Stepwise evolution of stable sociality in primates

Although much attention has been focused on explaining and describing the diversity of social grouping patterns among primates, less effort has been devoted to understanding the evolutionary history of social living. This is partly because social behaviours do not fossilize, making it difficult to infer changes over evolutionary time. However, primate social behaviour shows strong evidence for phylogenetic inertia, permitting the use of Bayesian comparative methods to infer changes in social behaviour through time, thereby allowing us to evaluate alternative models of social evolution. Here we present a model of primate social evolution, whereby sociality progresses from solitary foraging individuals directly to large multi-male/multi-female aggregations (approximately 52 million years (Myr) ago), with pair-living (approximately 16?Myr ago) or single-male harem systems (approximately 16?Myr ago) derivative from this second stage. This model fits the data significantly better than the two widely accepted alternatives (an unstructured model implied by the socioecological hypothesis or a model that allows linear stepwise changes in social complexity through time). We also find strong support for the co-evolution of social living with a change from nocturnal to diurnal activity patterns, but not with sex-biased dispersal. This supports suggestions that social living may arise because of increased predation risk associated with diurnal activity. Sociality based on loose aggregation is followed by a second shift to stable or bonded groups. This structuring facilitates the evolution of cooperative behaviours and may provide the scaffold for other distinctive anthropoid traits including coalition formation, cooperative resource defence and large brains.     

Basal metabolic rate and energetics of reproduction in therian mammals

Traditionally, the fact that reproduction in eutherian (= placental) mammals tends towards prolonged intrauterine development and short lactation has been interpreted as an evolutionary advance over the metatherian (= marsupial) short gestation and prolonged lactation. However, it has recently been postulated that marsupial reproduction involves low initial energy investment and may be advantageous by minimizing energy loss if conditions necessitate early termination. Moreover, because marsupials have basal metabolic rates (BMRs) 30% lower than those of most eutherians, it has been suggested that daily and total energy expenditures during reproduction may also be lower. We have now tested the predictions that low BMR is maintained during reproduction and that initial investment is lower in marsupials. Using indirect calorimetry, we have made the first longitudinal measurements of energy expenditure during reproduction for a marsupial and for two eutherian species with low BMRs. We find that initial investment is lowest in a eutherian and total energetic expenditures were greatest for the marsupial. We also find that, relative to BMR, all three species have increased mean maternal resting metabolic rates (RMRs) during both gestation and lactation; this is the first evidence that mammals with low BMRs can substantially elevate metabolism for prolonged periods during gestation and lactation.     

Skull of the large non-macrostomatan snake Yurlunggur from the Australian Oligo-Miocene

Understanding the origin and early evolution of snakes from lizards depends on accurate morphological knowledge of the skull in basal lineages, but fossil specimens of archaic snakes have been rare, and either fragmentary or difficult to study as a result of compression by enclosing sediments. A number of Cenozoic fossil snakes from Australia have vertebral morphology diagnostic of an extinct group, Madtsoiidae, that was widespread in Gondwana from mid-Cretaceous (Cenomanian) to Eocene times, and also reached Europe in the late Cretaceous period. Despite this long history, only about half the skull is known from the best-known species Wonambi naracoortensis, and the few known cranial elements of other species have added little further evidence for phylogenetic relationships. Conflicting hypotheses have been proposed for their relationships and evolutionary significance, either as basal ophidians with many ancestral (varanoid- or mosasaur-like) features, or advanced (macrostomatan) alethinophidians of little relevance to snake origins. Here I report two partial skeletons referred to Yurlunggur, from the late Oligocene and early Miocene of northern Australia, which together represent almost the complete skull and mandible. The exceptionally preserved skulls provide new evidence linking Yurlunggur with Wonambi and other madtsoiids, falsifying predictions of the macrostomatan hypothesis, and supporting the exclusion of Madtsoiidae from the clade including all extant snakes.     

First skulls of the early Eocene primate Shoshonius cooperi and the anthropoid-tarsier dichotomy

The phylogenetic relationships of living tarsiers and extinct omomyid primates are critical for deciphering the origin and relationships of primate higher taxa, particularly anthropoids. Three competing phylogenetic hypotheses are: (1) tarsiers are most closely related to early Cenozoic Omomyidae, particularly genera such as Necrolemur from the late Eocene of Europe; (2) tarsiers share a more recent common ancestry with anthropoids than they do with any known omomyid; (3) tarsiers and/or omomyids are most closely related to strepsirhines. The anatomy of four skulls of the early Eocene omomyid Shoshonius cooperi--the first cranial material recovered for this genus--strongly suggests that Shoshonius shares a more recent common ancestry with Tarsius than do either anthropoids or other Eocene omomyids for which cranial anatomy is known. If the primate suborder Haplorhini (anthropoids, omomyids, tarsiids) is monophyletic, the phylogenetic position of Shoshonius requires that anthropoids and Tarsius diverged by at least the early Eocene, some 15 million years before the first appearance of anthropoids in the fossil record.     

Complex social behaviour derived from maternal reproductive traits

A fundamental goal of sociobiology is to explain how complex social behaviour evolves, especially in social insects, the exemplars of social living. Although still the subject of much controversy, recent theoretical explanations have focused on the evolutionary origins of worker behaviour (assistance from daughters that remain in the nest and help their mother to reproduce) through expression of maternal care behaviour towards siblings. A key prediction of this evolutionary model is that traits involved in maternal care have been co-opted through heterochronous expression of maternal genes to result in sib-care, the hallmark of highly evolved social life in insects. A coupling of maternal behaviour to reproductive status evolved in solitary insects, and was a ready substrate for the evolution of worker-containing societies. Here we show that division of foraging labour among worker honey bees (Apis mellifera) is linked to the reproductive status of facultatively sterile females. We thereby identify the evolutionary origin of a widely expressed social-insect behavioural syndrome, and provide a direct demonstration of how variation in maternal reproductive traits gives rise to complex social behaviour in non-reproductive helpers.     

Tribosphenic mammal from the North American Early Cretaceous

The main groups of living mammals, marsupials and eutherians, are presumed to have diverged in the Early Cretaceous, but their early history and biogeography are poorly understood. Dental remains have suggested that the eutherians may have originated in Asia, spreading to North America in the Late Cretaceous, where an endemic radiation of marsupials was already well underway. Here I describe a new tribosphenic mammal (a mammal with lower molar heels that are three-cusped and basined) from the Early Cretaceous of North America, based on an unusually complete specimen. The new taxon bears characteristics (molarized last premolar, reduction to three molars) otherwise known only for Eutheria among the tribosphenic mammals. Morphometric analysis and character comparisons show, however, that its molar structure is primitive (and thus phylogenetically uninformative), emphasizing the need for caution in interpretation of isolated teeth. The new mammal is approximately contemporaneous with the oldest known Eutheria from Asia. If it is a eutherian, as is indicated by the available evidence, then this group was far more widely distributed in the Early Cretaceous than previously appreciated. An early presence of Eutheria in North America offers a potential source for the continent's Late Cretaceous radiations, which have, in part, proven difficult to relate to contemporary taxa in Asia.     

Body weight, diet and home range area in primates.

Primates show a strong positive relationship between body weight and home range area. Dietary habits also influence home range area. Folivorous primates occupy smaller home range areas for their body weight than do frugivores and omnivores. Primates generally require smaller home range area per individual than solitary terrestrial mammals, but primates living in social groups have much larger total home range than individual solitary mammals. This trend may necessitate higher expenditures of energy in food-gathering or modifications in movement patterns.     

Mammal teeth from the Cretaceous of Africa

We report here the discovery of two mammal teeth from the early Cretaceous of Cameroon. These, and some jaw fragments, all from Cameroon, are the only fossil evidence of mammalian evolution from Africa between late Jurassic and Paleocene, a span of at least 85 million years. A triangular upper tooth lacks the principal internal cusp of marsupials and placentals and is therefore of a similar evolutionary grade to most Jurassic and early Cretaceous therian mammals, but more primitive than the metatherian-eutherian grade. Early Cretaceous, or older, therian mammals are now known from all southern continents except Antarctica. The new find from Cameroon is consistent with the hypothesis that marsupials, the dominant living mammals of South America and Australia, were not present on any Gondwana continents until after the early Cretaceous separation of Africa by the opening of the South Atlantic.     

Changes in the tooth enamel of early Paleocene mammals allowing increased diet diversity

Hunter-Schreger bands (HSB) are seen in teeth that are composed of crossed sets of enamel prisms. They are present in the teeth of man and many other mammals, but absent in most insectivores and multituberculates. It has been suggested that the presence of HSB makes the tooth enamel less likely to split and is associated with chewing ability. We have traced the occurrence of HSB back to the arctonic condylarths of the early Palaeocene (Puercan) age; this must be close to the first appearance of the bands in placental mammals. Our data indicate that the teeth of almost all large mammals since the early Palaeocene have contained these bands, in an orientation that is optimal for limiting the propagation of vertical fractures. The appearance of the bands is associated with the differentiation of herbivores and carnivores from insectivores and our data indicate that their development was critical to the diversification of mammals because it allowed the use of new types of foods.     

Ramapithecines from China: evidence from tooth dimensions

Data obtained from ramapithecine specimens found in Asia, Africa and Europe have suggested the existence of two major subgroups, Ramapithecus and Sivapithecus, with Ramapithecus having pre-human status. Recently, however, it has been proposed that the fossils all belong to a single group, Sivapithecus, which is more closely related to the apes, in particular the orang-utan. Here we analyse data from a series of similar fossils which have been found in late Miocene coalfields in Lufeng, Yunnan Province, China. These include a number of almost complete jaws and five partial skulls which are more complete than any others so far known. A statistical analysis of the overall dimensions of the large number of teeth included in these finds shows that the differences between the groups previously assigned to Ramapithecus and Sivapithecus are greater than those found between the sexes in the most sexually dimorphic of the living great apes. Within the groups the distribution is bimodal and we suggest each group contains sex subgroups.     

关于各种收敛性关系的若干反例及两个新的定理

主要研究了Lp（p≥1）空间中的强收敛（依范数收敛）、弱收敛与几乎处处收敛、依测度收敛、一致收敛之间的关系,并举出了若干反例;进一步对函数序列或测度空间作某些假设,得到了一些肯定的蕴涵关系与重要的结论.     

关于各种收敛性关系的若干反例及两个新的定理

主要研究了Lp(p≥1)空间中的强收敛(依范数收敛)、弱收敛与几乎处处收敛、依测度收敛、一致收敛之间的关系,并举出了若干反例;进一步对函数序列或测度空间作某些假设,得到了一些肯定的蕴涵关系与重要的结论.     

A 61-million-person experiment in social influence and political mobilization

Human behaviour is thought to spread through face-to-face social networks, but it is difficult to identify social influence effects in observational studies, and it is unknown whether online social networks operate in the same way. Here we report results from a randomized controlled trial of political mobilization messages delivered to 61 million Facebook users during the 2010 US congressional elections. The results show that the messages directly influenced political self-expression, information seeking and real-world voting behaviour of millions of people. Furthermore, the messages not only influenced the users who received them but also the users' friends, and friends of friends. The effect of social transmission on real-world voting was greater than the direct effect of the messages themselves, and nearly all the transmission occurred between 'close friends' who were more likely to have a face-to-face relationship. These results suggest that strong ties are instrumental for spreading both online and real-world behaviour in human social networks.     

Chimpanzees are indifferent to the welfare of unrelated group members

Humans are an unusually prosocial species-we vote, give blood, recycle, give tithes and punish violators of social norms. Experimental evidence indicates that people willingly incur costs to help strangers in anonymous one-shot interactions, and that altruistic behaviour is motivated, at least in part, by empathy and concern for the welfare of others (hereafter referred to as other-regarding preferences). In contrast, cooperative behaviour in non-human primates is mainly limited to kin and reciprocating partners, and is virtually never extended to unfamiliar individuals. Here we present experimental tests of the existence of other-regarding preferences in non-human primates, and show that chimpanzees (Pan troglodytes) do not take advantage of opportunities to deliver benefits to familiar individuals at no material cost to themselves, suggesting that chimpanzee behaviour is not motivated by other-regarding preferences. Chimpanzees are among the primates most likely to demonstrate prosocial behaviours. They participate in a variety of collective activities, including territorial patrols, coalitionary aggression, cooperative hunting, food sharing and joint mate guarding. Consolation of victims of aggression and anecdotal accounts of solicitous treatment of injured individuals suggest that chimpanzees may feel empathy. Chimpanzees sometimes reject exchanges in which they receive less valuable rewards than others, which may be one element of a 'sense of fairness', but there is no evidence that they are averse to interactions in which they benefit more than others.     

Enhanced partner preference in a promiscuous species by manipulating the expression of a single gene

The molecular mechanisms underlying the evolution of complex behaviour are poorly understood. The mammalian genus Microtus provides an excellent model for investigating the evolution of social behaviour. Prairie voles (Microtus ochrogaster) exhibit a monogamous social structure in nature, whereas closely related meadow voles (Microtus pennsylvanicus) are solitary and polygamous. In male prairie voles, both vasopressin and dopamine act in the ventral forebrain to regulate selective affiliation between adult mates, known as pair bond formation, as assessed by partner preference in the laboratory. The vasopressin V1a receptor (V1aR) is expressed at higher levels in the ventral forebrain of monogamous than in promiscuous vole species, whereas dopamine receptor distribution is relatively conserved between species. Here we substantially increase partner preference formation in the socially promiscuous meadow vole by using viral vector V1aR gene transfer into the ventral forebrain. We show that a change in the expression of a single gene in the larger context of pre-existing genetic and neural circuits can profoundly alter social behaviour, providing a potential molecular mechanism for the rapid evolution of complex social behaviour.     

Audience drives male songbird response to partner's voice

According to the social intelligence hypothesis, social context represents an important force driving the selection of animal cognitive abilities such as the capacity to estimate the nature of the social relationships between other individuals. Despite this importance, the influence of this force has been assessed only in primates and never in other animals showing social interactions. In this way, avian communication generally takes place in a network of signallers and receivers, which represents an audience altering individual signalling behaviours. Indeed, vocal amplitude and repertoire are known to be socially regulated and the attitude towards the opposite sex may change depending on the audience. This 'audience effect' provides support for the reality of social awareness in some bird species. However no evidence has yet been found to suggest that birds are able to estimate the characteristics of the social relationships between group-mates. Here we show that the male of a gregarious songbird species--the zebra finch (Taeniopygia guttata)--pays attention to the mating status of conspecific pairs, and uses this information to control its behaviour towards its female partner.     

Antagonistic pathways in neurons exposed to body fluid regulate social feeding in Caenorhabditis elegans

Wild isolates of Caenorhabditis elegans can feed either alone or in groups. This natural variation in behaviour is associated with a single residue difference in NPR-1, a predicted G-protein-coupled neuropeptide receptor related to Neuropeptide Y receptors. Here we show that the NPR-1 isoform associated with solitary feeding acts in neurons exposed to the body fluid to inhibit social feeding. Furthermore, suppressing the activity of these neurons, called AQR, PQR and URX, using an activated K(+) channel, inhibits social feeding. NPR-1 activity in AQR, PQR and URX neurons seems to suppress social feeding by antagonizing signalling through a cyclic GMP-gated ion channel encoded by tax-2 and tax-4. We show that mutations in tax-2 or tax-4 disrupt social feeding, and that tax-4 is required in several neurons for social feeding, including one or more of AQR, PQR and URX. The AQR, PQR and URX neurons are unusual in C. elegans because they are directly exposed to the pseudocoelomic body fluid. Our data suggest a model in which these neurons integrate antagonistic signals to control the choice between social and solitary feeding behaviour.     

Unrelated helpers in a social insect

High-resolution genetic markers have revolutionized our understanding of vertebrate mating systems, but have so far yielded few comparable surprises about kinship in social insects. Here we use microsatellite markers to reveal an unexpected and unique social system in what is probably the best-studied social wasp, Polistes dominulus. Social insect colonies are nearly always composed of close relatives; therefore, non-reproductive helping behaviour can be favoured by kin selection, because the helpers aid reproductives who share their genes. In P. dominulus, however, 35% of foundress nestmates are unrelated and gain no such advantage. The P. dominulus system is unlike all other cases of unrelated social insects, because one individual has nearly complete reproductive dominance over subordinates who could have chosen other reproductive options. The only significant advantage that subordinates obtain is a chance at later reproduction, particularly if the queen dies. Thus, P. dominulus societies are functionally unlike other social insects, but similar to certain vertebrate societies, in which the unrelated helpers gain through inheritance of a territory or a mate.     

Earliest known proboscidean from early Eocene of north-west Africa

The earliest known proboscidean remains have now been found at a new early Eocene locality at Brezina in southern Algeria (El Kohol). These new finds, represented by complete skulls and postcranial material, show several unexpected derived characters shared with the modern representatives of the Elephantoidea and the Deinotheriidae, suggesting close phylogenetic affinities and demonstrating also the great antiquity of the differentiation of modern proboscideans in Africa. These remains have been dated by associated charophyte flora and vertebrate remains which constitute the oldest known vertebrate community from the African Eocene.     

Social evaluation by preverbal infants

The capacity to evaluate other people is essential for navigating the social world. Humans must be able to assess the actions and intentions of the people around them, and make accurate decisions about who is friend and who is foe, who is an appropriate social partner and who is not. Indeed, all social animals benefit from the capacity to identify individual conspecifics that may help them, and to distinguish these individuals from others that may harm them. Human adults evaluate people rapidly and automatically on the basis of both behaviour and physical features, but the ontogenetic origins and development of this capacity are not well understood. Here we show that 6- and 10-month-old infants take into account an individual's actions towards others in evaluating that individual as appealing or aversive: infants prefer an individual who helps another to one who hinders another, prefer a helping individual to a neutral individual, and prefer a neutral individual to a hindering individual. These findings constitute evidence that preverbal infants assess individuals on the basis of their behaviour towards others. This capacity may serve as the foundation for moral thought and action, and its early developmental emergence supports the view that social evaluation is a biological adaptation.