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.     

Telomere Biology and Cellular Aging in Nonhuman Primate Cells

To determine how cellular aging is conserved among primates, we analyzed the replicative potential and telomere shortening in skin fibroblasts of anthropoids and prosimians. The average telomere length of the New World primates Ateles geoffroyi (spider monkey) and Saimiri sciureus (squirrel monkey) and the Old World primates Macaca mulatta (rhesus monkey), Pongo pygmaeus (orangutan), and Pan paniscus (pigmy chimpanzee) ranged from 4 to 16 kb. We found that telomere shortening limits the replicative capacity of anthropoid fibroblasts and that the expression of human telomerase produced telomere elongation and the extension of their in vitro life span. In contrast the prosimian Lemur catta (ring-tailed lemur) had both long and short telomeres and telomere shortening did not provide an absolute barrier to immortalization. Following a transient growth arrest a subset of cells showing a reduced number of chromosomes overgrew the cultures without activation of telomerase. Here we show that the presence of continuous TTAGGG repeats at telomeres and rigorous control of replicative aging by telomere shortening appear to be conserved among anthropoid primates but is less effective in prosimian lemurs.     

Aspects of common marmoset basic biology and life history important for biomedical research

While common marmosets are increasingly used as alternative primate models in biomedical research, their life history, specialized behavior and unique physiology are not well known. This paper describes important marmoset attributes that are particularly relevant for biomedical research, including reproduction, neurobiology, immunology, endocrine signaling, obesity and aging, in addition to fetal and postnatal development. While common marmosets exhibit characteristic anthropoid primate traits, they clearly differ from Old World primates and humans in a variety of functions, including reproduction, endocrine signaling and immunology. These differences, however, permit the use of common marmosets in unconventional research strategies targeted on human pathology.     

Evaluating the “dual selection” hypothesis of canine reduction

A recently proposed model for canine reduction in hominid evolution (the “dual selection” model) suggests that canine reduction occurs as a result for incorporation of the canines into a functional incisal field. Among the evidence used to support this model are patterns of wear and occlusion of the canine teeth, particularly in female anthropoid primates. We examined wear and occlusal patterns of the canine teeth of 311 male and female anthropoid primates. We find no evidence that the canines are typically occluded tip-to-tip, or that they show wear patterns indicating a “gripping and pulling” function during food ingestion and processing. Furthermore, we do not find compelling evidence that the development of the mesial cristid is associated with canine reduction. While we agree that the mechanisms of selective pressures underlying canine reduction need to be investigated, the “dual selection” hypothesis is unsupported by comparative data. © 1996 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.     

Sexual Size Dimorphism,Canine Dimorphism,and Male-Male Competition in Primates

Sexual size dimorphism is generally associated with sexual selection via agonistic male competition in nonhuman primates. These primate models play an important role in understanding the origins and evolution of human behavior. Human size dimorphism is often hypothesized to be associated with high rates of male violence and polygyny. This raises the question of whether human dimorphism and patterns of male violence are inherited from a common ancestor with chimpanzees or are uniquely derived. Here I review patterns of, and causal models for, dimorphism in humans and other primates. While dimorphism in primates is associated with agonistic male mate competition, a variety of factors can affect male and female size, and thereby dimorphism. The causes of human sexual size dimorphism are uncertain, and could involve several non-mutually-exclusive mechanisms, such as mate competition, resource competition, intergroup violence, and female choice. A phylogenetic reconstruction of the evolution of dimorphism, including fossil hominins, indicates that the modern human condition is derived. This suggests that at least some behavioral similarities with Pan associated with dimorphism may have arisen independently, and not directly from a common ancestor.     

Investigation of the human Rh blood group system in nonhuman primates and other species with serologic and Southern blot analysis

To investigate the evolution of the Rh blood-group system in anthropoid apes, New and Old World monkeys, and nonprimate animals, serologic typing of erythrocytes from these species with antibodies specific for the human Rh blood-group antigens was performed. In addition, genomic DNA from these animals was analyzed on Southern blots with a human Rh-specific cDNA.Consistent with earlier reports, serologic results showed that gorilla and chimpanzee erythrocytes had epitopes recognized by human Rh D and c antisera, and gibbon erythrocytes were recognized by the c antisera. Surprisingly, some Old and New World monkeys also expressed a Rh c epitope on their erythrocytes. No erythrocytes from the nonprimate animals reacted specifically with any of the human Rh antisera.Southern blot analysis with a human Rh-specific cDNA probe detected Rh-related sequences in anthropoid apes, all New and Old World monkeys, and in most nonprimate animals tested. Although some Rh-related restriction fragments were conserved across species lines in primates, the Rh locus was more polymorphic in chimpanzees and gorillas than in humans. In addition, restriction fragments segregating with the presence of the D antigen in humans were present in the primate species that expressed the D antigen.     

Form and function of the oblique cord (chorda obliqua) in anthropoid primates

The oblique cord of the forearm in humans is a ligament connecting the anterolateral aspect of the ulna proximally to the posteromedial aspect of the radius distally, inserting just below the radial tuberosity. Its functional significance is uncertain, but it has been proposed that the ligament limits supination of the forearm or aids in resisting buckling failure in the curved radius. These functional explanations are unsatisfactory for bipedal humans who do not use their forelimbs in weight support. Furthermore, there are no evolutionary explanations for its presence in humans. The purpose of this study was to investigate the distribution and form of the oblique cord in non-human primates and to explore its possible functional significance and evolutionary origin in humans. Soft tissue dissections of anthropoid primates revealed the presence of an oblique cord in New and Old World monkeys and Asian apes. It was absent in all atelines. Passive manipulation of the two forearm bones in all specimens revealed that the ligament becomes most taut in pronation contrary to the proposed human condition. Isolated radii show that the oblique cord's radial insertion lacks a clear relationship with bone curvature, thus providing little support for the hypothesis of preventing buckling failure. The oblique cord's involvement in reducing bending strain in the curved radius is also unlikely. It is suggested here that the ligament may have a role in maintaining elbow stability in quadrupedal primates. Therefore, the function of the oblique cord in anthropoid primates suggests that its presence in modern humans may be a morphological and functional remnant from a quadrupedal ancestry.     

Contrasting histories of G6PD molecular evolution and malarial resistance in humans and chimpanzees

Although mutations in the glucose-6-phosphate dehydrogenase (G6PD) gene result in several blood-related diseases in humans, they also confer resistance to malarial infection. This association between G6PD and malaria was supported by population genetic analyses of the G6PD locus, which indicated that these mutations may have recently risen in frequency in certain geographic regions as a result of positive selection. Here we characterize nucleotide sequence variation in a 5.2-kb region of the G6PD locus in a population sample of 56 chimpanzees, as well as among 7 other nonhuman primates, to compare with that in humans in determining whether other primates that are impacted by malaria also exhibit patterns of G6PD polymorphism or divergence consistent with positive selection. We find that chimpanzees have several amino acid variants but that the overall pattern at G6PD in chimpanzees, as well as in Old and New World primates in general, can be explained by recent purifying selection as well as strong functional constraint dating back to at least 30-40 MYA. These comparative analyses suggest that the recent signature of positive selection at G6PD in humans is unique.     

The accelerated evolution of human cytochrome c oxidase – Selection for reduced rate and proton pumping efficiency?

The cytochrome c oxidase complex, complex VI (CIV), catalyzes the terminal step of the mitochondrial electron transport chain where the reduction of oxygen to water by cytochrome c is coupled to the generation of a protonmotive force that drive the synthesis of ATP. CIV evolution was greatly accelerated in humans and other anthropoid primates and appears to be driven by adaptive selection. However, it is not known if there are significant functional differences between the anthropoid primates CIV, and other mammals. Comparison of the high-resolution structures of bovine CIV, mouse CIV and human CIV shows structural differences that are associated with anthropoid-specific substitutions. Here I examine the possible effects of these substitutions in four CIV peptides that are known to affect proton pumping: the mtDNA-coded subunits I, II and III, and the nuclear-encoded subunit VIa2. I conclude that many of the anthropoid-specific substitutions could be expected to modulate the rate and/or the efficiency of proton pumping. These results are compatible with the previously proposed hypothesis that the accelerated evolution of CIV in anthropoid primates is driven by selection pressure to lower the mitochondrial protonmotive force and thus decrease the rate of superoxide generation by mitochondria.     

SINE insertions in cladistic analyses and the phylogenetic affiliations of Tarsius bancanus to other primates

Transpositions of Alu sequences, representing the most abundant primate short interspersed elements (SINE), were evaluated as molecular cladistic markers to analyze the phylogenetic affiliations among the primate infraorders. Altogether 118 human loci, containing intronic Alu elements, were PCR analyzed for the presence of Alu sequences at orthologous sites in each of two strepsirhine, New World and Old World monkey species, Tarsius bancanus, and a nonprimate outgroup. Fourteen size-polymorphic amplification patterns exhibited longer fragments for the anthropoids (New World and Old World monkeys) and T. bancanus whereas shorter fragments were detected for the strepsirhines and the outgroup. From these, subsequent sequence analyses revealed three Alu transpositions, which can be regarded as shared derived molecular characters linking tarsiers and anthropoid primates. Concerning the other loci, scenarios are represented in which different SINE transpositions occurred independently in the same intron on the lineages leading both to the common ancestor of anthropoids and to T. bancanus, albeit at different nucleotide positions. Our results demonstrate the efficiency and possible pitfalls of SINE transpositions used as molecular cladistic markers in tracing back a divergence point in primate evolution over 40 million years old. The three Alu insertions characterized underpin the monophyly of haplorhine primates (Anthropoidea and Tarsioidea) from a novel perspective.     

Chorionic gonadotropin has a recent origin within primates and an evolutionary history of selection

Chorionic gonadotropin (CG) is a critical signal in establishing pregnancy in humans and some other primates, but this placentally expressed hormone has not been found in other mammalian orders. The gene for one of its two subunits (CG beta subunit [CGbeta]) arose by duplication from the luteinizing hormone beta subunit gene (LHbeta), present in all mammals tested. In this study, 14 primate and related mammalian species were examined by Southern blotting and DNA sequencing to determine where in mammalian phylogeny the CGbeta gene originated. Bats (order Chiroptera), flying lemur (order Dermoptera), strepsirrhine primates, and tarsiers do not have a CGbeta gene, although they possess one copy of the LHbeta gene. The CGbeta gene first arose in the common ancestor of the anthropoid primates (New World monkeys, Old World monkeys, apes, and humans), after the anthropoids diverged from tarsiers. At least two subsequent duplication events occurred in the catarrhine primates, all of which possess multiple CGbeta copies. The LHbeta-CGbeta family of genes has undergone frequent gene conversion among the catarrhines, as well as periods of strong positive selection in the New World monkeys (platyrrhines). In addition, newly generated DNA sequences from the promoter of the CG alpha subunit gene indicate that platyrrhine monkeys use a different mechanism of alpha gene expression control than that found in catarrhines.     

COMPARATIVE ANALYSIS OF ANIMAL GROWTH: A PRIMATE CONTINUUM REVEALED BY A NEW DIMENSIONLESS GROWTH RATE COEFFICIENT

The comparative analysis of animal growth still awaits full integration into life‐history studies, partially due to the difficulty of defining a comparable measure of growth rate across species. Using growth data from 50 primate species, we introduce a modified "general growth model" and a dimensionless growth rate coefficient β that controls for size scaling and phylogenetic effects in the distribution of growth rates. Our results contradict the prevailing idea that slow growth characterizes primates as a group: the observed range of β values shows that not all primates grow slowly, with galago species exhibiting growth rates similar or above the mammalian average, while other strepsirrhines and most New World monkeys show limited reduction in growth rates. Low growth rate characterizes apes and some papionines. Phylogenetic regressions reveal associations between β and life‐history variables, providing tests for theories of primate growth evolution. We also show that primate slow growth is an exclusively postnatal phenomenon. Our study exemplifies how the dimensionless approach promotes the integration of growth rate data into comparative life‐history analysis, and demonstrates its potential applicability to other cases of adaptive diversification of animal growth patterns.     

Growth and sexual dimorphism in a population of hybrid macaques

Growth and sexual dimorphism have long been the focus of investigation for researchers interested in the life history and socioecology of nonhuman primates. Previous research has shown that sex differences in the duration of growth, or bimaturism, are primarily responsible for the sexual dimorphism observed in anthropoid primates with multimale–multifemale social structure, such as macaques. The present study investigates sex differences in patterns of craniofacial and somatometric growth relative to head and body size and relative to dental development in a population of hybrid macaques (Cercopithecidae: Macaca ) from Sulawesi, Indonesia. How these patterns may contribute to sexual dimorphism in this hybrid population is also examined. The results of the study suggest that there is no substantial effect on the levels of sexual dimorphism associated with hybridization in these macaques. Although sex differences in patterns of size-related, or allometric, growth patterns play a significant role in the development of sexual dimorphism for some cranial dimensions in these hybrids, bimaturism seems to be the primary component in the ontogeny of sexual dimorphism in this hybrid population. The observed levels of hybrid dimorphism and the predominant ontogenetic pattern of bimaturism characterized by prolonged male growth are consistent with previously published reports on dimorphism and growth in other cercopithecine primates.     

Heterochrony and sexual dimorphism in the skull of the Liberian chimpanzee (Pan troglodytes verus)

Allometric methods and theory derived from principles of relative growth provide new and powerful approaches to an understanding of the nature and development of sexual dimorphism among living primates. The Frankfurt collection of Liberian chimpanzee skulls and mandibles provides a large skeletal sample from a single natural population of wild shot animals, including individuals of all ages and both sexes, and allows investigation of allometric and heterochronic patterns of sexual dimorphism. Univariate, bivariate, and multivariate analyses are utilized in this study in order to ascertain the ontogenetic nature of male-female differences in the skull of the Liberian chimpanzee. The results of univariate and multivariate analyses indicate that, while overall levels of sexual dimorphism in the chimpanzee skull are small, the greatest differences are in dimensions of the viscerocranium, while neurocranial dimensions and orbital size tend to be less dimorphic. Bivariate regressions of 21 cranial variables against basicranial length document positive allometry in many facial and mandibular dimensions, and isometry or negative allometry for most neurocranial dimensions. The data confirm previous work in chimpanzees and other anthropoid primates suggesting that males and females are “ontogenetically scaled” in most cranial traits. That is, males and females share the same cranial growth trajectories, although ending up at different points. Both rate and time hypermorphosis are suggested as underlying causes of ontogenetic scaling in the Liberian chimpanzee.     

Sex and Status Effects on Primate Volubility: Clues to the Origin of Vocal Languages?

Natural human languages are predominantly vocal. This suggests that, during evolution, speech may have enhanced the efficiency, utility, or flexibility of previous vocal behaviors. If so, there may be parallels between certain aspects of the vocalization patterns of human and nonhuman primates. The literature on humans contains evidence for greater frequency of vocalization, or volubility, between female–female than male–male dyads, and greater volubility among individuals of higher than lower social rank or status. We analyzed two classes of vocalization in free-ranging vervet monkey infants. In both classes, females vocalized significantly more often than males, and high-ranking animals were more voluble than mid- and low-ranking animals. If these findings are confirmed in primates other than vervets, it is conceivable that the voice contributes to the solution of some pan-primate problems, offering clues to the vocal bias in human languages.     

The evolutionary origins of patriarchy

This article argues that feminist analyses of patriarchy should be expanded to address the evolutionary basis of male motivation to control female sexuality. Evidence from other primates of male sexual coercion and female resistance to it indicates that the sexual conflicts of interest that underlie patriarchy predate the emergence of the human species. Humans, however, exhibit more extensive male dominance and male control of female sexuality than is shown by most other primates. Six hypotheses are proposed to explain how, over the course of human evolution, this unusual degree of gender inequality came about. This approach emphasizes behavioral flexibility, cross-cultural variability in the degree of partriarchy, and possibilities for future change. This work was supported in part by NSF grant BNS-8857969. Barbara Smuts is a professor of psychology and anthropology at the University of Michigan. She received her B.A. in social anthropology at Harvard and her Ph.D. in bio-behavioral sciences at Stanford Medical School. She has studied the behavior of wild chimpanzees, baboons, and bottlenose dolphins and is particularly interested in evolutionary, comparative analyses of female-male relationships.     

Demography, life history, and social structure in Propithecus diadema edwardsi from 1986-2000 in Ranomafana National Park, Madagascar

Prosimian lemurs differ fundamentally from anthropoid primates in many traits related to social structure. By exploring the demography of Milne-Edwards' sifakas (Propithecus diadema edwardsi), and comparing it to other well-studied primates, we explore the effect of demographic and life-history factors on social structure. Specifically, we compare lemur survivorship and fertility patterns to two published composite models: one created for New World and another created for Old World monkeys. Using longitudinal data collected on individual Propithecus diadema edwardsi from four study groups from 1986-2000 in Ranomafana National Park, Madagascar, we quantify 1) group composition, 2) birth seasonality, 3) interbirth interval, 4) life-table values, and 5) population growth estimates. The mortality, survivorship, and life-expectancy schedules indicate high infant and juvenile mortality. Fertility remains high until death. The intrinsic rate of increase and net reproductive rate indicate a shrinking population. We suggest that high mortality rather than low fertility causes the observed population decline. While sifaka survivorship closely resembles New World patterns, fertility resembles Old World patterns, i.e., like New World monkeys, few sifakas survive to reproductive age, and those that do, reproduce at a slow rate resembling the Old World pattern. This necessarily impacts social structure. An adult sifaka at the end of her lifespan will have one only daughter who survives to reproductive age, compared to 3.4 for New World or 2.7 for Old World monkeys. Demography limits the formation of large kin-based groups for sifakas, and survivorship and fertility patterns do not easily permit sifakas to form large same-sex family groups.     

Toward a molecular paleontology of primate genomes

KpnI restriction of anthropoid primate DNAs, from a New World monkey to man, releases a series of segments that are remarkable among all of the alphoid DNAs in the constancy of their relative amounts in the various primate genomes, in their long-range organization, and in their internal sequence structure. These segments are labeled the KpnI A, B, C and D segments. Cross-hybridization analysis by Southern filter-transfer hybridization indicates that the KpnI segments represent separate and distinct families of alphoid DNAs. These families are termed the KpnI A, B, C and D families of alphoid sequences, of which only the KpnI A and B families were studied in detail here. - Evidence is presented suggesting that the KpnI segments do not exist as long, tandemly repeated sequences in the primate genome: rather, they may occur interspersed among other, perhaps nonalphoid sequences. From the stained gel patterns and from Southern filter-transfer hybridization experiments, the KpnI families appear to be absent from the genomes of the two prosimians studied - the galago and the black lemur. The KpnI A and B families are found among all of the anthropoid primates, including the New World capuchin monkey. The KpnI C family was detected in the genomes of the Old World anthropoid primates whereas the KpnI D family was detected only among the great apes and man. - The results are in accord with the observation (Musich et al., 1980) that with the continued evolutionary development of the primate Order, there has been a parallel trend toward an increased number and variety of alphoid DNA sequences. The properties of the KpnI families suggest that these sequences, unique among the alphoid DNAs, have been conservatively maintained throughout primate phylogeny and that they are among the most ancient of all primate DNAs.     

Polymorphism of glycophorins in nonhuman primate erythrocytes

Using immunoblotting techniques and polyclonal antisera to human erythrocyte glycophorin, we show that erythrocytes of several species of nonhuman primates, including representatives of anthropoid apes (19 chimpanzees, 3 gorillas, 6 orangutans, and 3 gibbons) and Old World monkeys (3 baboons, 5 rhesus monkeys, and 6 cynomologus macaques), contain human glycophorin-like molecules. Each species displays a unique glycophorin profile; in anthropoid apes the profile is more complex than in Old World monkeys and more similar to that seen in humans. The chimpanzee was the only species in which human -like glycophorin was detected but it differed from its human counterpart in electrophoretic mobility and reaction with M-specific monoclonal antibody. In contrast to humans, highly polymorphic glycophorin profiles were observed in each species of anthropoid apes and three distinct patterns were defined in each. No such polymorphism has been found so far among the Old World monkeys in the limited number of animals studied. The major glycophorins in all species but the chimpanzees failed to react with M- or N-specific monoclonal antibodies, suggesting structural differences from the human within the amino terminal regions. The reaction with the minor glycophorins showed inter- and intraspecies variability. All glycophorins, except -like glycophorin in the chimpanzee, reacted with the antiserum to the carboxyl terminal fragment of human glycophorin, indicating a structural relation to the human in this region. An unexpected correlation was observed, in the chimpanzee, between the patterns of electrophoretically resolved glycophorins and the V-A-B-D blood-group phenotypes, allowing the assignment of each determinant to specific glycophorin bands. The basis for the differences observed between human and nonhuman primate glycophorins is not clear but the possibilities include a common nonpolymorphic ancestor and differences in selective pressures.This research was supported by National Institutes of Health Grant 5 RO1 GM16389.