Relative growth,ontogeny, and sexual dimorphism in gorilla(Gorilla gorilla gorilla and G. g. beringei): Evolutionary and ecological considerations

Gorillas are the largest and among the most sexually dimorphic of all extant primates. While gorillas have been incorporated in broad-level comparisons among large-bodied hominoids or in studies of the African apes, comparisons between gorilla subspecies have been rare. During the past decade, however, behavioral, morphological, and molecular data from a number of studies have indicated that the western lowland (Gorilla gorilla gorilla) and eastern mountain (Gorilla gorilla beringei) subspecies differ to a greater extent than has been previously believed. In this study I compare patterns of relative growth of the postcranial skeleton to evaluate whether differences between subspecies result from the differential extension of common patterns of relative growth. In addition, patterns of ontogeny and sexual dimorphism are also examined. Linear skeletal dimensions and skeletal weight were obtained for ontogenetic series of male and female G.g. gorilla (n = 315) and G.g. beringei (n = 38). Bivariate and multivariate methods of analysis were used to test for differences in patterns of relative growth, ontogeny, and sexual dimorphism between sexes of each subspecies and in same-sex comparisons between subspecies. Results indicate males and females of both subspecies are ontogenetically scaled for postcranial proportions and that females undergo an earlier skeletal growth spurt compared to males. However, results also indicate that the onset of the female growth spurt occurs at different dental stages in lowland and mountain gorillas and that mountain gorillas may be characterized by higher rates of growth. Finally, data demonstrate lowland and mountain gorilla females do not differ significantly in adult body size, but mountain gorilla males are significantly larger than lowland gorilla males, suggesting mountain gorillas are characterized by a higher degree of sexual dimorphism in body size. Thus, although lowland and mountain gorillas do not appear to have evolved novel adaptations of the postcranium which correlate with differences in locomotor behavior, the present investigation establishes subspecies differences in ontogeny and sexual dimorphism which may be linked with ecological variation. Specifically, these findings are evaluated in the context of risk aversion models which predict higher growth rates and increased levels of sexual dimorphism in extreme folivores. Am. J. Primatol. 43:1–31, 1997. © 1997 Wiley-Liss, Inc.     

Muscular function and skull growth in the laboratory rat (Rattus norvegicus)

Bilateral masseterectomy in newly-born rats results in a diminution in cranial weight and size. Such reduction affects the facial skeleton to a greater overall extent than the braincase, although in each region it is the dimensions of length that are affected to a greater extent that are those of height or width. Such contrasts are not dependent upon changes in body weight.
Removal of both temporal muscles—a smaller component of the masticatory musculature—results in little change in cranial proportions other than an increase in width of the braincase.
Such findings can be related, first, to contrasts in the timing of growth in the braincase and facial skeleton and, second, to the extent to which muscular function is reduced.     

A novel transgenic mouse model of fetal encephalization and craniofacial development

There are surprisingly few experimental models of neural growthand cranial integration. This, and the dearth of informationregarding fetal brain development, detracts from a mechanisticunderstanding of cranial integration and its relevance to theontogenetic and interspecific patterning of the form of theskull. To address this shortcoming, our research uses transgenicmice expressing a stabilized form of β-catenin to isolatethe effects of encephalization on the development of the basi-and neuro-cranium. These mice develop highly enlarged brainsdue to an increase in neural precursor cells, and differencesbetween transgenic and wild-type mice are predicted to resultsolely from variation in relative brain size. By focusing onprenatal growth, this project adds to our understanding of acritically important period when major structural and functionalinterrelationships are established in the skull. Comparisonsof wild-type and transgenic mice were performed using microcomputedtomography (microCT) and magnetic resonance imaging (MRI). Theseanalyses show that the larger brains of the transgenic miceare associated with a larger neurocranium and an altered basicranialmorphology. However, body size and postcranial ossificationdo not seem to be affected by the transgene. Comparisons ofthe rate of postcranial and cranial ossification also pointto an unexpected effect of neural growth on skull development:increased fetal encephalization may result in a compensatorydecrease in the level of cranial ossification. Therefore, ifother life-history factors are held constant, the ontogeny ofa metabolically costly structure, such as a brain, may occurat the expense of other cranial structures. These analyses indicatethe benefits of a multifactorial approach to cranial integrationusing a mouse model.     

Relative growth of the limbs and trunk in sifakas: Heterochronic,ecological, and functional considerations

Limb, trunk, and body weight measurements were obtained for growth series of Milne-Edwards's diademed sifaka, Propithecus diadema edwardsi, and the golden-crowned sifaka, Propithecus tattersalli. Similar measures were obtained also for primarily adults of two subspecies of the western sifaka: Propithecus verreauxi coquereli, Coquerel's sifaka, and Propithecus verreauxi verreauxi, Verreaux's sifaka. Ontogenetic series for the larger-bodied P. d. edwardsi and the smaller-bodied P. tattersalli were compared to evaluate whether species-level differences in body proportions result from the differential extension of common patterns of relative growth. In bivariate plots, both subspecies of P. verreauxi were included to examine whether these taxa also lie along a growth trajectory common to all sifakas. Analyses of the data indicate that postcranial proportions for sifakas are ontogenetically scaled, much as demonstrated previously with cranial dimensions for all three species (Ravosa, 1992). As such, P. d. edwardsi apparently develops larger overall size primarily by growing at a faster rate, but not for a longer duration of time, than P. tattersalli and P. verreauxi; this is similar to results based on cranial data. A consideration of Malagasy lemur ecology suggests that regional differences in forage quality and resource availability have strongly influenced the evolutionary development of body-size variation in sifakas. On one hand, the rainforest environment of P. d. edwardsi imposes greater selective pressures for larger body size than the dry-forest environment of P. tattersalli and P. v. coquereli, or the semi-arid climate of P. v. verreauxi. On the other hand, as progressively smaller-bodied adult sifakas are located in the east, west, and northwest, this apparently supports suggestions that adult body size is set by dry-season constraints on food quality and distribution (i. e., smaller taxa are located in more seasonal habitats such as the west and northeast). Moreover, the fact that body-size differentiation occurs primarily via differences in growth rate is also due apparently to differences in resource seasonality (and juvenile mortality risk in turn) between the eastern rainforest and the more temperate northeast and west. Most scaling coefficients for both arm and leg growth range from slight negative allometry to slight positive allometry. Given the low intermembral index for sifakas, which is also an adaptation for propulsive hindlimb-dominated jumping, this suggests that differences in adult limb proportions are largely set prenatally rather than being achieved via higher rates of postnatal hindlimb growth. Our analyses further indicate that the larger-bodied P. d. edwardsi has a higher adult intermembral index than P. tattersalli and P. verreauxi, thus supporting the allometric argument regarding the interspecific scaling of limb proportions in arboreal primates which employ vertical postures (Cartmill, 1974,1985; Jungers, 1978, 1985). Lastly, additional analyses indicate that P. d. edwardsi exhibits significant sexual dimorphism where adult females are larger than adult males in about one-third of all adult comparisons, whereas P. tattersalli exhibits significant sexual dimorphism in about one-fifth of all adult comparisons. Among western sifakas, adult P. v. coquereli exhibit significant sex dimorphism in about one-third of all comparisons, whereas adult P. v. uerreauxi show no significant differences between the sexes. Given that all taxa are ontogenetically scaled, this suggests that sexual dimorphism develops via such processes as well. Interestingly, our data indicate that sex dimorphism is allometric, with larger-bodied taxa like P. d. edwardsi being more dimorphic.     

Actions and interactions of growth hormone and insulin-like growth factor-II: body and organ growth of transgenic mice

To characterize long-term actions and interactions of growth hormone (GH) and insulin-like growth factor-II (IGF-II) on postnatal body and organ growth, hemizygous phosphoenolpyruvate carboxykinase (PEPCK)-human IGF-II transgenic mice were crossed with hemizygous PEPCK-bovine GH transgenic mice. The latter are characterized by two-fold increased serum levels of IGF-I and exhibit markedly increased body, skeletal and organ growth. Four different genetic groups were obtained: mice harbouring the IGF-II transgene (I), the bGH transgene (B), or both transgenes (IB), and non- transgenic controls (C). These groups of mice have previously been studied for circulating IGF-I levels (Wolf et al., 1995a), whereas the present study deals with body and organ growth. Growth curves (week 3 to 12) were estimated by regression with linear and quadratic components of age on body weight and exhibited significantly (p < 0.001) greater linear coefficients in B and IB than in I and C mice. The linear coefficients of male I and C mice were significantly (p < 0.001) greater than those of their female counterparts, whereas this sex-related difference was absent in the bGH transgenic groups. The weights of internal organs as well as the weights of abdominal fat, skin and carcass were recorded from 3.5- to 8- month-old mice. In addition, organ weight-to-body weight-ratios (relative organ weights) were calculated. Except for the weight of abdominal fat, absolute organ weights were as a rule significantly greater in B and IB than in I and C mice. IGF-II overproduction as a tendency increased the weights of kidneys, adrenal glands, pancreas and uterus both in the absence and presence of the bGH transgene. Analysis of relative organ weights demonstrated significant (p < 0.05) effects of elevated IGF- II on the relative growth of kidneys (males and females) and adrenal glands (females), confirming our previous report on organ growth of PEPCK-IGF-II transgenic mice. In females, IGF-II and GH overproduction were additive in stimulating the growth of spleen and uterus, providing evidence for tissue-specific postnatal growth promoting effects by IGF-II in the presence of elevated IGF-I     

Ontogenetic plasticity in nonhuman primates: I. Secular trends in the Cayo Santiago macaques

Although secular trends toward increasing body size are apparent in many human populations, little is known about their occurrence in nonhuman primates. The Cayo Santiago skeletal collection of Macaca mulatta includes 101 adult animals (greater than or equal to 10 years of age) born at different times in the past 3 1/2 decades, so that variation in size may be examined relative to birth year. No secular trends in orbital height were observed in this sample, but in both sexes lengths of adult long bones increased significantly over time, while cranial dimensions and length of the second molar in female also showed significant variation with birth year. These changes were consistent with the history of provisioning of the animals and with fluctuations in population size. Low-order correlations were observed between birth year and body proportions, especially the crural index in males, a pattern that has also been observed in human populations. These findings argue that, in addition to biomechanics and heritage, diet may affect allometric relationships and that an inherent plasticity or malleability of the growth process may be characteristic of nonhuman as well as human primates.     

Sequential changes in weight of the skeleton and in length of long limb bones of Macaca mulatta.

In a collection of 274 monkeys (Macaca mulatta) the relative weight of the dry, fat-free skeleton, expressed as a proportion of total body weight, increases significantly throughout the gestational period to approximately 6% with only random variation after birth. The weight of the fetal skeleton increases exponentially with age. In the postnatal period the skeletal weight increases asymptotically to adulthood, which is considered to be 6.5 years of age. Equations for estimating skeletal weight are presented. Of four subdivisions of the skeleton, the skul contributes the greatest proportion of total skeletal weight in the fetal stage with the proportion decreasing to adulthood. The contributions of the other subdivisions, postcranial axial, superior limb, and inferior limb, and inferior limb, are nearly equal in the fetal stage, with that of only the inferior limb increasing to adulthood, when it makes up the greatest proportion of total skeletal weight. Until the last third of the gestational period, the humerus is longer than the femur and the radius longer than the tibia. Thereafter, the inferior limbs grow at a faster rate than the superior limbs, resulting in an intermembral index of approximately 95% by birth and less than 90% by adulthood.     

Prediction of body weight of fossil Artiodactyla

Many dimensions of the postcranial skeleton of ruminant artiodactyls scale closely with body weight and are therefore potentially useful as predictors of body weight in fossil species. Using 45 dimensions of the skeleton a series of predictive equations was generated based on the scaling relationships of the family Bovidae. As a test of their usefulness these equations were used to predict body weights of a number of living ruminant artiodactyls, and six genera of fossil artiodactyls. For most species body weight estimates within 25° of actual weight were given by the mean of the predicted weights from all measurements except lengths of long bones. While femur length was a reasonable predictor of body weight, lengths of distal long bones were unreliable and should not be used as indicators of relative or absolute body weights. Some non-length measurements are biased in certain taxonomic groups; the possibility of erroneous estimates from such measurements can be reduced by using as many estimators of body weight as are available. No species of artiodactyl tested is so highly modified in all dimensions that all results were erroneous. Subsets of measurements which might be available from a typical fossil fragment also gave reliable results.     

Allometry and adaptation in the catarrhine postcranial skeleton

Seven measurements were taken on the postcranial skeleton of 249 specimens representing ten species of catarrhine primates and tested to determine their relationship with size. Size was measured as skeletal weight on each individual. It was found that the interspecific line based on the entire sample was in some cases determined not only by morphological adjustments for size variation but also by changes in locomotor adaptations of differently sized species within the sample. It is suggested that it is consequently preferable to study allometric relationships within a species or within a group of species that differ in size but are similar in their mode of locomotion. The allometric analysis reveals some interesting patterns within the data. Limb lengths scaled with either negative allometry or isometry over the entire sample. Within the species groups isometry was the rule except for pongid femurs, which showed negative scaling. Humerus length scaled at the same rate in pongids as in cercopithecoids but had a slightly higher intercept value. While colobines and cercopithecines scaled at similar rates for all seven dimensions, the colobine line was shifted to a position above that for cercopithecines in every case. It is suggested that this is a result of adaptation for leaping in the former group. Other implications of the allometric results are discussed.     

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.     

Human stanniocalcin-1 or -2 expressed in mice reduces bone size and severely inhibits cranial intramembranous bone growth

Stanniocalcin-1 (STC1) and -2 (STC2) are highly related, secreted, homodimeric glycoproteins that are significantly upregulated by different forms of stress including high phosphate levels. Transgenic mice that constitutively express either human STC1 or STC2 exhibit intra-uterine growth restriction and permanent post-natal growth retardation. STC1 is expressed in chondrocytic and osteoblastic cells during murine development and can enhance differentiation of calvarial cells in culture. Therefore, there is mounting evidence that stanniocalcins (STCs) modulate bone development in vivo. To further define the effects of stanniocalcins on skeletal development, we performed a series of measurements on components of the axial, appendicular, and cranial skeleton in transgenic and wildtype mice. We show that skeletal growth is retarded and that the intramembranous bones of the cranium exhibit a particularly severe delay in suture closure. The posterior frontal suture remains patent throughout the lifetime of human STC1 and STC2 transgenic mice. We did not observe significant effects on chondrogenesis: however, calvarial cells exhibited reduced viability, proliferation and delayed differentiation, indicating that developing osteoblasts are particularly sensitive to the levels of STCs. Given the evidence linking STC1 to cellular phosphate homeostasis, we assessed the expression of a variety of phosphate regulators in transgenic and wildtype calvarial cells and found significantly lower levels of Mepe, Dmp1, Sfrp4 in transgenic cells without a change in Pit1 or Pit2. Collectively these data support a direct regulatory role for STCs in osteoblasts and suggest that overexposure to these factors inhibits normal skeletal development without significant changes in patterning.     

Allometry and adaptation of body proportions and stature in African pygmies

We have analyzed the growth allometry of external body proportions in Efe pygmies from Zaire and combined these data with values from the literature for comparable dimensions in adult pygmies and nonpygmies. We sequentially tested the hypotheses that adult proportion differences between 1) male vs. female Efe, and 2) pygmies vs. nonpygmies result from ontogenetic scaling, or the differential extension of common patterns of growth allometry. Results indicate an almost complete concordance of allometric trajectories for male and female Efe. These preliminary analyses also strongly suggest that adult nonpygmy Africans generally differ from pygmies in their terminal size and correlated allometric consequences, rather than in more fundamental alterations of underlying patterns of growth. Biacromial diameter emerges as the measurement most likely to depart from this general pattern. These results provide further evidence that shifts in systemic growth hormones yielding differences in terminal overall body size may be accompanied by global and coordinated allometric transformations. Certain proportion differences previously interpreted by some as specific evidence of primitive retention in pygmies in fact reflect simple growth allometric correlates of the derived rapid size decrease in these groups. Selected divergent body proportions characterizing adult pygmies, previously interpreted by some as independent evidence of climatic adaptation, also reflect such allometric correlates of ontogenetic scaling. We critically assess arguments that the small overall body size of pygmies was specifically selected for reasons of thermoregulatory efficiency, and consider an alternative or complementary scenario, based on selection for small size in order to reduce caloric requirements. © 1996 Wiley-Liss, Inc.     

Muscle-bone relationships in mice selected for different body conformations

Some muscle-bone relationships were studied in terms of gastrocnemius muscle weight, femur and tibia length and femur and tibia weight in four lines of mice (CBi-, CBi+, CBi/L and CBi/C) artificially selected for different body conformations and in the unselected control line (CBi). CBi- (low body weight--short tail) and CBi+ (high body weight--long tail) lines were divergently selected following the positive genetic correlation between body weight and tail (skeleton) length (agonistic selection). In contrast, CBi/L (low body weight--long tail) and CBi/C (high body weight--short tail) were also divergently selected but against the aforementioned correlation (antagonistic selection). The relationship between bone length and muscle weight was interpreted based on the assumption that the increased tension generated by the longitudinal growth of a bone, brings about an increase in the mass of the muscles attached to it. All CBi+, CBi/C and CBi/L mice showed enlarged femurs and tibias, but only those genotypes simultaneously selected for high body weight (CBi+ and CBi/C) showed heavier muscles than controls. The CBi+ and CBi- genotypes with agonistic selection differ in bone length and muscle weight, as it would be expected of the allometric modification of their body conformation, showing the associated longitudinal bone growth-muscle growth. CBi/C and CBi/L mice, with a non-allometric modification of body conformation, exhibited the same bone length but different muscle weight. Consequently, the antagonistic criterion allowed to confirm that the genetic influence on of the proposed muscle-bone relationships could be modified, thus making it possible to lengthen the bone through selection of a long skeleton and to avoid the correlated effect on muscle mass, by selecting for a low body weight, bringing forth presumptive evidence that both processes were genetically independent.     

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

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

Relative growth of the limbs and trunk in the African apes

Examination of relative growth and allometry is important for our understanding of the African apes, as they represent a closely related group of species of increasing body size. This study presents a comparison of ontogenetic relative growth patterns of some postcranial dimensions in Pan paniscus, Pantroglodytes, and Gorilla gorilla. Interspecific proportion differences among the three species are also analyzed. It is stressed that reliable ontogenetic information can only be obtained if subadults are examined-growth data cannot be inferred from static adult scaling. Results indicate that some postcranial relative growth patterns are very similar in the three species, suggesting differential extrapolation of a common growth pattern, whereas for other proportion comparisons the growth trends differ markedly among the species, producing distinct shape differences in the adults Interspecific shape changes among the three species are characterized by positive allometry of chest girth and negative allometry of body height and leg length. It is suggested that relative decrease of leg length with increasing body size among the African pongids might be expected on biomechanical grounds, in order to maintain similar locomotor abilities of climbing arborealism and quadrupedal terrestrialism. Relative to body weight or trunk length, the limbs of the bonobo (Pan paniscus) are longer than in the common chimpanzee or the gorilla, with a lower intermembral index. This may most closely resemble the primitive condition for the African apes.     

Allometry of the postnatal cranial ontogeny and sexual dimorphism in Otaria byronia (Otariidae)

We studied the cranial postnatal ontogeny of Otaria byronia in order to detect sexual dimorphism in allometric terms, analyzing the rate of growth of functional variables linked to specific capacities as bite and head movements. We used 20 linear measurements to estimate allometric growth applying bivariate and multivariate analyses in females and males separately. Males were also analyzed in two partitioned subsets considering non-adult and adult stages, when the dimorphism is accentuated in order to reach optimal performance for intra-sexual competition. In the comparison of the employed techniques, we detected an empirical relationship between our multivariate results and the ordinary least square bivariate analysis. The quantitative analyses revealed different ontogenetic trajectories between non-adult and adult males in most variables, suggesting that the adult skull is not a scaled version of subadult skull. For instance, variables related with longitudinal dimensions decreased their allometric coefficients when the adult stage was reached, whereas those related with breadth or vertical dimensions increased their values. In adult males this could indicate that skull breadth and height are more important than longitudinal growth, relative to overall skull size. Conversely, inter-sexual comparisons showed that females and non-adult males shared similar ontogenetic growth trends, including more allometric trends than did males along their own ontogenetic trajectory. In general, adult males exhibited higher allometric coefficients than non-adult males in variables associated with bite and sexual behavior, whereas in comparison to females the latter showed higher coefficients values in these variables. Such patterns indicate a complex mode of growth in males beyond the growth extension, and are in partial agreement with changes previously reported for this and other species in the family Otariidae.     

Scaling of lumbar vertebrae in anthropoids and implications for evolution of the hominoid axial skeleton

We investigated allometric relationships between vertebral centrum cranial surface areas and body weight and skeletal lumbar length in extant platyrrhine and cercopithecid species. Platyrrhines have smaller lumbar vertebral centra regarding the cranial surface area relative to their body weight than extant catarrhines. However, the stress to the spine of quadrupeds is not only influenced by the body weight but also its length, which contributes to the amount of bending moment. Our results indicated that platyrrhines and cercopithecids have similar lumbar vertebral centrum surface areas when they are scaled on the product of the body weight and skeletal lumbar length. Platyrrhines generally tend to have relatively short lumbar columns for a given body weight. As a result of this tendency, their vertebral centra appear relatively small if only body weight is taken into account. The centrum surface area is rather constant relative to the product of the body weight and skeletal lumbar length within platyrrhines or cercopithecids, despite the fact that skeletal lumbar length is in itself rather variable relative to body weight. This result indicates that the vertebral centrum articular area, the lumbar column length and the body weight are strongly correlated with each other and that such relationships are similar between platyrrhines and cercopithecids. These relationships were observed using both the zygapophyseal and rib definitions of the lumbar vertebrae. However, they were more clearly observed when the zygapophyseal definition was adopted. It appeared that lumbar vertebrae of Proconsul nyanzae (KNM−MW 13142) had distinctively smaller surface areas relative to its body weight and lumbar length than for platyrrhines and cercopithecids, differing from extant hominoids, which have comparatively larger lumbar vertebrae. In the case of Morotopithecus, the lumbar vertebral surface area seems to be as large as in extant platyrrhines and cercopithecids if it had a reduced number of lumbar vertebrae. It is uncertain whether its lumbar vertebral surface area was as large as in extant hominoids. Electronic Publication