上软骨、内睑部关节距等呈负异速生长,外睑部关节距呈同速生长;听囊等感受结构呈正异速生长,与Emerson等人的观点有所不同。基于中华蟾蜍幼体蝌蚪各期样本之间颅骨的发育存在着较大的差异,在实验样本的选取中既要考虑Gosner的分期,还要考虑同期蝌蚪个体体型大小。     

Patterns of cranial shape variation in the Papionini (Primates: Cercopithecinae)

Traditional classifications of the Old World monkey tribe Papionini (Primates: Cercopithecinae) recognized the mangabey genera Cercocebus and Lophocebus as sister taxa. However, molecular studies have consistently found the mangabeys to be diphyletic, with Cercocebus and Mandrillus forming a clade to the exclusion of all other papionins. Recent studies have identified cranial and postcranial features which distinguish the Cercocebus-Mandrillus clade, however the detailed similarities in cranial shape between the mangabey genera are more difficult to reconcile with the molecular evidence. Given the large size differential between members of the papionin molecular clades, it has frequently been suggested that allometric effects account for homoplasy in papionin cranial form. A combination of geometric morphometric, bivariate, and multivariate methods was used to evaluate the hypothesis that allometric scaling contributes to craniofacial similarities between like-sized papionin taxa. Patterns of allometric and size-independent cranial shape variation were subsequently described and related to known papionin phylogenetic relationships and patterns of development.Results confirm that allometric scaling of craniofacial shape characterized by positive facial allometry and negative neurocranial allometry is present across adult papionins. Pairwise comparisons of regression lines among genera revealed considerable homogeneity of scaling within the Papionini, however statistically significant differences in regression lines also were noted. In particular, Cercocebus and Lophocebus exhibit a shared slope and significant vertical displacement of their allometric lines relative to other papionins. These findings give no support to narrowly construed hypotheses of uniquely shared patterns of allometric scaling, either between sister taxa or across all papionins. However, more general allometric trends do appear to account for a substantial proportion of papionin cranial shape variation, most notably in those features which have influenced traditional morphological phylogenies. Examination of size-uncorrelated shape variation gives no clear support to molecular phylogenies, but underscores the absence of morphometric similarities between the mangabey genera when size effects are controlled. Patterns of allometric and size-uncorrelated shape variation indicate conservatism of cranial form in non- Theropithecus papionins, and suggest that Papio represents the primitive morphometric pattern for the African papionins. Lophocebus exhibits a divergent morphometric pattern, clearly distinguishable from other papionins, most notably Cercocebus. These results clarify patterns of cranial shape variation among the extant Papionini and lay the groundwork for studies of related fossil taxa.     

Chondrocranial ontogeny of Pelodytes punctatus (Anura: Pelodytidae). Response to competition: geometric morphometric and allometric change analysis

Garriga, N. and Llorente, G.A. 2011. Chondrocranial Ontogeny of Pelodytes punctatus (Anura: Pelodytidae). Response to competition: Geometric Morphometric and Allometric Change Analysis. —Acta Zoologica (Stockholm) 93 : 453–464. The chondrocranial development of Pelodytes punctatus is described, from tadpole to froglet, and compared with that of other taxa reported previously, such as species in the Pelobatidae, Pipidae, Ranidae, Hylidae, Bombinatoridae, Leptodactylidae, or Microhylidae families. The comparison leads us to suggest that the ontogeny of the anuran chondrocranium is very conservative, making it difficult to discern phylogenetic or ecologic patterns. Chondrocranial development is also analyzed to quantify shape changes and allometries during ontogeny, using linear and geometric morphometrics. The main shape change observed follows the general pattern of vertebrate postnatal development. The allometric analysis indicates the presence of different functional units in the chondrocranium that could be subjected to different pressures. Finally, tadpoles were raised in two conditions of competition to compare their chondrocranium development. The largest shape differences between the two conditions are located in the anterior region of the cranium and fit the general response to competition stress by increasing growth rate. Comparison of the scaling pattern between Pelodytes and Rana sylvatica and Bufo americanus shows differences, principally in the oral region, that do not fit with the general allometric pattern in larval anurans proposed in previous studies.     

Early development of chondrocranium in the tailed frog Ascaphus truei (Amphibia: Anura): Implications for anuran palatoquadrate homologies

Chondrocranial development in Ascaphus truei was studied by serial sectioning and graphical reconstruction. Nine stages (21–29; 9–18 mm TL) were examined. Mesodermal cells were distinguished from ectomesenchymal (neural crest derived) cells by retained yolk granules. Ectomesenchymal parts of the chondrocranium include the suprarostrals, pila preoptica, anterior trabecula, and palatoquadrate. Mesodermal parts of the chondrocranium include the orbital cartilage, posterior trabecula, parachordal, basiotic lamina, and otic capsule. Development of the palatoquadrate is as follows. The pterygoid process first connects with the trabecula far rostrally; their fusion progresses caudally. The ascending process connects with a mesodermal bar that extends from the orbital cartilage to the otic capsule, and forms the ventral border of the dorsal trigeminal outlet. This bar is the “ascending process” of Ascaphus adults; it is a neurocranial, not palatoquadrate structure. The basal process chondrifies in an ectomesenchymal strand running from the quadrate keel to the postpalatine commissure. Later, the postpalatine commissure and basal process extend anteromedially to contact the floor of the anterior cupula of the otic capsule, creating separate foramina for the palatine and hyomandibular branches of the facial nerve. Based on these data, and on comparison with other frogs and salamanders, the anuran anterior quadratocranial commissure is homologized with the pterygoid process of salamanders, the anuran basal process (=“pseudobasal” or “hyobasal” process) with the basal process of salamanders, and the anuran otic ledge with the basitrabecular process of salamanders. The extensive similarities in palatoquadrate structure and development between frogs and salamanders, and lacking in caecilians, are not phylogenetically informative. Available information on fossil outgroups suggests that some of these similarities are primitive for Lissamphibia, whereas for others the polarity is uncertain. J. Morphol. 231:63-100, 1997. © 1997 Wiley-Liss, Inc.     

Cranial capacity/cranial base relationships and prediction of vault form: A canonical correlation analysis

Canonical correlation analysis was used to test an hypothesized morphological relationship between vault form and cranial capacity relative to length of the chondrocranium. Ninety-five adult male Czech skulls were measured for vault form expressed as length, width and height of the brain case; the chondrocranium was represented by nasion-basion and basion-opisthion lengths. In terms of explained variation, the first and most important dimension of covariation between vault and chondrocranial variables was size. The second most significant dimension of covariation expressed the hypothesized shape relationships—i.e., overall size being equal, the shorter the chondrocranial base relative to cranial capacity, the shorter and wider the vault. Furthermore, the competing hypothesis that vault form is determined by facial length proved untenable since facial length was predictive of vault shape only when measured as prosthion-basion, a measure that incorporates basal length. When corrected for basal length, facial length is unrelated to vault form. The results are consistent with the assumption that phylogenetic and microevolutionary trends toward brachycephaly in man stem from changes in the relationship between two components of skull growth, the chondrocranial base and the brain.     

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.     

Modern humans are not (quite) isometric

Allometric relationships are important sources of information for many types of anthropological and biological research. The baseline for all allometric relationships is isometry (or geometric similarity), the principal that shape is invariant of size. Here, we formally test for geometric similarity in modern humans, looking at the maximum lengths of four long bones (humerus, radius, femur, and tibia). We use Jolicoeur's multivariate allometry method to examine globally distributed samples of human populations, both collectively and individually. Results indicate that humans are not geometrically similar, although morphological deviations from isometry are small.     

Testing the cranial evolutionary allometric ‘rule’ in Galliformes

Recent comparative studies have indicated the existence of a common cranial evolutionary allometric (CREA) pattern in mammals and birds, in which smaller species have relatively smaller faces and bigger braincases than larger species. In these studies, cranial allometry was tested using a multivariate regression between shape (described using landmarks coordinates) and size (i.e. centroid size), after accounting for phylogenetic relatedness. Alternatively, cranial allometry can be determined by comparing the sizes of two anatomical parts using a bivariate regression analysis. In this analysis, a slope higher or lower than one indicates the existence of positive or negative allometry, respectively. Thus, in those species that support the CREA ‘rule’, positive allometry is expected for the association between face size and braincase size, which would indicate that larger species have disproportionally larger faces. In this study, I applied these two approaches to explore cranial allometry in 83 Galliformes (Aves, Galloanserae), ranging in mean body weight from 30 g to 2.5 kg. The multivariate regression between shape and centroid size revealed the existence of a significant allometric pattern resembling CREA, whereas the second analysis revealed a negative allometry for beak size and braincase size (i.e. contrary to the CREA ‘rule’, larger galliform species have disproportionally shorter beaks than smaller galliform species). This study suggests that the presence of CREA may be overestimated when using cranium size as the standard measurement.     

Does allometry account for shape variability in <Emphasis Type="Italic">Ephedrus persicae</Emphasis> Froggatt (Hymenoptera: Braconidae: Aphidiinae) parasitic wasps?

We analysed linear measurements on various parts of the body and the configuration of 11 landmarks on the wing in a large sample of Ephedrus persicae that had emerged from 13 aphid host species, to assess whether static allometry (a measure of the scaling relationship between traits in a population of individuals at the same ontogenetic stage) accounts for variation in body shape. The analysed specimens came from several localities in Europe, Asia Minor, Japan and South America, and cover a large portion of the distribution area of E. persicae. We found that allometry accounts for variation in body shape among different biotypes within the E. persicae group. The allometric slopes for head size (HD), petiolus width (PETW), mesoscutum width (MSC), and ovipositor sheath length (OVPL) diverged significantly among biotypes, indicating biotype-specific allometries. The analysis of allometric variation in wing shape showed that the pattern and direction of allometric changes also differed among individuals that had emerged from different hosts. Our results (observed divergences in the directions of allometric slopes of particular morphometric traits and wing shape) suggest that allometric relations within E. persicae are not conserved, so that allometry itself changes, evolving differently in aphid parasitoids that emerge from different hosts.     

The larval chondrocranium of Pelodytes punctatus,with a review of tadpole chondrocrania

The larval chondrocranium of the pelobatoid anuran Pelodytes punctatus was studied, using Alcian blue-alizarin stained and cleared whole preparations, serial sections, and gross dissections. This beaked tadpole is an unspecialized pond dweller and its chondrocranium closely resembles those of other ecologically similar tadpoles of diverse systematic relationships. Detailed analysis, however, shows many differences among the chondrocrania of anuran larvae. Among other features, these include the configurations of suprarostrals, fronto-parietal fenestrae, palatoquadrate suspensoria, the ligamentum or cartilago tectum of the muscular process of the quadrate and the circumoral ligaments. The lateral circumoral ligament permits differentiation of beaked discoglossoidean and ranoidean larvae. Microhyloids conform to the ranoidean pattern in this feature. Pipoids either lack it or seem to conform to the discoglossoidean pattern. Use of these larval features as key characters enables assignment of Pelodytes to an uncertain position among pelobatoid frogs. This is totally congruent with previous assignments based on adult features and is used to support the hypothesis that anuran phylogenies based on larval characters will closely resemble, in major features at least, those based solely on adult characters.     

Miniaturization and its effects on cranial morphology in plethodontid salamanders, genus Thorius (Amphibia, Plethodontidae): II. The fate of the brain and sense organs and their role in skull morphogenesis and evolution

Relative size and arrangement of the brain and paired sense organs are examined in three species of Thorius, a genus of minute, terrestrial salamanders that are among the smallest extant tailed tetrapods. Analogous measurements of representative species of three related genera of larger tropical (Pseudoeurycea, Chiropterotriton) and temperate (Plethodon) salamanders are used to identify changes in gross morphology of the brain and sense organs that have accompanied the evolution of decreased head size in Thorius and their relation to associated changes in skull morphology. In adult Thorius, relative size (area measured in frontal plane, and length) of the eyes, otic capsules, and brain each is greater than in adults of all of the larger genera; relative size of the nasal capsules is unchanged or slightly smaller. Interspecific scaling phenomena--negative allometry of otic capsule, eye and brain size, isometry or slight positive allometry of nasal capsule size, all with respect to skull length--also are characteristic of intraspecific (ontogenetic) comparisons in both T. narisovalis and Pseudoeurycea goebeli. Predominance of the brain and eyes in Thorius results in greater contact and overlap among these structures and the nasal capsules in the anterior portion of the head. This is associated with anterior displacement of both the eyes and nasal capsules, which now protrude anterior to the skull proper; a change in eye shape; and medial deformation of anterior braincase walls. Posteriorly, predominance of the otic capsules has effected a reorientation of the jaw suspensorium to a fully vertical position that is correlated with the novel presence of a posteriorly directed squamosal process and shift in origin of the quadropectoralis muscle. Many of these changes in cranial morphology may be explained simply as results of mechanical (physical) interactions among the skeletal, nervous, and sensory components during head development at reduced size. This provides further evidence of the role of nervous, sensory, and other "soft" tissues in cranial skeletal morphogenesis, and reinforces the need to consider these tissues in analyses of skull evolution.     

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

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

Phylogenetic analysis of the African papionin basicranium using 3‐D geometric morphometrics: The need for improved methods to account for allometric effects

The basicranium has been argued to contain a strong phylogenetic signal in previous analyses of primate cranial morphology. Therefore, further study of basicranial morphology may offer new insights into controversial phylogenetic relationships within primate groups. In this study, I apply 3‐D geometric morphometric techniques in a phylogenetic analysis of the African papionin basicranium. The effects of allometry strongly influence African papionin basicranial morphology and, unless these size effects are controlled or eliminated, phylogenetic analyses suggest traditional phylogenetic groupings of small taxa (mangabeys) and large taxa (geladas, mandrills, drills, and baboons). When the effects of allometry are eliminated by excluding size‐correlated principal components (PCs) or by regression analysis with retention of residuals, phylogenetic analyses of African papionin basicranial morphology are incongruent with recent molecular and morphological studies. By contrast, a cladistic analysis of basicranial characters using the narrow allometric coding method suggests the same phylogenetic relationships as recent molecular and morphological studies. These results suggest that important phylogenetic information is contained within the size‐correlated data, and this information is being discarded during the attempt to eliminate the effects of body size. Future 3‐D morphometric studies of phylogeny should focus on the development of new methodologies to adjust for allometric effects, as current techniques appear to be ill‐equipped to deal with the case of a size‐disparate, lower‐level taxonomic group. Am J Phys Anthropol, 2010. © 2010 Wiley‐Liss, Inc.     

Postmetamorphic ontogenetic allometry and the evolution of skull shape in Nest‐building frogs Leptodactylus (Anura: Leptodactylidae)

Allometry constitutes an important source of morphological variation. However, its influence in head development in anurans has been poorly explored. By using geometric morphometrics followed by statistical and comparative methods we analyzed patterns of allometric change during cranial postmetamorphic ontogeny in species of Nest‐building frogs Leptodactylus (Leptodactylidae). We found that the anuran skull is not a static structure, and allometry plays an important role in defining its shape in this group. Similar to other groups with biphasic life‐cycle, and following a general trend in vertebrates, ontogenetic changes mostly involve rearrangement in rostral, otoccipital, and suspensorium regions. Ontogenetic transformations are paralleled by shape changes associated with evolutionary change in size, such that the skulls of species of different intrageneric groups are scaled to each other, and small and large species show patterns of paedomorphic/peramorphic features, respectively. Allometric trajectories producing those phenotypes are highly evolvable though, with shape change direction and magnitude varying widely among clades, and irrespective of changes in absolute body size. These results reinforce the importance of large‐scale comparisons of growth patterns to understand the plasticity, evolution, and polarity of morphological changes in different clades.     

Understanding reproductive allometry in turtles: A slippery “slope”

Measures of reproductive output in turtles are generally positively correlated with female body size. However, a full understanding of reproductive allometry in turtles requires logarithmic transformation of reproductive and body size variables prior to regression analyses. This allows for slope comparisons with expected linear or cubic relationships for linear to linear and linear to volumetric variables, respectively. We compiled scaling data using this approach from published and unpublished turtle studies (46 populations of 25 species from eight families) to quantify patterns among taxa. Our results suggest that for log–log comparisons of clutch size, egg width, egg mass, clutch mass, and pelvic aperture width to shell length, all scale hypoallometrically despite theoretical predictions of isometry. Clutch size generally scaled at ~1.7 to 2.0 (compared to an isometric expectation of 3.0), egg width at ~0.5 (compared to an expectation of 1.0), egg mass at ~1.1 to 1.3 (3.0), clutch mass at ~2.5 to 2.8 (3.0), and pelvic aperture width at 0.8–0.9 (1.0). We also found preliminary evidence that scaling may differ across years and clutches even in the same population, as well as across populations of the same species. Future investigators should aspire to collect data on all these reproductive parameters and to report log–log allometric analyses to test our preliminary conclusions regarding reproductive allometry in turtles.     

Cranial neural-crest migration and chondrogenic fate in the oriental fire-bellied toad Bombina orientalis: Defining the ancestral pattern of head development in anuran amphibians

We assess cranial neural-crest cell migration and contributions to the larval chondrocranium in the phylogenetically basal and morphologically generalized anuran Bombina orientalis (Bombinatoridae). Methods used include microdissection, scanning electron microscopy, and vital dye labeling, in conjunction with confocal and fluorescence microscopy. Cranial neural-crest cells begin migrating before neural-fold closure and soon form three primary streams. These streams contribute to all cranial cartilages except two medial components of the hyobranchial skeleton (basihyal and basibranchial cartilages), the posterior portion of the trabecular plate, and the otic capsule, the embryonic origin of which is unknown. Chondrogenic fate is regionalized within the cranial neural folds, with the anterior regions contributing to anterior cartilages and the posterior regions to posterior cartilages. A neural-crest contribution also was consistently observed in several cranial nerves and the connective tissue component of many cranial muscles. Notwithstanding minor differences among species in the initial configuration of migratory streams, cranial neural-crest migration and chondrogenic potential in metamorphosing anurans seem to be highly stereotyped and evolutionarily conservative. This includes a primary role for the neural crest in the evolutionary origin of the paired suprarostral and infrarostral cartilages, two prominent caenogenetic features of the rostral skull unique to anuran larvae. Our results provide a model of the ancestral pattern of embryonic head development in anuran amphibians. This model can serve as a basis for examining the ontogenetic mechanisms that underlie the diversity of cranial morphology and development displayed by living frogs, as well as the evolutionary consequences of this diversity. © 1996 Wiley-Liss, Inc.     

草兔胚后发育过程中头骨大小与形状变化的几何形态学分析(兔形目:兔科)

在本文中,我们使用几何形态学的研究方法对58 个处于不同年龄阶段的草兔头骨进行了分析。分析中总共使用来自头骨背面、腹面和侧面的180 个标点和半标点。研究结果表明,草兔在胚后发育早期即迅速建立起与成年个体近似的形态结构,组成头骨的不同形态单元存在显著的异速生长现象,主要的形变发生在幼年至年龄1 阶段,即出生后的6 个月以内。从大小的变化来看,鼻骨在胚后发育过程中呈现正的异速生长,额骨和眼眶区则与头骨整体大小变化基本等速,而顶骨、听泡和枕骨大孔则呈现显著的负异速生长。我们亦用几何形态学的方法绘制出头骨在生长发育早期和晚期不同部位的形态变化轨迹,这一结果显示较显著的形状变化发生在鼻骨、前颌骨、眶上突和头骨的纵轴方向。头骨整体形态在胚后发育过程中伸长并变窄。这些变化将有利于幼兔较早实现完善的头部系统的建立,尤其有利于提高呼吸系统的通风能力,提高在高强度的捕食压力下保持警觉,在多样的运动过程中保持身体平稳的能力,也可能进一步提高了对固态食物的处理能力。这种异速生长模式可能是善于奔跑的植食性哺乳动物在功能需求上的一种适应性进化特征。