A convergent interaction engine: vocal communication among marmoset monkeys.

To understand the primate origins of the human interaction engine, it is worthwhile to focus not only on great apes but also on callitrichid monkeys (marmosets and tamarins). Like humans, but unlike great apes, callitrichids are cooperative breeders, and thus habitually engage in coordinated joint actions, for instance when an infant is handed over from one group member to another. We first explore the hypothesis that these habitual cooperative interactions, the marmoset interactional ethology, are supported by the same key elements as found in the human interaction engine: mutual gaze (during joint action), turn-taking, volubility, as well as group-wide prosociality and trust. Marmosets show clear evidence of these features. We next examine the prediction that, if such an interaction engine can indeed give rise to more flexible communication, callitrichids may also possess elaborate communicative skills. A review of marmoset vocal communication confirms unusual abilities in these small primates: high volubility and large vocal repertoires, vocal learning and babbling in immatures, and voluntary usage and control. We end by discussing how the adoption of cooperative breeding during human evolution may have catalysed language evolution by adding these convergent consequences to the great ape-like cognitive system of our hominin ancestors. This article is part of the theme issue 'Revisiting the human 'interaction engine': comparative approaches to social action coordination'.

The reluctant innovator: orangutans and the phylogeny of creativity.

Young orangutans are highly neophobic, avoid independent exploration and show a preference for social learning. Accordingly, they acquire virtually all their learned skills through exploration that is socially induced. Adult exploration rates are also low. Comparisons strongly suggest that major innovations, i.e. behaviours that have originally been brought into the population through individual invention, are made where ecological opportunities to do so are propitious. Most populations nonetheless have large innovation repertoires, because innovations, once made, are retained well through social transmission. Wild orangutans are therefore not innovative. In striking contrast, zoo-living orangutans actively seek novelty and are highly exploratory and innovative, probably because of positive reinforcement, active encouragement by human role models, increased sociality and an expectation of safety. The explanation for this contrast most relevant to hominin evolution is that captive apes generally have a highly reduced cognitive load, in particular owing to the absence of predation risk, which strongly reduces the costs of exploration. If the orangutan results generalize to other great apes, this suggests that our ancestors could have become more curious once they had achieved near-immunity to predation on the eve of the explosive increase in creativity characterizing the Upper Palaeolithic Revolution.

The evolutionary origin of human hyper-cooperation.

Proactive, that is, unsolicited, prosociality is a key component of our hyper-cooperation, which in turn has enabled the emergence of various uniquely human traits, including complex cognition, morality and cumulative culture and technology. However, the evolutionary foundation of the human prosocial sentiment remains poorly understood, largely because primate data from numerous, often incommensurable testing paradigms do not provide an adequate basis for formal tests of the various functional hypotheses. We therefore present the results of standardized prosociality experiments in 24 groups of 15 primate species, including humans. Extensive allomaternal care is by far the best predictor of interspecific variation in proactive prosociality. Proactive prosocial motivations therefore systematically arise whenever selection favours the evolution of cooperative breeding. Because the human data fit this general primate pattern, the adoption of cooperative breeding by our hominin ancestors also provides the most parsimonious explanation for the origin of human hyper-cooperation.

Parentage-based pedigree reconstruction reveals female matrilineal clusters and male-biased dispersal in nongregarious Asian great apes, the Bornean orang-utans (Pongo pygmaeus).

Philopatry and sex-biased dispersal have a strong influence on population genetic structure, so the study of species dispersal patterns and evolutionary mechanisms shaping them are of great interest. Particularly nongregarious mammalian species present an underexplored field of study: despite their lower levels of sociality compared to group-living species, interactions among individuals do occur, providing opportunities for cryptic kin selection. Among the least gregarious primates are orang-utans (genus: Pongo), in which preferential associations among females have nevertheless been observed, but for which the presence of kin structures was so far unresolved because of the equivocal results of previous genetic studies. To clarify relatedness and dispersal patterns in orang-utans, we examined the largest longitudinal set of individuals with combined genetic, spatial and behavioural data. We found that males had significantly higher mitochondrial DNA (mtDNA) variation and more unique haplotypes, thus underscoring their different maternal ancestries compared to females. Moreover, pedigree reconstruction based on 24 highly polymorphic microsatellite markers and mtDNA haplotypes demonstrated the presence of three matrilineal clusters of generally highly related females with substantially overlapping ranges. In orang-utans and possibly other nongregarious species, comparing average biparental relatedness (r) of males and females to infer sex-biased dispersal is extremely problematic. This is because the opportunistic sampling regime frequently employed in nongregarious species, combined with overlapping space use of distinct matrilineal clusters, leads to a strong downward bias when mtDNA lineage membership is ignored. Thus, in nongregarious species, correct inferences of dispersal can only be achieved by combining several genetic approaches with detailed spatial information.

Infanticide and reproductive restraint in a polygynous social mammal.

Alpha male chacma baboons experience uncontested access to individual estrus females. Consequently, alpha male paternity certainty is high and underpins significant levels of infanticide by immigrant males that, in turn, has selected for male defense of infants. There is also, however, a high probability that alpha males will be absent during the period when their own offspring are vulnerable, suggesting selection for additional countermeasures. We use data from a long-term study to test the prediction that alpha male chacma baboons cede reproductive opportunities to subordinate males and that this leads to the presence of other fathers that can serve as a buffer against infanticidal attack. We found that subordinate males obtained significantly more conceptive opportunities than predicted by priority of access alone, and that this occurred because alpha males did not consort all receptive periods. There was no evidence that this was due to energetic constraint, large male cohorts, alpha male inexperience, or the competitive strength of queuing subordinates. The number of males who benefited from concession and the length of time that they were resident relative to those who did not benefit in this way greatly reduced the probability that infants of alpha males would face immigrant males without a surrogate father whose own offspring were vulnerable. The absence of such males was associated with observed infanticide as well as, unexpectedly, an increased likelihood of takeover when alpha males with vulnerable infants were present.

Life history of wild Sumatran orangutans (Pongo abelii).

We present life history data on wild Sumatran orangutans gleaned from a 32-year and a 5.5-year study. Estimated age at first reproduction was 15.4 years. At 9.3 years, the average interbirth interval for this population is the longest ever recorded for any great ape population, significantly longer than that of a Bornean orangutan population. We find that age-specific mortality of Sumatran orangutans does not differ between sexes and is significantly lower than that of wild chimpanzees. We conclude that orangutan life history is the slowest among extant great apes. In accordance with their slow life history, longevity in the wild is estimated to be at least 58 years for males and at least 53 for females. We find no evidence for menopause. These data suggest that compared to the ancestral state, humans have undergone less of an increase in longevity than commonly assumed, and have experienced selection on earlier cessation of reproduction.

Health status of young children during therapy for advanced neuroblastoma.

BACKGROUND: The purpose of this study was to describe the health status experienced by young children during various phases of therapy for advanced neuroblastoma. METHODS: Nineteen patients aged 2.00-4.99 years at the time of diagnosis of neuroblastoma (stages 3 or 4) who received active therapy between 1996 and 2000 were enrolled on the study. Their parents provided proxy assessments of their health status at a maximum of 10 assessment points during therapy using the Comprehensive Health Status Classification System for Pre-school Children (CHSCS-PS), which assesses level of function on 10 separate health domains. RESULTS: Eighty-six assessment questionnaires were completed. Maximum morbidity was reported immediately following diagnosis and in the 2-3 weeks following bone marrow transplantation. The greatest morbidity was observed in the pain, self-care, mobility, and emotion domains. CONCLUSIONS: In addition to facing a high risk of mortality, young children being treated for advanced neuroblastoma also experience considerable morbidity.

Inter-observer agreement of a comprehensive health status classification system for pre-school children among patients with Wilms' tumor or advanced neuroblastoma.

We assessed inter-observer agreement on a new comprehensive health status classification system for preschool children (CHSCS-PS). Prospective assessments of children aged 2-4.9 years at the time of diagnosis of neuroblastoma (stages 3-4, excluding 4S) or Wilms' tumor (stages II-V) were collected independently from a parent and nurse by self-report during therapy. Responses were used to determine functional status on 10 health domains, as well as an overall disability score. Inter-observer agreement was evaluated by a kappa statistic for agreement about levels within individual domains, and by an intraclass correlation coefficient (ICC) for agreement of overall disability scores. Twenty-four parent/nurse pairs of assessments were collected. Agreement was almost perfect for mobility and self-care, substantial for emotion and pain, and slight for speech. There was high percent agreement for vision, hearing, dexterity, learning and remembering, and thinking and problem solving, but insufficient variability in responses to calculate a kappa statistic. The ICC for overall disability scores between observers was 0.86, indicating strong agreement. Given the need for, and paucity of, instruments for the measurement of health-related quality of life in very young children, these results strongly support further evaluation of the CHSCS-PS.

Loss of oestrus, concealed ovulation and paternity confusion in free-ranging Hanuman langurs.

Ovarian cycles in catarrhine primates are uniquely characterized by prolonged periods of sexual activity in which the timings of ovulation and copulation do not necessarily correspond. According to current hypotheses of primate social evolution, extended sexuality in multi-male groups might represent part of a female strategy to confuse paternity in order to reduce the risk of infanticide by males. We test this hypothesis by examining mating behaviour in relation to timing of ovulation and paternity outcome in a multi-male group of free-living Hanuman langurs. Using faecal progestogen measurements, we first document that female langurs have extended receptive periods in which the timing of ovulation is highly variable. Next, we demonstrate the capacity for paternity confusion by showing that ovulation is concealed from males and that copulations progressively decline throughout the receptive phase. Finally, we demonstrate multiple paternity, and show that despite a high degree of monopolization of receptive females by the dominant male, non-dominant males father a substantial proportion of offspring. We believe that this is the first direct evidence that extended periods of sexual activity in catarrhine primates may have evolved as a female strategy to confuse paternity.

Geographic variation in tool use on Neesia fruits in orangutans.

Geographic variation in the presence of skilled behavior may reflect geographic variation in genetic predispositions or ecological conditions (accompanied by reliable expression during development), or it may reflect the vagaries of invention and the appropriate social conditions for persistence. In this study, we compare the feeding techniques and tool-using skills used by orangutans to extract the nutritious seeds from Neesia fruits between Suaq Balimbing on Sumatra and Gunung Palung on Borneo, and map the distribution of Neesia tool use in Sumatran swamps. We show that neither genetics nor ecology is sufficient to explain the distribution of this tool use, confirming earlier findings on chimpanzees. We conclude that the ability to learn to use tools determines the geographic distribution. It is impossible to distinguish between the history of invention and the conditions for social transmission as the causal factors, but the high density and the social tolerance at Suaq Balimbing create propitious conditions for the maintenance of the skill as a tradition once it has been invented. High orangutan densities in the other Sumatran coastal swamps with Neesia tool use support the conclusion that suitable transmission conditions are the critical factor to explain the geographic distribution of skills such as feeding tool use.

The development of symmetrical OKN in infants: quantification based on OKN acuity for nasalward versus temporalward motion.

We quantified OKN asymmetry in 140 normal infants, 3-24 months old, by varying spatial frequency to determine OKN acuity for temporal-to-nasal (T-N) versus nasal-to-temporal (N-T) motion. At all ages, OKN acuity was asymmetrical (better for T-N than for N-T motion) but the size of the asymmetry decreased from 3.2 to 0.7 octaves between 3-24 months, primarily because of improvements in OKN acuity for N-T motion. The results suggest that immaturities in the cortical pathways involved in OKN persist until at least 2 years of age.

Comparative tests of primate cognition: different scaling methods produce different results.

Although early comparative studies supported hypotheses that ecological demands selected for primate cognition, later work indicated that social demands were more important. One difference between earlier and later studies is that earlier studies scaled brain structures by (A) taking residuals from an interspecific regression of the brain structure in question on body mass, whereas later studies scaled them by (B) taking residuals from an interspecific regression of the brain structure in question on another brain structure or by (C) taking ratios of the brain structure in question to another brain structure. We conducted a series of comparative tests to explore the possibility that the different methods are responsible for the discrepancy between earlier and later studies. Specifically, we tested the ability of a social variable - group size - and an ecological variable - home range size - to explain variation in the non-V1 isocortex (isocortex minus primary visual cortex) when this structure was scaled with the three different methods. In multiple regression analysis, group size was a better predictor of the non-V1 isocortex with method (B). With methods (A) and (C), however, results were ambiguous: either home range size or group size explained more of the variation, depending on the inclusion of outliers, the use of independent contrasts, and whether home range size was scaled relative to body mass. We examine the three scaling methods and find no reasonable basis for preferring any of them. Hence, our results do not allow a distinction between social and ecological hypotheses. The general implications of our study are that (1) previous comparative studies are inconclusive and (2) further research is needed to develop a scaling method where relative measures of brain structure size are demonstrated to correspond with behavioral performance.

The conditions for tool use in primates: implications for the evolution of material culture.

In order to identify the conditions that favored the flourishing of primate tool use into hominid technology, we examine inter- and intraspecific variation in manufacture and use of tools in extant nonhuman primates, and develop a model to account for their distribution. We focus on tools used in acquiring food, usually by extraction. Any model for the evolution of the use of feeding tools must explain why tool use is found in only a small subset of primate species, why many of these species use tools much more readily in captivity, why routine reliance on feeding tools is found in only two species of ape, and why there is strong geographic variation within these two species. Because ecological factors alone cannot explain the distribution of tool use in the wild, we develop a model that focuses on social and cognitive factors affecting the invention and transmission of tool-using skills. The model posits that tool use in the wild depends on suitable ecological niches (especially extractive foraging) and the manipulative skills that go with them, a measure of intelligence that enables rapid acquisition of complex skills (through both invention and, more importantly, observational learning), and social tolerance in a gregarious setting (which facilitates both invention and transmission). The manipulative skills component explains the distribution across species of the use of feeding tools, intelligence explains why in the wild only apes are known to make and use feeding tools routinely, and social tolerance explains variation across populations of chimpanzees and orangutans. We conclude that strong mutual tolerance was a key factor in the explosive increase in technology among hominids, probably intricately tied to a lifestyle involving food sharing and tool-based processing or the acquisition of large, shareable food packages.

Assessment of health status and health-related quality of life in survivors of Hodgkin's disease in childhood.

Although the great majority of children with Hodgkin's disease survive with modern treatment strategies, the list of late sequelae is long, yet there is no published information on the comprehensive health status and health-related quality of life (HRQL) in this population. In the experience of a single institution, survivors of Hodgkin's disease in childhood were invited to self-report on their health status using a 15-item questionnaire connected to the Health Utilities Index, a series of multi-attribute health status classification systems that, in turn, are linked to preference functions which provide single-attribute and global utility scores for HRQL. The mean global utility score was 0.85 (on a 0 = dead to 1. 0 = perfect health scale), a figure less than that in survivors of acute lymphoblastic leukemia (ALL) but comparable to that in survivors of brain tumors (0.84) or extremely low birthweight (ELBW 0.82). The burden of morbidity is emphasized by the ratio of the numbers of health states per patient:0.67 for survivors of Hodgkin's disease, 0.66 for survivors of brain tumors, 0.39 for survivors of ELBW, 0.47 for survivors of high-risk ALL and 0.28 for survivors of standard-risk ALL. In Hodgkin's disease survivors, the attributes affected most commonly and severely were pain, cognition and emotion. This experience demands exploration of the health status and HRQL in a much larger cohort of such survivors, perhaps in the context of co-operative group studies.

The socioecology of fission-fusion sociality in Orangutans.

Fission-fusion systems can have the group or the individual as their primary unit. In group-based fission-fusion systems, predation risk reduction is the major benefit to grouping, in the individual-based ones the benefits are likely to be primarily social. Orangutans, like chimpanzees, are examples of an individual-based fission-fusion species. The orangutans inhabiting a Sumatran swamp forest (Suaq Balimbing) are more likely than elsewhere to form travel parties. As elsewhere, the main benefits of grouping are social: mating opportunities, protection from harassment and socialization of infants. Most animals also incur costs, but these are relatively low at Suaq Balimbing due to the high productivity of the swamp. Costs seem to be disproportionately high for females with mid-sized infants, who avoid parties.

The effects of dominance rank and group size on female lifetime reproductive success in wild long-tailed macaques,Macaca fascicularis.

Demographic changes were recorded throughout a 12-year period for three social groups ofMacaca fascicularis in a natural population at Ketambe (Sumatra, Indonesia). We examined the prediction that females' lifetime reproductive success depended on dominance rank and group size. Average birth rate was 0.53 (184 infants born during 349 female years). For mature females (aged 8-20 yr) birth rate reflected physical condition, being higher in years with high food availability and lower in the year following the production of a surviving infant. High-ranking females were significantly more likely than low-ranking ones to give birth again when they did have a surviving offspring born the year before (0.50 vs 0.26), especially in years with relatively low food availability (0.37 vs 0.10). Controlled comparisons of groups at different sizes indicate a decline in birth rate with rroup size only once a group has exceeded a certain size. The dominance effect on birth rate tended to be strongest in large groups.Survival of infants was rank-dependent, but the survival of juveniles was not. There was a trend for offspring survival to be lower in large groups than in mid-sized or small groups. However, rank and group size interacted, in that rank effects on offspring survival were strongest in large groups. High-ranking females were less likely to die themselves during their top-reproductive years, and thus on average had longer reproductive careers.We estimated female lifetime reproductive success based on calculated age-specific birth rates and survival rates. The effects of rank and group size (contest and scramble) on birth rate, offspring survival, age of first reproduction for daughters, and length of reproductive career, while not each consistently statistically significant, added up to substantial effects on estimated lifetime reproductive success. The group size effects explain why large groups tend to split permanently.Since females are philopatric in this species, and daughters achieve dominance rank positions similar to their mother, a close correlation is suggested between the lifetime reproductive success of mothers and daughters. For sons, too, maternal dominance affected their reproductive success: high-born males were more likely to become top-dominant (in another group). These data support the idea that natural selection has favored the evolution of a nepotistic rank system in this species, even if the annual benefits of dominance are small.

Exploratory study on the economic value of a closed farming system on Dutch dairy farms.

A closed farming system may prevent the introduction of infectious diseases on to dairy farms and could be a good starting point for the eradication of these diseases. In order to introduce a closed farming system, farmers need to be made aware of how these diseases are introduced into the herd. Farmers will be more likely to implement a closed farming system when the economic value is quantified and attractive. An exploratory study was carried out to investigate the technical and economic results of closed dairy farms. Farms that purchased cattle and/or shared pasture (defined as 'open' farms) differed in technical results from farms that did not ('closed' farms). The results of the discriminant analysis showed that the 'closed' farms incurred lower costs for veterinary services, had a lower average age at first calving and a higher birth rate per 100 dairy cows. A linear regression analysis was carried out to investigate the influence of the farming system on economic performance. Being 'closed' was found to increase the net profit by 0.31 Pound per 100 kg of milk, or approximately 25 Pounds per cow per year or 5 per cent of the typical net return to labour and management (1 Pound = Dfl 2.80 in November 1996).

Primate species richness is determined by plant productivity: implications for conservation.

The explanation of patterns in species richness ranks among the most important tasks of ecology. Current theories emphasize the interaction between historical and geographical factors affecting the size of the regional species pool and of locally acting processes such as competitive exclusion, disturbance, productivity, and seasonality. Local species richness, or alpha diversity, of plants and primary consumers has been claimed to peak in habitats of low and intermediate productivity, which, if true, has major implications for conservation. Here, by contrast, we show that local richness of Neotropical primates (platyrrhines) is influenced by both historical biogeography and productivity but not by tree species richness or seasonality. This pattern indicates that habitats with the highest plant productivity are also the richest for many important primary consumers. We show further that fragmentation of Amazonian rain forests in the Pleistocene, if it occurred, appears to have had a negligible influence on primate alpha species richness.

Infanticide risk and the evolution of male-female association in primates.

Year-round association between adult males and females is common in primates, even though internal gestation and lactation predispose males to mate-desertion in the majority of mammals. Because there is little a priori support for alternative explanations, we hypothesized that permanent male-female association in primates serves to reduce the risk of infanticide by strange males whenever females and infants are closely associated. For a phylogenetic test of this hypothesis, we reconstructed the evolution of male-female and female-infant association among primates. The results of Maddison's concentrated changes test confirmed the prediction that mother-infant association, as opposed to infant parking, and female-male association did not evolve independently. Changes in litter size and activity, in contrast, were not significantly associated with evolutionary changes in male-female association. Thus, we demonstrate a fundamental link between primate life history and social behaviour, explain the most basic type of variation in primate social organization, and propose an additional determinant of social organization that may also operate in other mammals.

Intrasexual competition and body weight dimorphism in anthropoid primates.

Body weight dimorphism in anthropoid primates has been thought to be a consequence of sexual selection resulting from male-male competition for access to mates. However, while monogamous anthropoids show low degrees of weight dimorphism, as predicted by the sexual selection hypothesis, polygynous anthropoids show high variation in weight dimorphism that is not associated with measures of mating system or sex ratio. This observation has led many to debate the role of other factors such as dietary constraints, predation pressure, substrate constraints, allometric effects, and phylogeny in the evolution of anthropoid weight dimorphism. Here, we re-evaluate variation in adult body weight dimorphism in anthropoids, testing the sexual selection hypothesis using categorical estimates of the degree of male-male intrasexual competition ("competition levels"). We also test the hypotheses that interspecific variation in body weight dimorphism is associated with female body weight and categorical estimates of diet, substrate use, and phylogeny. Weight dimorphism is strongly associated with competition levels, corroborating the sexual selection hypothesis. Weight dimorphism is positively correlated with increasing female body weight, but evidence suggests that the correlation reflects an interaction between overall size and behavior. Arboreal species are, on average, less dimorphic than terrestrial species, while more frugivorous species tend to be more dimorphic than folivorous or insectivorous species. Several alternative hypotheses can explain these latter results. Weight dimorphism is correlated with taxonomy, but so too are competition levels. We suggest that most taxonomic correlations of weight dimorphism represent "phylogenetic niche conservatism"; however, colobines show consistently low degrees of weight dimorphism for reasons that are not clear.