The social brain hypothesis

Conventional wisdom over the past 160 years in the cognitive and neurosciences has assumed that brains evolved to process factual information about the world. Most attention has therefore been focused on such features as pattern recognition, color vision, and speech perception. By extension, it was assumed that brains evolved to deal with essentially ecological problem-solving tasks. © 1998 Wiley-Liss, Inc.     

Brain reorganization,not relative brain size,primarily characterizes anthropoid brain evolution

Comparative analyses of primate brain evolution have highlighted changes in size and internal organization as key factors underlying species diversity. It remains, however, unclear (i) how much variation in mosaic brain reorganization versus variation in relative brain size contributes to explaining the structural neural diversity observed across species, (ii) which mosaic changes contribute most to explaining diversity, and (iii) what the temporal origin, rates and processes are that underlie evolutionary shifts in mosaic reorganization for individual branches of the primate tree of life. We address these questions by combining novel comparative methods that allow assessing the temporal origin, rate and process of evolutionary changes on individual branches of the tree of life, with newly available data on volumes of key brain structures (prefrontal cortex, frontal motor areas and cerebrocerebellum) for a sample of 17 species (including humans). We identify patterns of mosaic change in brain evolution that mirror brain systems previously identified by electrophysiological and anatomical tract-tracing studies in non-human primates and functional connectivity MRI studies in humans. Across more than 40 Myr of anthropoid primate evolution, mosaic changes contribute more to explaining neural diversity than changes in relative brain size, and different mosaic patterns are differentially selected for when brains increase or decrease in size. We identify lineage-specific evolutionary specializations for all branches of the tree of life covered by our sample and demonstrate deep evolutionary roots for mosaic patterns associated with motor control and learning.     

Correlated evolution of brain regions involved in producing and processing facial expressions in anthropoid primates

Anthropoid primates are distinguished from other mammals by having relatively large primary visual cortices (V1) and complex facial expressions. We present a comparative test of the hypothesis that facial expression processing coevolved with the expansion of V1 in anthropoids. Previously published data were analysed using phylogenetic comparative methods. The results of our study suggest a pattern of correlated evolution linking social group size, facial motor control and cortical visual processing in catarrhines, but not platyrrhines. Catarrhines that live in relatively large social groups tended to have relatively large facial motor nuclei, and relatively large primary visual cortices. We conclude that catarrhine brains are adapted for producing and processing complex facial displays.     

Sperm competition and brain size evolution in mammals

The ‘expensive tissue hypothesis’ predicts a size trade‐off between the brain and other energetically costly organs. A specific version of this hypothesis, the ‘expensive sexual tissue hypothesis’, argues that selection for larger testes under sperm competition constrains brain size evolution. We show here that there is no general evolutionary trade‐off between brain and testis mass in mammals. The predicted negative relationship between these traits is not found for rodents, ungulates, primates, carnivores, or across combined mammalian orders, and neither does total brain mass vary according to the level of sperm competition as determined by mating system classifications. Although we are able to confirm previous reports of a negative relationship between brain and testis mass in echolocating bats, our results suggest that mating system may be a better predictor of brain size in this group. We conclude that the expensive sexual tissue hypothesis accounts for little or none of the variance in brain size in mammals, and suggest that a broader framework is required to understand the costs of brain size evolution and how these are met.     

Adaptive evolution of four microcephaly genes and the evolution of brain size in anthropoid primates

The anatomical basis and adaptive function of the expansion in primate brain size have long been studied; however, we are only beginning to understand the genetic basis of these evolutionary changes. Genes linked to human primary microcephaly have received much attention as they have accelerated evolutionary rates along lineages leading to humans. However, these studies focus narrowly on apes, and the link between microcephaly gene evolution and brain evolution is disputed. We analyzed the molecular evolution of four genes associated with microcephaly (ASPM, CDK5RAP2, CENPJ, MCPH1) across 21 species representing all major clades of anthropoid primates. Contrary to prevailing assumptions, positive selection was not limited to or intensified along the lineage leading to humans. In fact we show that all four loci were subject to positive selection across the anthropoid primate phylogeny. We developed clearly defined hypotheses to explicitly test if selection on these loci was associated with the evolution of brain size. We found positive relationships between both CDK5RAP2 and ASPM and neonatal brain mass and somewhat weaker relationships between these genes and adult brain size. In contrast, there is no evidence linking CENPJ and MCPH1 to brain size evolution. The stronger association of ASPM and CDK5RAP2 evolution with neonatal brain size than with adult brain size is consistent with these loci having a direct effect on prenatal neuronal proliferation. These results suggest that primate brain size may have at least a partially conserved genetic basis. Our results contradict a previous study that linked adaptive evolution of ASPM to changes in relative cortex size; however, our analysis indicates that this conclusion is not robust. Our finding that the coding regions of two widely expressed loci has experienced pervasive positive selection in relation to a complex, quantitative developmental phenotype provides a notable counterexample to the commonly asserted hypothesis that cis-regulatory regions play a dominant role in phenotypic evolution.     

The evolution of face processing in primates

The ability to recognize faces is an important socio-cognitive skill that is associated with a number of cognitive specializations in humans. While numerous studies have examined the presence of these specializations in non-human primates, species where face recognition would confer distinct advantages in social situations, results have been mixed. The majority of studies in chimpanzees support homologous face-processing mechanisms with humans, but results from monkey studies appear largely dependent on the type of testing methods used. Studies that employ passive viewing paradigms, like the visual paired comparison task, report evidence of similarities between monkeys and humans, but tasks that use more stringent, operant response tasks, like the matching-to-sample task, often report species differences. Moreover, the data suggest that monkeys may be less sensitive than chimpanzees and humans to the precise spacing of facial features, in addition to the surface-based cues reflected in those features, information that is critical for the representation of individual identity. The aim of this paper is to provide a comprehensive review of the available data from face-processing tasks in non-human primates with the goal of understanding the evolution of this complex cognitive skill.     

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

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

Problems of body-weight estimation in fossil primates

Body-weight estimates of fossil primates are commonly used to infer many important aspects of primate paleobiology, including diet, ecology, and relative encephalization. It is important to examine carefully the methodologies and problems associated with such estimates and the degree to which one can have confidence in them. New regression equations for predicting body weight in fossil primates are given which provide body-weight estimates for most nonhominid primate species in the fossil record. The consequences of using different subgroups (evolutionary “grades”) of primate species to estimate fossil-primate body weights are explored and the implications of these results for interpreting the primate fossil record are discussed. All species (fossil and extant) were separated into the following “grades”: prosimian grade, monkey grade, ape grade, anthropoid grade, and all-primates grade. Regression equations relating lower molar size to body weight for each of these grades were then calculated. In addition, a female-anthropoid grade regression was also calculated for predicting body weight infernales of extinct, sexually dimorphic anthropoid species. These equations were then used to generate the fossil-primate body weights. In many instances, the predicted fossil-primate body weights differ substantially from previous estimates.     

The fossil evidence of anthropoid brain evolution

The endocast of Aegyptopithecus, a 27 million year old ape, reveals that its brain was advanced over that of prosimians and comparable to that of modern anthropoids in relative size and in having expanded visual cortex, reduced olfactory bulbs, and a central sulcus separating primary somatic sensory and motor cortex. The early appearance of those features suggests that they may have been among the adaptations responsible for the evolution of anthropoids from prosimian ancestors. The frontal lobe was relatively smaller in Aegyptopithecus than in modern anthropoids. An endocast of Dolichocebus, one of the oldest known New World monkeys (25–30 million years old), reveals visual cortex expanded as in modern anthropoids. The 19 million year old Napak frontal bone displays a hominoid rather than cercopithecoid sulcal pattern. An 18 million year old endocast of the ape Dryopithecus (Proconsul) was neither monkey-like nor primitive, as originally described, but rather apelike and essentially modern in all observable features. The oldest undoubted Old World monkey endocast, from nine million year old Mesopithecus, reveals that the brain was modern in sulcal pattern and proportions. The sulcal pattern was like that of modern colobines, but that appears to be the more primitive condition, from which features characteristic of modern cercopithecine brains have evolved. The brain of six million year old Libypithecus was similar to that of Mesopithecus. A two million year old endocast of “Dolichopithecus” arvernensis displays a modern cercopithecine sulcal pattern.     

The evolution of non-maternal care in anthropoid primates: a test of the hypotheses

The amount of non-maternal care (allocare) found in primates varies greatly from species to species. Our paper examines this variation and focuses on possible reasons why mothers in some anthropoid primate species are prepared to relinquish their infants to other carers whereas others are not. We use data collected from the literature to test a number of hypotheses that attempt to explain the observed variation in non-maternal care. Analyses were carried out using comparative methods that control for the influence of both body size and phylogeny on life-history and ecological variation. The results support previous studies of both primates and other mammals in finding a clear link between the amount of allocare provided and female reproductive rates. Species with high allocare levels grow rapidly post-natally and wean their infants at a younger age (but at the same relative size) than species of the same body size with lower allocare levels. This early weaning allows high allocare species to support higher birth rates than low allocare species but does not result in earlier maturation. Our results, therefore, suggest that mothers allow non-maternal care of their infants in order to increase their own reproductive output. It is not clear whether such a strategy also benefits the infant, as we could find no link between the presence of allocare and early maturation (which would increase the infant's reproductive output) or between allocare levels and infant survival (as measured by vulnerability to infanticide). This suggests that mothers and infants might come into conflict over transfer to other carers, as the benefits to the mother may not be accompanied by benefits to the infant. However, although mothers may benefit from allocare in some circumstances, they will not be expected to allow allocare if the costs are high (e.g. if there is a high risk to the infant).     

Accelerated evolution of the electron transport chain in anthropoid primates

Mitochondria are both the power plant of the cell and a central integrator of signals that govern the lifespan, replication and death of the cell. Perhaps as a consequence, genes that encode components of the mitochondrial electron transport chain (ETC) are generally conserved. Therefore, it is surprising that many of these genes in anthropoid primates (New World monkeys, Old World monkeys and apes, including humans) have been major targets of darwinian positive selection. Sequence comparisons have provided evidence that marked increases of non-synonymous substitution rates occurred in anthropoid ETC genes that encode subunits of Complex III and IV, and the electron carrier molecule cytochrome c (CYC). Two important questions are: (i) how has evolution altered ETC function? and; (ii) how might functional changes in the ETC be linked to evolution of an expanded neocortical brain?     

The evolution of brain size and intelligence in man

The brain size of hominids has increased approximately threefold during the evolution of the hominids fromAustralopithecus toHomo sapiens. It is proposed that the principal reason for this increase is that larger brains conferred greater intelligence, and greater intelligence conferred a selection advantage. A number of anthropologists have difficulty accepting this thesis because they believe that brain size is not associated with intelligence in man. Evidence is reviewed, and new evidence from two studies is presented, to show that brain size as measured by head size is positively correlated with intelligence as measured by intelligence tests. On two recent samples statistically significant correlations of .21 and .30 were obtained between estimates of brain size and IQ. It is considered that brain size is positively associated with intelligence in man and that this is the major reason for the increase in brain size of the hominids during the last 3.2 million years.     

Effects of domestication on brain structure and behavior in mammals

The domestication of mammals has led to a reduction of brain size in general. There are, however, species-specific differences concerning the degree of mass decrease. Certain parts of the brains are also involved to different degrees but altogether rather unique effects are characteristic for domesticated mammals at different evolutionary levels. These changes in brain size and proportions are compared with behavioral changes due to domestication. They are valued as a result of artificial selection according to human demands, and thus, in zoological terms, they are interpreted as intraspecific adaptations to the special «ecological niche» of domestication.     

The evolution of animal 'cultures' and social intelligence

Decades-long field research has flowered into integrative studies that, together with experimental evidence for the requisite social learning capacities, have indicated a reliance on multiple traditions ('cultures') in a small number of species. It is increasingly evident that there is great variation in manifestations of social learning, tradition and culture among species, offering much scope for evolutionary analysis. Social learning has been identified in a range of vertebrate and invertebrate species, yet sustained traditions appear rarer, and the multiple traditions we call cultures are rarer still. Here, we examine relationships between this variation and both social intelligence--sophisticated information processing adapted to the social domain--and encephalization. First, we consider whether culture offers one particular confirmation of the social ('Machiavellian') intelligence hypothesis that certain kinds of social life (here, culture) select for intelligence: 'you need to be smart to sustain culture'. Phylogenetic comparisons, particularly focusing on our own study animals, the great apes, support this, but we also highlight some paradoxes in a broader taxonomic survey. Second, we use intraspecific variation to address the converse hypothesis that 'culture makes you smart', concluding that recent evidence for both chimpanzees and orangutans support this proposition.     

Setting priorities for the conservation of terrestrial vertebrates in Hungary

The first step towards the preservation of endangered species is to establish an appropriate ranking system, which assigns different nature conservation priority scores to different taxa. The system developed by Millsap et al. (Wildlife Monograph 1990, 111: 1–57) has been modified and applied to the mammal, bird, reptile, and amphibian species of Hungary. Three variable groups have been compiled, including eight (measuring biological characteristics), three (features of the Hungarian population) and five (evaluation of research and conservation actions) variables, respectively. In cooperation with several experts, we gave scores to all 379 taxa considered. The most endangered taxon proved to be the Hungarian Meadow Viper (Vipera ursinii rakosiensis), which occurs only in Hungary with just a few hundred individuals. The species rank depends on the availability and quality of data, so it is urgent to devote more effort to survey and monitoring projects. We present a possible application of the species list, where the taxa are grouped according to their legal status in Hungary (strictly protected, protected, partly protected and not protected), and the validity of this categorisation was tested by applying multivariate discriminant analysis. Only 58.36% of the species were correctly classified. The reasons for stronger than expected protection include popularity, attractiveness, and local rarity, while reasons for lower protection include preference for hunting and control of predators and pests.     

Neocortex evolution in primates: the "social brain" is for females

According to the social intelligence hypothesis, relative neocortex size should be directly related to the degree of social complexity. This hypothesis has found support in a number of comparative studies of group size. The relationship between neocortex and sociality is thought to exist either because relative neocortex size limits group size or because a larger group size selects for a larger neocortex. However, research on primate social evolution has indicated that male and female group sizes evolve in relation to different demands. While females mostly group according to conditions set by the environment, males instead simply go where the females are. Thus, any hypothesis relating to primate social evolution has to analyse its relationship with male and female group sizes separately. Since sex-specific neocortex sizes in primates are unavailable in sufficient quantity, I here instead present results from phylogenetic comparative analyses of unsexed relative neocortex sizes and female and male group sizes. These analyses show that while relative neocortex size is positively correlated with female group size, it is negatively, or not at all correlated with male group size. This indicates that the social intelligence hypothesis only applies to female sociality.     

Frequent non-reciprocal exchange in microsatellite-containing-DNA-regions of vertebrates

Microsatellites are DNA-fragments containing short repetitive motifs with 2–10 bp. They are highly variable in most species and distributed throughout the whole genome. It is broadly accepted that their high degree of variability is closely associated with mispairing of DNA-strands during the replication phase, termed slippage, although recombination is also observed. The aim of this study is to demonstrate evidence that non-reciprocal recombination processes changing the total genomic structure are common in microsatellites and flanking regions. We sequenced DNA fragments from birds in which microsatellites are located, and analyzed the structure of the microsatellites and their flanking regions. Additionally, other data and those from literature of three microsatellite regions of primates coding for the Ataxin-2, the Huntingtin and the TATA-box binding protein were analyzed. The structures of seven avian and three primate microsatellites support the hypothesis that non-reciprocal recombination is a common process that may also contribute considerably to the variation at microsatellite loci. We conclude that results of population genetic studies that are analyzed statistically with methods based on stepwise mutation models should be interpreted with caution if no detailed information on the allelic variation of microsatellites is available.