Evolution of human growth

The human pattern of growth and development (ontogeny) appears to differ markedly from patterns of ontogeny in other primate species. Humans present complex and sinuous growth curves for both body mass and stature. Many human proportions change dramatically during ontogeny, as we reach sizes that are among the largest of living primates. Perhaps most obviously, humans grow for a long time, with the interval between birth and maturation exceeding that of all other primate species. These ontogenetic traits are as distinctive as other key derived human traits, such as a large brain and language. Ontogenetic adaptations are also linked to human social organization, particularly by necessitating high levels of parental investment during the first several years of life.     

LIFE HISTORY VARIATION IN PRIMATES

Extensive variation in life-history patterns is documented across primate species. Variables included are gestation length, neonatal weight, litter size, age at weaning, age at sexual maturity, age at first breeding, longevity, and length of the estrous cycle. Species within genera and genera within subfamilies tend to be very similar on most measures, and about 85% of the variation remains when the subfamily is used as the level for statistical analysis. Variation in most life-history measures is highly correlated with variation in body size, and differences in body size are associated with differences in behavior and ecology. Allometric relationships between life-history variables and adult body weight are described; subfamily deviations from best-fit lines do not reveal strong correlations with behavior or ecology. However, for their body size, some subfamilies show consistently fast development across life-history stages while others are characteristically slow. One exception to the tendency for relative values to be positively correlated is brain growth: those primates with relatively large brains at birth have relatively less postnatal brain growth. Humans are a notable exception, with large brains at birth and high postnatal brain growth.     

Homoplasy and the evolution of ontogeny in papionin primates

Recent advances in developmental biology reveal that patterns of morphological development, even during early phases, may be highly susceptible to evolutionary change. Consequently, developmental data may be uninformative with regard to distinguishing homology and homoplasy. The present analysis evaluates postnatal ontogeny in papionin primates to test hypotheses about homology and homoplasy during later periods of development. Specifically, the analysis studies the allometric bases of craniometric resemblances among four papionin genera to test the hypothesis that homoplasy in adult cranial form, particularly of baboons (Papio) and mandrills (Mandrillus), is underwritten by divergent patterns of development. Bivariate and multivariate allometric analyses demonstrate that the developmental patterns in Papio baboons diverge markedly from ontogenetic allometric trajectories in other papionin species. The resemblances between Papio and Mandrillus (assuming that patterns of development in smaller papionins are ancestral) are largely consequences of perinatal increases in relative brain size in juvenile Papio. Postnatal growth to large size and strong negative allometry of neurocranial form results in shape similarities because developmental pathways for large papionin genera intersect. Analyses show that allometric data may not be particularly informative in revealing homoplasy. However, placed into proper phylogenetic context, such data illustrate derived patterns of development that may reflect critically important life-history or ontogenetic adaptations.     

Newborn: Adult brain ratios in hominid evolution

The ratio of newborn to adult brain size varies widely in primates. These variations provide an index of the different degrees of postnatal brain growth in the different members of the primate order. The uniquely low figure for Homo sapiens indicates a greater degree of postnatal brain growth and therefore postnatal dependence and also a greater need and opportunity for social organisation. An attempt is made to determine the newborn:adult brain ratio in a proto-human population, Australopithecus africanus. Two possible causes of the reduction of the ratio in hominid evolution are discussed. The first is the limiting confines of the maternal pelvis adapted primarily for orthograde progression rather than parturition. The second concerns the resultant of a set of three paired variables between the members of each pair of which there exists an allometric relationship. These are the relation between brain and body size in the adult, feto-maternal weight allometry and the relation between newborn brain-size and birth weight.     

Evolution of human growth prolongation

This investigation evaluates hypotheses that seek to explain temporal retardation or prolongation of human ontogeny. Current hypotheses that address this issue are poorly defined and conflate several distinct theoretical positions. A model that predicts homogeneity in the extension of human growth periods is evaluated. This model is contrasted with two alternatives. The first alternative predicts heterogeneity in the extension of human growth periods. The second anticipates that human growth prolongation is the result of the uniquely derived “insertion” of a human childhood period into an ancestral ontogenetic trajectory. Allometric analyses of body mass growth data from 21 species of anthropoid primates suggest that human female and male ontogenies often depart from patterns established by other primates, but these departures are not uniformly exceptional. Comparisons imply that derived changes in human growth are heterogeneous. Relative to interspecific expectations, early growth periods are much prolonged, but later growth periods are actually reduced. Moreover, the attributes of early growth periods, including growth rates, timing of growth events, and size-for-age, are highly variable across primates. Low correlations among growth periods suggest independence among growth phases. These analyses highlight minimal distinctions between competing models (heterogeneous extension and insertion hypotheses) that attempt to explain human growth prolongation. More important, the present study facilitates refinements of causal models that have been proposed to explain human growth prolongation. Specifically, human growth prolongation may be related to derived changes in patterns of brain development. Alternatively, metabolic factors may have exerted influences on human ontogeny. However, models that predict long growth periods as a byproduct of metabolic factors do not adequately explain temporal retardation of human ontogeny. Am J Phys Anthropol 107:331–350, 1998. © 1998 Wiley-Liss, Inc.     

Brain Size Growth and Life History in Human Evolution

Increases in endocranial volume (a measure of brain size) play a major role in human evolution. Despite the importance of brain size increase, the developmental bases of human brain size evolution remain poorly characterized. Comparative analyses of endocranial volume size growth illustrate that distinctions between humans and other primates are consequences of differences in rates of brain size growth, with little evidence for differences in growth duration. Evaluation of available juvenile fossils shows that earliest hominins do not differ perceptibly from chimpanzees (Pan). However, rapid and human-like early brain growth apparently characterized Homo erectus at about 1?Ma before present. Neandertals show patterns of brain growth consistent with modern humans during infancy, but reach larger sizes than modern humans as a result of differences in later growth. Growth analyses reveal commonalities in patterns of early brain size growth during the last million years human evolution, despite major increases in adult size. This result implies consistency across hominins in terms of maternal metabolic costs of infancy. Continued size growth past infancy in Neandertals and modern humans, when compared to earlier hominins, may have cognitive implications. Differences between Neandertals and modern humans are implied, but difficult to define with certainty.     

Socioecology and the ontogeny of sexual size dimorphism in anthropoid primates

This study examines statistical correlations between socioecological variables (including measures of group composition, intermale competition, and habitat preference) and the ontogeny of body size sexual dimorphism in anthropoid primates. A regression-based multivariate measure of dimorphism in body weight ontogeny is derived from a sample of 37 species. Quantitative estimates of covariation between socioecological variables and this multivariate measure are evaluated. Statistically significant covariation between the ontogeny of dimorphism and socioecological variables, with the possible exception of habitat preference, is observed. Sex differences in ontogeny are lacking in species that exhibit low levels of intermale competition and are classifiable as species with monogamous/polyandrous mating systems. Among dimorphic species, two modes of dimorphic growth are apparent, which seem to be related to different kinds of group compositions. Multimale/multifemale species tend to become dimorphic through bimaturism (sex differences in duration of growth) with minimal sex differences in growth rate. Single-male/multifemale species tend to attain dimorphism through differences in rate of growth, often with limited bimaturism. Measures of intermale competition may also covary with these modes of dimorphic growth, but the relations among these variables are sometimes ambiguous. Correlations between dimorphic growth and behavioral variables may reflect alternative life history strategies in primates. Specifically, the ways in which risks faced by subadult males are distributed and the relations of these risks to growth rates seem to influence the evolution of size ontogenies. The absence of dimorphic ontogeny in some species can be tied to similar distributions of risk in each sex. In taxa that become dimorphic primarily through rate differences in growth, the lifetime distribution of risks for males may change rapidly. In contrast, males may face a pattern of uniformly changing or stable risk in species that become dimorphic through bimaturism. Finally, much variation recorded by this study remains unexplained, providing additional evidence of the need to specially examine female ontogeny before primate body size dimorphism can be satisfactorily explained. © 1995 Wiley-Liss, Inc.     

Comparative Perspectives on Bimaturism, Ontogeny, and Dimorphism in Lemurid Primates

We address questions regarding the general absence of dimorphism in lemurid primates (Hapalemur, Eulemur, and Varecia) through comparative analyses of ontogeny. We described and analyzed body mass growth data for 9 lemurid taxa and compared them to similar data for anthropoid primates. Lemurids tend to grow rapidly over a short period of time when compared to anthropoid primates of similar body sizes. Size variation among lemurid taxa arises primarily as a consequence of differences in rates of growth. Comparative analyses of body mass growth data suggest that natural selection has produced ontogenetic adaptations in lemurids that center on relatively short periods of growth. Reduced growth periods preclude the evolution of sexual dimorphism through bimaturism—a sex difference in the length of the growth period—despite high levels of intermale competition. Selective factors related to seasonal variability of lemurid habitats play important roles in limiting the potential for the evolution of bimaturism. Other selective factors that limit bimaturism are related to female reproductive synchrony. In combination, they favor relatively early male maturation, precluding sexual selection that would otherwise promote the evolution of dimorphism through bimaturism. Natural selection on growth rates may preclude somatic responses to sexual selection that involve elevated male growth rates. In general, existing ontogenetic or life history adaptations appear to restrict responses to sexual selection in male lemurids.     

Human encephalization and developmental timing

Human evolution is frequently analyzed in the light of changes in developmental timing. Encephalization in particular has been frequently linked to the slow pace of development in Homo sapiens. The "brain allometry extension" theory postulates that the progressive extension of a conserved primate brain allometry into postnatal life was the basis for brain enlargement in the human lineage. This study shows that published primate and human growth data do not corroborate this model. Instead, the unique encephalization of H. sapiens is alternatively described as the result of evolutionary changes in three aspects of developmental timing. The first is a moderate extension in the duration of brain growth relative to our closest extant relatives, contrary to the view that human brain growth is drastically prolonged into postnatal life. Second, humans evolved a derived brain allometry in comparison with chimpanzees and early hominins. Third, humans (and other anthropoid primates to a lesser degree) display a significant retardation in early postnatal body growth in comparison with other mammals, which directly affects adult encephalization in our species. The rejection of the "brain allometry extension" model may require a reevaluation of the adaptive scenarios proposed to explain how human encephalization evolved.     

Bone Growth Dynamics of the Facial Skeleton and Mandible in <Emphasis Type="Italic">Gorilla gorilla</Emphasis> and <Emphasis Type="Italic">Pan troglodytes</Emphasis>

Adult craniofacial morphology results from complex processes that involve growth by bone modelling and interactions of skeletal components to keep a functional and structural balance. Previous analyses of growth dynamics in humans revealed critical changes during late ontogeny explaining particular morphological features in our species. Data on bone modelling patterns from other primate species could help us to determine whether postnatal changes in the growth dynamics of the craniofacial complex are human specific or are shared with other primates. However, characterizations of bone modelling patterns through ontogeny in non-human hominids are scarce and restricted to isolated data on facial and mandibular regions. In the present study, we analyse the bone modelling patterns in an ontogenetic series of Pan and Gorilla to infer the growth dynamics of their craniofacial complex during postnatal development. Our results show that both Pan troglodytes and Gorilla gorilla are characterized by species-specific bone modelling patterns indicative of a mainly forward growth direction during postnatal development. Both species show minor but consistent ontogenetic changes in the distribution of bone modelling fields in specific regions of the face and mandible, in contrast to other regions which show more constant bone modelling patterns. In addition, we carry out a preliminary integrative study merging histological and geometric morphometric data. Both approaches yield highly complementary data, each analysis providing details on specific growth dynamics unavailable to the other. Moreover, geometric morphometric data show that ontogenetic variation in the modelling pattern of the mandibular ramus may be linked to sexual dimorphism.     

Understanding primate brain evolution

We present a detailed reanalysis of the comparative brain data for primates, and develop a model using path analysis that seeks to present the coevolution of primate brain (neocortex) and sociality within a broader ecological and life-history framework. We show that body size, basal metabolic rate and life history act as constraints on brain evolution and through this influence the coevolution of neocortex size and group size. However, they do not determine either of these variables, which appear to be locked in a tight coevolutionary system. We show that, within primates, this relationship is specific to the neocortex. Nonetheless, there are important constraints on brain evolution; we use path analysis to show that, in order to evolve a large neocortex, a species must first evolve a large brain to support that neocortex and this in turn requires adjustments in diet (to provide the energy needed) and life history (to allow sufficient time both for brain growth and for 'software' programming). We review a wider literature demonstrating a tight coevolutionary relationship between brain size and sociality in a range of mammalian taxa, but emphasize that the social brain hypothesis is not about the relationship between brain/neocortex size and group size per se; rather, it is about social complexity and we adduce evidence to support this. Finally, we consider the wider issue of how mammalian (and primate) brains evolve in order to localize the social effects.     

Developmental variation in salmonid populations

Salmonid life-history patterns vary within and between species, and within and between populations. Two major developmental conversions ( sensu Smith-Gill) occur in the life of salmonids: smolting, in which freshwater adaptations are exchanged for marine ones; and sexual maturation. Each process is circannual, endogenously rhythmic but synchronized by photoperiod. Each involves a choice of developmental route, whose direction depends on the individual's responses to prior feeding opportunity, and its current metabolic performance. Data are presented from laboratory and farm experiments on Atlantic salmon, Salmo salar L., designed to test this developmental model. The findings are used to interpret variation in these developmental characteristics, and their consequences for life-history patterns, evident over the geographical range of Atlantic salmon and other salmonids.     

Why do female primates have such long lifespans and so few babies? or Life in the slow lane

A major goal of life history studies is to identify and explain features of the life history of individual species that follow broad rules across many groups of organisms, features that are characteristic of particular phylogenetic lineages, and features that are specific adaptations, to local ecological situations. In recent years we have developed a general theory of life history that interrelates many aspects of ontogeny and reproduction across a wide range of organisms. Contrasted to most other mammals, primates have long average adult lifespans and few babies per year for their adult body size. This new theory suggests that these aspects of life history follow directly from the fact that primates have slow individual growth rates. This slow growth rate is thus the basic phenomenon that needs explanation to understand primate slowness.     

Ontogeny and diachronic changes in sexual dimorphism in the craniofacial skeleton of rhesus macaques from Cayo Santiago, Puerto Rico

Insight into the ontogeny of sexual dimorphism is important to our understanding of life history, ecology, and evolution in primates. This study applied a three-dimensional method, Euclidean Distance Matrix Analysis, to investigate sexual dimorphism and its diachronic changes in rhesus macaque (Macaca mulatta) skulls. Twenty-one landmarks in four functional areas of the craniofacial skeleton were digitized from macaques of known age and sex from the Cayo Santiago collections. Then, a series of mean form matrices, form difference matrices, and growth matrices were computed to demonstrate growth curves, rates and duration of growth, and sexual dimorphism within the neurocranium, basicranium, palate, and face. The inclusion of fully adult animals revealed a full profile of sexual dimorphism. Additionally, we demonstrate for the first time diachronic change in adult sexual dimorphism caused by extended growth in adult females. A quicker growth rate in males from ages 2 to 8 was offset by a longer duration of growth in adult females that resulted in diminished dimorphism between the ages of 8 and 15. Four functional areas showed different sex-specific growth patterns, and the rate and duration of growth in the anterior facial skeleton contributed most to the changing profiles of sexual dimorphism. The late maturation in size of the female facial skeleton corresponds to later and less complete fusion of facial sutures. The prolongation of growth in females is hypothesized to be an evolutionary response to high levels of intrasexual competition, as is found in other primate species such as common chimpanzees with similar colony structure and reproductive behavior. Further investigation is required to determine (1) if this phenomenon observed in craniofacial skeletons is linked to sexual dimorphism in body size, and (2) whether this diachronic change in sexual dimorphism is species specific. The changing profile of sexual dimorphism in adult rhesus macaques suggests caution in studying sexual dimorphism in fossil primate and human forms.     

Primates and the evolution of long, slow life histories

Primates are characterized by relatively late ages at first reproduction, long lives and low fertility. Together, these traits define a life-history of reduced reproductive effort. Understanding the optimal allocation of reproductive effort, and specifically reduced reproductive effort, has been one of the key problems motivating the development of life-history theory. Because of their unusual constellation of life-history traits, primates play an important role in the continued development of life-history theory. In this review, I present the evidence for the reduced reproductive effort life histories of primates and discuss the ways that such life-history tactics are understood in contemporary theory. Such tactics are particularly consistent with the predictions of stochastic demographic models, suggesting a key role for environmental variability in the evolution of primate life histories. The tendency for?primates to specialize in high-quality, high-variability food items may make them particularly susceptible to environmental variability and explains their?low reproductive-effort tactics. I discuss recent applications of life-history theory to human evolution and emphasize the continuity between models used to explain peculiarities of human reproduction and senescence with the long, slow life histories of primates more generally.     

Brain size, development and metabolism in birds and mammals

Recent hypotheses that variation in brain size among birds and mammals result from differences in metabolic allocation during ontogeny are tested.
Indices of embryonic and post-embryonic brain growth are defined. Precocial birds and mammals have high embryonic brain growth indices which are compensated for by low post-embryonic indices (with the exception of Homo supiens ). In contrast, altricial birds and mammals have low embryonic and high post-embryonic indices. Altricial birds have relatively small brains at hatching and develop relatively large brains as adults, but among mammals there is no equivalent correlation between variation in adult relative brain sizes and state of neonatal development.
Compensatory brain development in both birds and mammals is associated with compensatory parental metabolic allocation. In comparison with altricial development, precocial development is characterized by higher levels of brain growth and parental metabolic allocation prior to hatching or birth and lower levels subsequently. Differences between degrees of postnatal investment by the parents in the young of precocial birds versus precocial mammals may result in the different patterns of adult brain size associated with precociality versus altriciality in the two groups.
The allometric exponent scaling brain on body size differs among taxonomic levels in birds. The exponent is higher for some parts of the brain than others, irrespective of taxonomic level. Unlike mammals, the exponents for birds do not show a general increase with taxonomic level. These pattcrns call into question recent interpretations of the allometric exponent in birds. and the reason for changes in exponent with taxonomic level.     

The Ontogeny of Encephalization: Tradeoffs Between Brain Growth,Somatic Growth,and Life History in Hominoids and Platyrrhines

This study examines variation in brain growth relative somatic growth in four hominoids and three platyrrhines to determine whether there is a trade-off during ontogeny. I predicted that somatic growth would be reduced during periods of extensive brain growth, and species with larger degrees of encephalization would reach a smaller body size at brain growth completion because more energy is directed towards the brain. I measured cranial capacity and skeletal size in over 500 skeletal specimens from wild populations. I calculated nonlinear growth curves and velocity curves to determine brain/body growth allometry during ontogeny. In addition, I calculated linear regressions to describe the brain/body allometry during the postnatal period prior to brain size reaching an asymptote. The results showed that somatic growth is not substantially reduced in species with extensive brain growth, and body size at brain growth completion was larger in species with greater degrees of encephalization. Furthermore, large body size at brain growth completion was not correlated with interbirth interval, but was significantly correlated with prolonged juvenile periods and late age at maturity when data were corrected for phylogeny. These results indicate that neither reduction in body growth nor reproductive rate are compensatory mechanisms for the energetic costs of brain growth. Other avenues for meeting energetic costs must be in effect. In addition, the results show that somatic growth in encephalized species is particularly slow during the juvenile period after brain growth at or near completion, suggesting that these growth patterns are explained by reasons other than energetic costs.     

Ontogenetic correlates of diet in Malagasy lemurs

There is a well-documented relationship between development and other life-history parameters among anthropoid primates. Smaller-bodied anthropoids tend to mature more rapidly than do larger-bodied species. Among anthropoids of similar body sizes, folivorous species tend to grow and mature more quickly than do frugivorous species, thus attaining adult body size at an earlier age. This pattern conforms to the expectations of Janson and van Schaik's "ecological risk aversion hypothesis," which predicts that rates of growth and maturation should vary in inverse relation to the intensity of intraspecific feeding competition. According to the ecological risk aversion hypothesis (RAH), species experiencing high intraspecific feeding competition will grow and mature slowly to reduce the risk of mortality due to food shortages. Species experiencing low levels of intraspecific feeding competition will shorten the juvenile period to reduce the overall duration of this high-risk portion of the life cycle. This paper focuses on development and maturation in lemurs. We show that folivorous lemurs (such as indriids) grow and mature more slowly than like-sized frugivorous lemurs (e.g., most lemurids), but tend to exhibit faster dental development. Their dental developmental schedules are accelerated on an absolute scale, relative to craniofacial growth, and relative to particular life-history landmarks, such as weaning. Dental development has a strong phylogenetic component: even those lemurids that consume substantial amounts of foliage have slower dental development than those indriids that consume substantial amounts of fruit. Implications of these results for the RAH are discussed, and an explanation for this hypothesis' failure to predict lemur growth schedules is offered. We propose that the differing developmental schedules of folivorous and frugivorous lemurs may reflect different solutions to the ecological problem of environmental instability: some rely on a strategy of low maternal input and slow returns, while others rely on a strategy of high maternal input and fast returns.     

Growth,development, and parental care in the western tarsier (Tarsius bancanus) in captivity: Evidence for a “slow” life-history and nonmonogamous mating system

I studied reproduction, prenatal and postnatal growth rates, behavioral ontogeny, and parental care in nine captive births to two wild-caught pairs of Tarsius bancanusover a 5-year period. T. bancanusinvariably gives birth to a single infant of approximately 20% maternal body mass after an extremely long gestation period. The fetal growth rate is among the slowest recorded for any mammal and the relative postnatal growth rate to physical maturity is the lowest in a sample of 26 prosimian species examined. These life-history variables, and a slow rate of reproduction, contribute to an extremely low г _max in this and other species of Tarsius.The relative rate of behavioral development, especially foraging and locomotor behaviors, is extremely rapid for a specialized predator. Infants attained nutritional independence at approximately 80 days and perfected hunting skills without apparent help from either parent. Mothers were very protective of their young and kept fathers from having contact with infants through heightened agonism after birth, and thus , there was no evidence of direct paternal care. The data suggest that there is an energetic/dietary basis for slow pre- and postnatal growth rates, but an extremely large neonatal brain size enables the rapid behavioral development and neuromuscular coordination necessary for this specialized predator to attain early nutritional independence. The captive and field data also suggest that extremely restrictive conditions exist for the purported monogamous mating system of T. bancanusand that an alternative mating system is more likely.