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.     

Functional and ecological significance of relative growth in Alligator

Allometric coefficients are calculated for 27 cranial and 39 postcranial measurements of a growth series of Alligator mississipiensis that spans a size range of an order of magnitude. Developmental patterns are quite-well canalized, as expressed in coefficients of variation of 8 to 10 for isometric variables. A multivariate expression of allometry is discovered using principal components analysis. A number of allometric coefficients have expression in known aspects of the life history of Alligator. Negative allometry of limb lengths and limb proportions shows an ontogenetic decrease in importance of the limbs throughout life, and observations show large animals to be more dependent on water than small ones. Isometry of skull length with respect to body length represents an adaptation to ever-increasing size of prey items as body size increases. Positive allometry of snout length and size of the upper temporal fenestrae finds parallel in the structure of the highly aquatic gavial.     

The life and times of Robert Smith

Summary

Robert Smith (1874–1900) is credited with having made the first systematic ecological studies to be carried out in Britain. His childhood in Dundee is described and consideration is given to the possible influence of his brother William and of the countryside of Angus and Ayrshire in forming his early interest in field botany and vegetation science. His pioneering studies were encouraged by Patrick Geddes and D'Arcy Thompson, and later by Charles Flahault in Montpellier, so that Smith became an outstanding teacher and researcher at a time of momentous developments in the natural sciences.     

Evolution of brain–body allometry in Lake Tanganyika cichlids

Brain size is strongly associated with body size in all vertebrates. This relationship has been hypothesized to be an important constraint on adaptive brain size evolution. The essential assumption behind this idea is that static (i.e., within species) brain–body allometry has low ability to evolve. However, recent studies have reported mixed support for this view. Here, we examine brain–body static allometry in Lake Tanganyika cichlids using a phylogenetic comparative framework. We found considerable variation in the static allometric intercept, which explained the majority of variation in absolute and relative brain size. In contrast, the slope of the brain–body static allometry had relatively low variation, which explained less variation in absolute and relative brain size compared to the intercept and body size. Further examination of the tempo and mode of evolution of static allometric parameters confirmed these observations. Moreover, the estimated evolutionary parameters indicate that the limited observed variation in the static allometric slope could be a result of strong stabilizing selection. Overall, our findings suggest that the brain–body static allometric slope may represent an evolutionary constraint in Lake Tanganyika cichlids.     

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

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

Analysing the allometry of multiple interacting traits

Since form and function are tightly integrated in plants, and since plant attributes often scale allometrically, it follows that plant allometry is inherently multivariate. Unfortunately, traditional statistical methods for studying allometric relationships are very restrictive and do not allow one to model multivariate allometric patterns that follow realistic biological hypotheses. In this paper I describe a new statistical test (‘d-sep test’) that allows one to test, and potentially falsify, alternative multivariate orderings of cause-and-effect in the context of allometry.     

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.     

Geometric morphometrics and leaf phenotypic plasticity: assessing fluctuating asymmetry and allometry in European white oaks (Quercus)

Because plants are unable to move away from unfavourable habitats and environmental perturbations, leaf phenotypic plasticity facilitates light absorption and gas exchange. Oaks (Quercus spp.) are particularly known for their adaptability and plastic phenotypes, and leaf allometry and developmental instability may represent important mechanisms for their adaptation to environments and evolution. Because of its important role in the adaptation of plant populations to different environments, allometry can be involved in diversifying selection. Developmental instability is related to environmental perturbations and stresses by producing random deviations in structures characterized by bilateral symmetry, such as oak leaves. In addition, developmental instability can also arise from genetic bottlenecks or as a result of hybridization. The splitting of symmetric and asymmetric components of variation and their separate analysis allows the variability in leaf shape traits to be summarized, reducing the variation produced by developmental instability. The geometric morphometric approach is a useful method for the study of leaf asymmetry and allometric patterns. This method provides an important tool for the visualization of shape attributes that characterize species with highly variable leaf phenotypic patterns. In this study, leaf shape and size variability of three white oak species was investigated by means of a two‐dimensional landmark‐based method providing improved knowledge of variance partitioning, species discrimination, fluctuating asymmetry and allometric patterns of variation resulting from the different analyses. © 2015 The Linnean Society of London, Botanical Journal of the Linnean Society, 2015, 179 , 335–348.     

Quantitative genetic variation in static allometry in the threespine stickleback

The common pattern of replicated evolution of a consistent shape-environment relationship might reflect selection acting in similar ways within each environment, but divergently among environments. However, phenotypic evolution depends on the availability of additive genetic variation as well as on the direction of selection, implicating a bias in the distribution of genetic variance as a potential contributor to replicated evolution. Allometry, the relationship between shape and size, is a potential source of genetic bias that is poorly understood. The threespine stickleback, Gasterosteus aculeatus, provides an ideal system for exploring the contribution of genetic variance in body shape allometry to evolutionary patterns. The stickleback system comprises marine populations that exhibit limited phenotypic variation, and young freshwater populations which, following independent colonization events, have often evolved similar phenotypes in similar environments. In particular, stickleback diversification has involved changes in both total body size and relative size of body regions (i.e., shape). In a laboratory-reared cohort derived from an oceanic Alaskan population that is phenotypically and genetically representative of the ancestor of the diverse freshwater populations in this region, we determined the phenotypic static allometry, and estimated the additive genetic variation about these population-level allometric functions. We detected significant allometry, with larger fish having relatively smaller heads, a longer base to their second dorsal fin, and longer, shallower caudal peduncles. There was additive genetic variance in body size and in size-independent body shape (i.e., allometric elevation), but typically not in allometric slopes. These results suggest that the parallel evolution of body shape in threespine stickleback is not likely to have been a correlated response to selection on body size, or vice versa. Although allometry is common in fishes, this study highlights the need for additional data on genetic variation in allometric functions to determine how allometry evolves and how it influences phenotypic evolution.     

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 development in larval Rana sylvatica (Anura: Ranidae): morphometric analysis of cranial allometry and ontogenetic shape change

This study provides baseline quantitative data on the morphological development of the chondrocranium in a larval anuran. Both linear and geometric morphometric methods are used to quantitatively analyze size-related shape change in a complete developmental series of larvae of the wood frog, Rana sylvatica. The null hypothesis of isometry was rejected in all geometric morphometric and most linear morphometric analyses. Reduced major axis regressions of 11 linear chondrocranial measurements on size indicate a mixture of allometric and isometric scaling. Measurements in the otic and oral regions tend to scale with negative allometry and those associated with the palatoquadrate and muscular process scale with isometry or positive allometry. Geometric morphometric analyses, based on a set of 11 chondrocranial landmarks, include linear regression of relative warp scores and multivariate regression of partial warp scores and uniform components on log centroid size. Body size explains about one-quarter to one-third of the total shape variation found in the sample. Areas of regional shape transformation (e.g., palatoquadrate, otic region, trabecular horns) are identified by thin-plate spline deformation grids and are concordant with linear morphometric results. Thus, the anuran chondrocranium is not a static structure during premetamorphic stages and allometric patterns generally follow scaling predictions for tetrapod cranial development. Potential implications regarding larval functional morphology, cranial development, and chondrocranial evolution in anurans are discussed.     

Modes of ontogenetic allometric shifts in crocodylian vertebrae

During postnatal ontogeny of vertebrates, allometric trends in certain morphological units or dimensions can shift drastically among isometry, positive allometry, and negative allometry. However, detailed patterns of allometric transitions in certain timings have not been explored well. Identifying the presence and nature of allometric shifts is essential for understanding the patterns of changes in relative size and shape and the proximal factors that are controlling these changes mechanistically. Allometric trends in 10 selected vertebrae (cervical 2–caudal 2) from hatchlings to very mature individuals of Alligator mississippiensis (Archosauria, Crocodylia) are reported in the present study. Allometric coefficients in 12 vertebral dimensions are calculated and compared relative to total body length, including centrum, neural spine, transverse process, zygapophysis, and neural pedicle. During the postnatal growth, positive allometry is the most common type of relative change (10 of the 12 dimensions), although the diameter of the neural canal shows a negative allometric trend. However, when using spurious breaks (i.e. allometric trends subdivided into growth stages using certain growth events, and key body sizes and/or ages), vertebral parts exhibit various pathways of allometric shifts. Based on allometric trends in three spurious breaks, separated by the end of endochondral ossification (body length: approximnately 0.9 m), sexual maturity (1.8 m), and the stoppage of body size increase (2.8 m), six types of ontogenetic allometric shifts are established. Allometric shifts exhibit a wide range from positive allometry restricted only in the early postnatal stage (Type I) to life‐long positive allometry (Type VI). This model of ontogenetic allometric shifts is then applied to interpret potential mechanisms (causes) of allometric changes, such as (1) growth itself (when allometric trend gradually decreases to isometric or negative allometric change: Type II–IV allometric shift); (2) developmental constraint (when positive allometry is limited only in the early growth stage: Type I allometric shift); and (3) functional or biomechanical drive (when positive allometry continues throughout ontogeny: Type VI allometric shift).     

Developmental constraints on the evolution of wing-body allometry in Manduca sexta

Artificial selection on body size in Manduca sexta produced genetic strains with large and small body sizes. The wing-body allometries of these strains differed significantly from the wild type. Selection on small body size led to a change in the scaling of wing and body size without changing the allometry: the wings were smaller relative to the body, but to the same degree at all body sizes. Selection for large body size led to a change in allometry with a decrease in the allometric coefficient, wing size becoming progressively smaller relative to body as body size increased. When larvae were deprived of food so as to produce adults of a range of small body sizes, all strains retained the same allometric coefficient but showed an increase in the scaling factor. Thus individuals starved as larvae had a smaller adult body size but had proportionally larger wings than fed individuals. We analyzed the developmental processes that could give rise to this pattern of allometries. Differences in the relative growth of body and wing disks can account for the differences in the allometric coefficients among the three body size strains. The change in wing-body allometry at large body sizes was primarily due to an insufficient time period for growth. The available time period for growth of the wing imaginal disks poses a significant constraint on the proportional growth of wings, and thus on the evolution of large body size.     

Weapon allometry varies with latitude in the New Zealand giraffe weevil

Animal body size commonly shows a relationship with latitude to the degree that this phenomenon is one of the few ‘rules’ discussed in evolutionary ecology: Bergmann's rule. Although exaggerated secondary sexual traits frequently exhibit interesting relationships with body size (allometries) and are expected to evolve rapidly in response to environmental variation, the way in which allometry might interact with latitude has not been addressed. We present data showing latitudinal variation in body size and weapon allometry for the New Zealand giraffe weevil (Lasiorhynchus barbicornis). Males display an extremely elongated rostrum used as a weapon during fights for access to females. Consistent with Bergmann's rule, mean body size increased with latitude. More interestingly, weapon allometry also varied with latitude, such that lower latitude populations exhibited steeper allometric slopes between weapon and body size. To our knowledge, this is the first study to document a latitudinal cline in weapon allometry and is therefore a novel contribution to the collective work on Bergmann's rule and secondary sexual trait variation.     

Models of ontogenetic allometry in cladoceran morphology studies

Ontogenetic variation of morphological traits in cladocerans is usually analysed by a simple allometry function. We found that common cyclomorphic and inducible traits in Bosmina and Daphnia sometimes deviate from simple allometry, however. Consequently, simple allometric analysis may at times be inadequate since important aspects of the ontogenetic development may not be revealed. We suggest that other allometric models should be used more extensively in ontogenetic studies of cladocerans morphology. Especially, complex allometric functions may help analyse the effects of size-selective predation on morphological defence traits when predators prefer prey of intermediate size. Guest editor: Piet Spaak Cladocera: Proceedings of the 7th International Symposium on Cladocera     

Tree height–diameter allometry across the United States

The relationship between tree height and diameter is fundamental in determining community and ecosystem structure as well as estimates of biomass and carbon storage. Yet our understanding of how tree allometry relates to climate and whole organismal function is limited. We used the Forest Inventory and Analysis National Program database to determine height–diameter allometries of 2,976,937 individuals of 293 tree species across the United States. The shape of the allometric relationship was determined by comparing linear and nonlinear functional forms. Mixed‐effects models were used to test for allometric differences due to climate and floristic (between angiosperms and gymnosperms) and functional groups (leaf habit and shade tolerance). Tree allometry significantly differed across the United States largely because of climate. Temperature, and to some extent precipitation, in part explained tree allometric variation. The magnitude of allometric variation due to climate, however, had a phylogenetic signal. Specifically, angiosperm allometry was more sensitive to differences in temperature compared to gymnosperms. Most notably, angiosperm height was more negatively influenced by increasing temperature variability, whereas gymnosperm height was negatively influenced by decreasing precipitation and increasing altitude. There was little evidence to suggest that shade tolerance influenced tree allometry except for very shade‐intolerant trees which were taller for any given diameter. Tree allometry is plastic rather than fixed and scaling parameters vary around predicted central tendencies. This allometric variation provides insight into life‐history strategies, phylogenetic history, and environmental limitations at biogeographical scales.     

Sexual selection,phenotypic variation,and allometry in genitalic and non‐genitalic traits in the sexually size‐dimorphic stick insect Micrarchus hystriculeus

The mobility hypothesis could explain the evolution of female‐biased size dimorphism if males with a smaller body size and longer legs have an advantage in scramble competition for mates. This hypothesis is tested by performing a selection analysis in the wild on Micrarchus hystriculeus (Westwood) (Phasmatodea), a sexually size dimorphic stick insect endemic to New Zealand. This analysis examined the form and strength of sexual selection on body size, leg lengths (front, mid and hind), and clasper size (a genitalic trait), and also quantified the degree of phenotypic variation and the allometric scaling pattern of these traits. By contrast to the mobility hypothesis, three lines of evidence were found to support significant stabilizing sexual selection on male hind leg length: a significant nonlinear selection gradient, negative static allometry, and a low degree of phenotypic variation. Hind leg length might be under stabilizing selection in males if having average‐sized legs facilitates female mounting or improves a male's ability to achieve the appropriate copulation position. As predicted, a negative allometric scaling pattern and low phenotypic variation of clasper size is suggestive of stabilizing selection and supports the ‘one‐size‐fits‐all’ hypothesis. Opposite to males, the mid and hind leg lengths of females showed positive static allometry. Relatively longer mid and hind leg lengths in larger females might benefit individuals via the better support of their larger abdomens. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 113 , 471–484.     

Do mating strategies determine genital allometry in African mole rats (Bathyergidae)?

Allometry describes the relationship of components of an organism with change in overall body size and has become the focus of numerous studies on the evolution of genitalia. Typically, negative allometry is observed in insects and is explained by stabilizing selection whereas the very few studies on mammals have shown a positive allometric relationship of genitalia in the body size, thought to have arisen as a result of sexual selection. However, all mammal species studied to date are thought to use mainly post-copulatory mating strategies. Across mammals, however, both pre-and post-copulatory strategies occur (although the two are not mutually exclusive). We propose that where pre-copulatory strategies are mainly used, no reproductive benefits would result from evolving positively allometric genitalia. As such, mammal genitalia are not typically positively allometric but rather allometry will, to a certain degree, be determined by mating strategy. We tested this prediction using four species of African mole rats (Bathyergidae) exhibiting variation in their life histories and mating strategies. Although generally supported, in that positive allometry did not occur in species that we assumed use mainly pre-mating strategies, positive allometry did not occur in either of the promiscuous species thought to use post-copulatory strategies. We suggest, therefore, that while mating strategies may tentatively determine genital allometry, whether positively allometric genitalia occur also depends on a number of complex interacting factors. In addition, this study provides further evidence and empirical support for the co-evolution of male and female genitalia in mammals.     

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.