Brian T. Shea

Ontogenetic approaches to sexual dimorphism in anthropoids

Studies of sexual dimorphism have traditionally focused on the static differences in size and shape between adult males and females. In this paper, I suggest that an investigation of the ontogenetic bases of sexual dimorphism can provide new insights and information unobtainable from studies concerned only with adult endpoints. While growth is often viewed as simply the developmental pathway utilized to attain final adult size and shape, we must recognize that it is the entire pattern of sex-differentiated growth, and not merely the adult endpoints, which is adaptive and the target of natural selection. The importance of an ontogenetic approach to the analysis of sexual dimorphism is also demonstrated by the fact that a given morphologicalresult (e.g., a certain degree of adult weight dimorphism) may be attained by very different developmentalprocesses, signalling selection for quite different factors. The need to analyze the ontogenetic bases of sexual dimorphism in size and shape has recently been recognized by Jarman, in his study of dimorphism in large terrestrial herbivores. Here I combine aspects of Jarman’s approach with those of allometry and heterochrony in an analysis of sexual dimorphism in selected anthropoid primates. It is demonstrated that although all dimorphic anthropoids appear to be characterized by somebimaturism, the degree varies significantly. Marked weight dimorphism in certain species is primarily produced by an increased differentiation of female and male growthrates, while in other species the primary change involves differences in thetime or duration of growth between the sexes. These variations are illustrated with anthropoid genera such asMiopithecus, Cercopithecus, Erythrocebus, Macaca, Papio, Pan, andGorilla. It is suggested that additional ontogenetic investigations of other anthropoids will help clarify some of the socioecological bases of this variation in the ways of attaining an adult dimorphic state. This will contribute to our understanding of the complex factors underlying and producing sexual dimorphism in primates and other mammals.

Size and Diet in the Evolution of African Ape Craniodental Form

Interspecific differences in craniodental morphology among Pan paniscus, Pan troglodytes, and Gorilla gorilla are analyzed. These apes differ in both diet and body size, and thus present an excellent example in which to apply an allometric criterion of subtraction in order to determine morphological differences which might be related to divergent dietary specialization. The use of ontogenetic allometry in particular as a criterion of subtraction is discussed. Bivariate and multivariate results indicate that most of the variation in skull form among the species relates to the extension of a common growth trend to different sizes. Comparative analysis of growth trajectories reveals a number of differences, but none that appear to relate to a reorganization of skull proportions which might correspond to a dietary shift towards increased folivory. The dentition clearly exhibits non-allometric shape changes corresponding to the dietary differences, however. The meaning of these differences between cranial and dental patterns is discussed.

An Allometric Perspective on the Morphological and Evolutionary Relationships between Pygmy (Pan Paniscus) and Common (Pan troglodytes) Chimpanzees

The pygmy chimpanzee (Pan paniscus), or bonobo, has been the object of considerable primatological interest since its “discovery” in the late 1920s and early 1930s. Because pygmy and common chimpanzees differ in average adult size (although the amount of difference and degree of overlap are debatable), many have suggested that morphological differences between the species may be size-related, or allometric. For example, Corruccini and McHenry (1979) and McHenry and Corruccini, (1981) analyzed the cranium, postcranium, and dentition of P. paniscus and P. troglodytes, and concluded that many of the shape differences between the two species are due to allometry. Horn (1979) has made a similar suggestion. By contrast, Zihlman and others (e.g., Zihlman and Cramer, 1978; Zihlman et al., 1978; Zihlman, 1979, 1981) have argued that allometry cannot be invoked to explain the morphological differences between the chimpanzee species. In fact, Zihlman (1981, p. 6) suggests that we might view allometry as a “favorite anatomical fudge factor” which has obscured our understanding of the two chimpanzee species. In this paper and in other works (Shea, 1981a, 1982, 1983a-d; Coolidge and Shea, 1982), I have also analyzed the morphological differences between the chimpanzee species (and among the African pongids as a group) from an allometric perspective.

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 derive 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.

Heterochrony in Primates

Until recently the study of heterochrony in primate evolution has focused primarily on arguments concerning human neoteny. Swiss zoologist Julius Kollman (1905), who introduced the term neoteny in the late 1800s, suggested that early humans could be traced to pygmy groups that had developed from anthropoid apes via juvenilization and neoteny. De Beer (1930), building on Bolk’s (1926, 1929) important work, made human evolution one of the central examples in his classic work Embryology and Evolution, which established the study of heterochrony within the modern synthesis. Continued emphasis is evidenced in the work of Abbie (1952, 1958, 1964), Montagu (1962, 1981), and Gould (1977).

Bonobos: Generalized Hominid Prototypes or Specialized Insular Dwarfs? [and Comments and Replies]

Neontological, biochemical, and paleontological data indicate that the bonobo, Pan paniscus, is a specialized form that possesses relatively small teeth, is quadrupedally adapted, and is only minimally sexually dimorphic. The various specializations of bonobos could be adaptations to ecological restrictions encountered in the terrestrial island of tropical forest that comprises their home range. Bonobos possess specializations quite different from those present in either Miocene apes or the earliest known hominids and should not be considered as suitable living models of the primitive hominoid or hominid condition.

Unfinished business: Mahalanobis and a clockwork orang

Abstract Skulls of orang-utan and chimpanzee were studied by multivariate analysis, keeping the sexes separate. Skulls of Pongo pygmaeus from south-western Borneo were found to be as distinct from skulls from the remainder of Borneo as were those from Sumatra. Although Pan paniscus separated well from other chimpanzees, the conventionally recognised subspecies of Pan troglodytes did not separate well; localised samples within the conventional subspecies proved in some cases to be at least as distinctive. This emphasises that “accepted” taxonomy must in no case be taken as given, but must be subject to continual testing.

Ontogenetic Allometry and Scaling

The two great syntheses that established the study of allometry were D’Arcy Thompson’s (1917, 1942, 1961) On Growth and Form and Julian Huxley’s (1932) Problems of Relative Growth. The bulk of Thompson’s volume dealt with the mechanical and physical factors underlying shape transformation. In his chapter entitled “The rate of growth, ” however, Thompson (1942, p. 79) stressed that “the form of an organism is determined by its rate of growth in various directions; hence rate of growth deserves to be studied as a necessary preliminary to the theoretical study of form.” Huxley’s (1932) work built on Thompson’s foundation through extensive empirical and theoretical investigations of relative, or differential, growth in organisms. Huxley showed that a simple power function, Y = bX k , could often describe correlated changes between growing parts (X and Y) of the body. He also analyzed ontogenetic allometry (relative growth, or heterogony, as Huxley labeled it) in terms of growth gradients, taxonomy, genetics, and evolutionary transformations. Huxley’s approach to the study of size and shape, there fore, was explicitly rooted in the analysis of growing form; we often term this growth allometry, in order to distinguish it from size allometry, which focuses on allometric changes in static adult series (Simpson, et al., 1960).

Phyletic size change and brain/body allometry: A consideration based on the African pongids and other primates

A problematic aspect of brain/body allometry is the frequency of interspecific series which exhibit allometry coefficients of approximately 0.33. This coefficient is significantly lower than the 0.66 value which is usually taken to be the interspecific norm. A number of explanations have been forwarded to account for this finding. These include (1) intraspecificallometry explanations, (2) nonallometric explanations, and (3) Jerison’s “extraneurons” hypothesis, among others. The African apes, which exhibit a lowered interspecific allometry coefficient, are used here to consider previous explanations. These are found to be inadequate in a number of ways, and an alternative explanation is proposed. This explanation is based on patterns of brain and body size change during ontogeny and phytogeny. It is argued that the interspecific allometry coefficient in African apes parallels the intraspecific one because similar ontogenetic modifications of body growth separate large and small forms along each curve. In both cases, body size differences are produced primarily by growth in later postnatal periods, during which little brain growth occurs. Data on body growth, neonatal scaling, and various lifehistory traits support this explanation. This work extends previous warnings that sizecorrected estimates of relative brain size may not correspond very closely to our understanding of the behavioral capacities of certain species in lineages characterized by rapid change in body size.

Ontogenetic scaling of skeletal proportions in the talapoin monkey

The talapoin monkey is distinct from its close relatives in the genus Cercopithecus in a variety of morphological and ecological features, inclining some to place it in its own genus, Miopithecus . It is also the smallest of the extant catarrhines, and in this investigation the extent to which the morphological distinctions of the talapoin monkey are the result of allometric factors is analysed. A series of cranial and postcranial measurements were taken on the skeletons of young and adult talapoin monkeys ( C. talapoin ) and moustached monkeys ( C. cephus ). Ontogenetic scaling (i.e., allometric extrapolation) was utilized as a criterion of substraction in both bivariate and multivariate comparative allometric analysis. Adult cranial and postcranial proportions do differ significantly between C. talapoin and C. cephus , but in almost all cases these adult shape differences result from the sharing of common underlying patterns of ontogenetic allometry. Use of additional data from Verheyens (1962) monograph suggests that the marked differences in skull form within the Cercopithecus group (from talapoin to patas monkeys) may also be primarily a product of ontogenetic scaling. The specific postcranial proportions seen in adult talapoins do not accord with expectations derived from several recent biomechanical models for primates which engage in frequent leaping and climbing behaviors, though the comparative growth allometric perspective utilized here does clarify these adult shape differences. The predominantly paedomorphic morphology of the talapoin monkey appears to be a direct and correlated allometric consequence of a decrease in overall growth rates and terminal body size, which may be related to increased propensities for leaping behavior and a more insectivorous diet.