Cognitive adaptations of social bonding in birds

The 'social intelligence hypothesis' was originally conceived to explain how primates may have evolved their superior intellect and large brains when compared with other animals. Although some birds such as corvids may be intellectually comparable to apes, the same relationship between sociality and brain size seen in primates has not been found for birds, possibly suggesting a role for other non-social factors. But bird sociality is different from primate sociality. Most monkeys and apes form stable groups, whereas most birds are monogamous, and only form large flocks outside of the breeding season. Some birds form lifelong pair bonds and these species tend to have the largest brains relative to body size. Some of these species are known for their intellectual abilities (e.g. corvids and parrots), while others are not (e.g. geese and albatrosses). Although socio-ecological factors may explain some of the differences in brain size and intelligence between corvids/parrots and geese/albatrosses, we predict that the type and quality of the bonded relationship is also critical. Indeed, we present empirical evidence that rook and jackdaw partnerships resemble primate and dolphin alliances. Although social interactions within a pair may seem simple on the surface, we argue that cognition may play an important role in the maintenance of long-term relationships, something we name as 'relationship intelligence'.     

Innovation in the collective brain

Innovation is often assumed to be the work of a talented few, whose products are passed on to the masses. Here, we argue that innovations are instead an emergent property of our species'' cultural learning abilities, applied within our societies and social networks. Our societies and social networks act as collective brains. We outline how many human brains, which evolved primarily for the acquisition of culture, together beget a collective brain. Within these collective brains, the three main sources of innovation are serendipity, recombination and incremental improvement. We argue that rates of innovation are heavily influenced by (i) sociality, (ii) transmission fidelity, and (iii) cultural variance. We discuss some of the forces that affect these factors. These factors can also shape each other. For example, we provide preliminary evidence that transmission efficiency is affected by sociality—languages with more speakers are more efficient. We argue that collective brains can make each of their constituent cultural brains more innovative. This perspective sheds light on traits, such as IQ, that have been implicated in innovation. A collective brain perspective can help us understand otherwise puzzling findings in the IQ literature, including group differences, heritability differences and the dramatic increase in IQ test scores over time.     

Social intelligence in the spotted hyena (Crocuta crocuta)

If the large brains and great intelligence characteristic of primates were favoured by selection pressures associated with life in complex societies, then cognitive abilities and nervous systems with primate-like attributes should have evolved convergently in non-primate mammals living in large, elaborate societies in which social dexterity enhances individual fitness. The societies of spotted hyenas are remarkably like those of cercopithecine primates with respect to size, structure and patterns of competition and cooperation. These similarities set an ideal stage for comparative analysis of social intelligence and nervous system organization. As in cercopithecine primates, spotted hyenas use multiple sensory modalities to recognize their kin and other conspecifics as individuals, they recognize third-party kin and rank relationships among their clan mates, and they use this knowledge adaptively during social decision making. However, hyenas appear to rely more intensively than primates on social facilitation and simple rules of thumb in social decision making. No evidence to date suggests that hyenas are capable of true imitation. Finally, it appears that the gross anatomy of the brain in spotted hyenas might resemble that in primates with respect to expansion of frontal cortex, presumed to be involved in the mediation of social behaviour.     

A claim in search of evidence: reply to Manger’s thermogenesis hypothesis of cetacean brain structure

In a recent publication in Biological Reviews, Manger (2006) made the controversial claim that the large brains of cetaceans evolved to generate heat during oceanic cooling in the Oligocene epoch and not, as is the currently accepted view, as a basis for an increase in cognitive or information‐processing capabilities in response to ecological or social pressures. Manger further argued that dolphins and other cetaceans are considerably less intelligent than generally thought. In this review we challenge Manger’s arguments and provide abundant evidence that modern cetacean brains are large in order to support complex cognitive abilities driven by social and ecological forces.     

On the evolution of brain size in relation to migratory behaviour in birds

Migratory birds appear to have relatively smaller brain size compared to sedentary species. It has been hypothesized that initial differences in brain size underlying behavioural flexibility drove the evolution of migratory behaviour; birds with relatively large brains evolved sedentary habits and those with relatively small brains evolved migratory behaviour (migratory precursor hypothesis). Alternative hypotheses suggest that changes in brain size might follow different behavioural strategies and that sedentary species might have evolved larger brains because of differences in selection pressures on brain size in migratory and nonmigratory species. Here we present the first evidence arguing against the migratory precursor hypothesis. We compared relative brain volume of three subspecies of the white-crowned sparrow: sedentary Zonotrichia leucophrys nuttalli and migratory Z. l. gambelii and Z. l. oriantha. Within the five subspecies of the white-crowned sparrow, only Z. l. nuttalli is strictly sedentary. The sedentary behaviour of Z. l. nuttalli is probably a derived trait, because Z. l. nuttalli appears to be the most recent subspecies and because all species ancestral to Zonotrichia as well as all older subspecies of Z. leucophrys are migratory. Compared to migratory Z. l. gambelii and Z. l. oriantha, we found that sedentary Z. l. nuttalli had a significantly larger relative brain volume, suggesting that the larger brain of Z. l. nuttalli evolved after a switch to sedentary behaviour. Thus, in this group, brain size does not appear to be a precursor to the evolution of migratory or sedentary behaviour but rather an evolutionary consequence of a change in migratory strategy.     

Co‐evolution of cerebral and cerebellar expansion in cetaceans

Cetaceans possess brains that rank among the largest to have ever evolved, either in terms of absolute mass or relative to body size. Cetaceans have evolved these huge brains under relatively unique environmental conditions, making them a fascinating case study to investigate the constraints and selection pressures that shape how brains evolve. Indeed, cetaceans have some unusual neuroanatomical features, including a thin but highly folded cerebrum with low cortical neuron density, as well as many structural adaptations associated with acoustic communication. Previous reports also suggest that at least some cetaceans have an expanded cerebellum, a brain structure with wide‐ranging functions in adaptive filtering of sensory information, the control of motor actions, and cognition. Here, we report that, relative to the size of the rest of the brain, both the cerebrum and cerebellum are dramatically enlarged in cetaceans and show evidence of co‐evolution, a pattern of brain evolution that is convergent with primates. However, we also highlight several branches where cortico‐cerebellar co‐evolution may be partially decoupled, suggesting these structures can respond to independent selection pressures. Across cetaceans, we find no evidence of a simple linear relationship between either cerebrum and cerebellum size and the complexity of social ecology or acoustic communication, but do find evidence that their expansion may be associated with dietary breadth. In addition, our results suggest that major increases in both cerebrum and cerebellum size occurred early in cetacean evolution, prior to the origin of the major extant clades, and predate the evolution of echolocation.     

Evolution of ASPM is associated with both increases and decreases in brain size in primates

A fundamental trend during primate evolution has been the expansion of brain size. However, this trend was reversed in the Callitrichidae (marmosets and tamarins), which have secondarily evolved smaller brains associated with a reduction in body size. The recent pursuit of the genetic basis of brain size evolution has largely focused on episodes of brain expansion, but new insights may be gained by investigating episodes of brain size reduction. Previous results suggest two genes (ASPM and CDK5RAP2) associated with microcephaly, a human neurodevelopmental disorder, may have an evolutionary function in primate brain expansion. Here we use new sequences encoding key functional domains from 12 species of callitrichids to show that positive selection has acted on ASPM across callitrichid evolution and the rate of ASPM evolution is significantly negatively correlated with callitrichid brain size, whereas the evolution of CDK5RAP2 shows no correlation with brain size. Our findings strongly suggest that ASPM has a previously unsuspected role in the evolution of small brains in primates. ASPM is therefore intimately linked to both evolutionary increases and decreases in brain size in anthropoids and is a key target for natural selection acting on brain size.     

Dolphin genome provides evidence for adaptive evolution of nervous system genes and a molecular rate slowdown

Cetaceans (dolphins and whales) have undergone a radical transformation from the original mammalian bodyplan. In addition, some cetaceans have evolved large brains and complex cognitive capacities. We compared approximately 10 000 protein-coding genes culled from the bottlenose dolphin genome with nine other genomes to reveal molecular correlates of the remarkable phenotypic features of these aquatic mammals. Evolutionary analyses demonstrated that the overall synonymous substitution rate in dolphins has slowed compared with other studied mammals, and is within the range of primates and elephants. We also discovered 228 genes potentially under positive selection (dN/dS > 1) in the dolphin lineage. Twenty-seven of these genes are associated with the nervous system, including those related to human intellectual disabilities, synaptic plasticity and sleep. In addition, genes expressed in the mitochondrion have a significantly higher mean dN/dS ratio in the dolphin lineage than others examined, indicating evolution in energy metabolism. We encountered selection in other genes potentially related to cetacean adaptations such as glucose and lipid metabolism, dermal and lung development, and the cardiovascular system. This study underlines the parallel molecular trajectory of cetaceans with other mammalian groups possessing large brains.     

Marmoset monkeys evaluate third-party reciprocity

Many non-human primates have been observed to reciprocate and to understand reciprocity in one-to-one social exchanges. A recent study demonstrated that capuchin monkeys are sensitive to both third-party reciprocity and violation of reciprocity; however, whether this sensitivity is a function of general intelligence, evidenced by their larger brain size relative to other primates, remains unclear. We hypothesized that highly pro-social primates, even with a relatively smaller brain, would be sensitive to others'' reciprocity. Here, we show that common marmosets discriminated between human actors who reciprocated in social exchanges with others and those who did not. Monkeys accepted rewards less frequently from non-reciprocators than they did from reciprocators when the non-reciprocators had retained all food items, but they accepted rewards from both actors equally when they had observed reciprocal exchange between the actors. These results suggest that mechanisms to detect unfair reciprocity in third-party social exchanges do not require domain-general higher cognitive ability based on proportionally larger brains, but rather emerge from the cooperative and pro-social tendencies of species, and thereby suggest this ability evolved in multiple primate lineages.     

Pandora's growing box: Inferring the evolution and development of hominin brains from endocasts

The brain of modern humans is an evolutionary and developmental outlier: At birth, it has the size of an adult chimpanzee brain and expands by a factor of 2 during the first postnatal year. Large neonatal brain size and rapid initial growth contrast with slow maturation, which extends well into adolescence. When, how, and why this peculiar pattern of brain ontogeny evolved and how it is correlated with structural changes in the brain are key questions of paleoanthropology. Because brains and their ontogenies do not fossilize, indirect evidence from fossil hominin endocasts needs to be combined with evidence from modern humans and our closest living relatives, the great apes. New fossil finds permit a denser sampling of hominin endocranial morphologies along ontogenetic and evolutionary time lines. New brain imaging methods provide the basis for quantifying endocast‐brain relationships and tracking endocranial and brain growth and development noninvasively. Combining this evidence with ever‐more detailed knowledge about actual and fossil “brain genes,” we are now beginning to understand how brain ontogeny and structure were modified during human evolution and what the adaptive significance of these modifications may have been.     

Socially induced brain development in a facultatively eusocial sweat bee Megalopta genalis (Halictidae)

Changes in the relative size of brain regions are often dependent on experience and environmental stimulation, which includes an animal''s social environment. Some studies suggest that social interactions are cognitively demanding, and have examined predictions that the evolution of sociality led to the evolution of larger brains. Previous studies have compared species with different social organizations or different groups within obligately social species. Here, we report the first intraspecific study to examine how social experience shapes brain volume using a species with facultatively eusocial or solitary behaviour, the sweat bee Megalopta genalis. Serial histological sections were used to reconstruct and measure the volume of brain areas of bees behaving as social reproductives, social workers, solitary reproductives or 1-day-old bees that are undifferentiated with respect to the social phenotype. Social reproductives showed increased development of the mushroom body (an area of the insect brain associated with sensory integration and learning) relative to social workers and solitary reproductives. The gross neuroanatomy of young bees is developmentally similar to the advanced eusocial species previously studied, despite vast differences in colony size and social organization. Our results suggest that the transition from solitary to social behaviour is associated with modified brain development, and that maintaining dominance, rather than sociality per se, leads to increased mushroom body development, even in the smallest social groups possible (i.e. groups with two bees). Such results suggest that capabilities to navigate the complexities of social life may be a factor shaping brain evolution in some social insects, as for some vertebrates.     

Beyond the phenotypic gambit: molecular behavioural ecology and the evolution of genetic architecture

Most studies of behaviour examine traits whose proximate causes include sensory input and neural decision-making, but conflict and collaboration in biological systems began long before brains or sensory systems evolved. Many behaviours result from non-neural mechanisms such as direct physical contact between recognition proteins or modifications of development that coincide with altered behaviour. These simple molecular mechanisms form the basis of important biological functions and can enact organismal interactions that are as subtle, strategic and interesting as any. The genetic changes that underlie divergent molecular behaviours are often targets of selection, indicating that their functional variation has important fitness consequences. These behaviours evolve by discrete units of quantifiable phenotypic effect (amino acid and regulatory mutations, often by successive mutations of the same gene), so the role of selection in shaping evolutionary change can be evaluated on the scale at which heritable phenotypic variation originates. We describe experimental strategies for finding genes that underlie biochemical and developmental alterations of behaviour, survey the existing literature highlighting cases where the simplicity of molecular behaviours has allowed insight to the evolutionary process and discuss the utility of a genetic knowledge of the sources and spectrum of phenotypic variation for a deeper understanding of how genetic and phenotypic architectures evolve.     

Understanding primate brain evolution

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

A comparison of neuropeptide immunocytochemistry in fluid-fixed and freeze-dried brains

Summary Immunocytochemical staining of luteinizing hormone-releasing hormone (LHRH), somatostatin, and neurophysin was compared in rat brains fixed with 1) formalin, 2) Bouin's solution, 3) freeze-dried (FD), or 4) freeze-dried + paraformaldehyde vapor perfused (FDV). The distribution of LHRH fibers was similar in all preparations; however, beads of granular reaction product often appeared finer and more numerous in the median eminence of FD- and FDV brains. Positively stained LHRH perikarya were not observed in any of the preparations. In contrast, somatostatin-immunoreactive perikarya were present in the fluid-fixed and FD brains, although few were observed in FDV brains. Somatostatin-immunoreactive fibers were present in all preparations, but appeared most numerous in the median eminence of FD brains. Staining of neurophysin-containing perikarya and fibers was similar in all preparations. These observations suggest that the FD brain can provide a suitable tissue substrate for immunocytochemistry, demonstrating staining comparable to or surpassing that of more conventional preparations. However, staining of antigens in FD brain was not uniformly successful and may depend on stereochemical characteristics of each antigen as well as properties of the primary antisera used in the staining procedure.     

Programmed cell death in trypanosomatids

It has generally been assumed that apoptosis and other forms of programmed cell death evolved to regulate growth and development in multicellular organisms. However, recent work has shown that some parasitic protozoa have evolved a cell suicide pathway analogous to the process described as apoptosis in metazoa. In this review, Susan Welburn, Marcello Barcinski and Gwyn Williams discuss the possible implications of a cell suicide pathway in the vector-borne Trypanosomatids.     

d-Aspartate in Human Brain

The presence of the biologically uncommon D-aspartic acid (D-aspartate) in human brain white matter has been previously reported. The earlier study has now been expanded to include D/L-aspartate ratios from 67 normal brains. The data show that the D-aspartate content increases rapidly from 1 year to approximately 35 years of age, levels off in middle age, and then appears to decrease somewhat. The D-aspartate content in gray matter remains at a consistently low level (half of that found in white matter) throughout the human life span. Within the limitations of current analytical methods, there was no detectable difference in D/L-aspartate ratios in white and gray matter of brains with Alzheimer's disease and several other pathologies when compared with brains of normal subjects. However, the presence of a significant D-aspartate level in white matter during the adult life span may lead to changes in protein configuration related to dysfunctions associated with the aging brain.     

Introduction to ‘Origin and evolution of the nervous system’

In 1665, Robert Hooke demonstrated in Micrographia the power of the microscope and comparative observations, one of which revealed similarities between the arthropod and vertebrate eyes. Utilizing comparative observations, Saint-Hilaire in 1822 was the first to propose that the ventral nervous system of arthropods corresponds to the dorsal nervous system of vertebrates. Since then, studies on the origin and evolution of the nervous system have become inseparable from studies about Metazoan origins and the origins of organ systems. The advent of genome sequence data and, in turn, phylogenomics and phylogenetics have refined cladistics and expanded our understanding of Metazoan phylogeny. However, the origin and evolution of the nervous system is still obscure and many questions and problems remain. A recurrent problem is whether and to what extent sequence data provide reliable guidance for comparisons across phyla. Are genetic data congruent with the geological fossil records? How can we reconcile evolved character loss with phylogenomic records? And how informative are genetic data in relation to the specification of nervous system morphologies? These provide some of the background and context for a Royal Society meeting to discuss new data and concepts that might achieve insights into the origin and evolution of brains and nervous systems.     

Queen Dominance May Reduce Worker Mushroom Body Size in a Social Bee

The mushroom body (MB) is an area of the insect brain involved in learning, memory, and sensory integration. Here, we used the sweat bee Megalopta genalis (Halictidae) to test for differences between queens and workers in the volume of the MB calyces. We used confocal microscopy to measure the volume of the whole brain, MB calyces, optic lobes, and antennal lobes of queens and workers. Queens had larger brains, larger MB calyces, and a larger MB calyces:whole brain ratio than workers, suggesting an effect of social dominance in brain development. This could result from social interactions leading to smaller worker MBs, or larger queen MBs. It could also result from other factors, such as differences in age or sensory experience. To test these explanations, we next compared queens and workers to other groups. We compared newly emerged bees, bees reared in isolation for 10 days, bees initiating new observation nests, and bees initiating new natural nests collected from the field to queens and workers. Queens did not differ from these other groups. We suggest that the effects of queen dominance over workers, rather than differences in age, experience, or reproductive status, are responsible for the queen–worker differences we observed. Worker MB development may be affected by queen aggression directly and/or manipulation of larval nutrition, which is provisioned by the queen. We found no consistent differences in the size of antennal lobes or optic lobes associated with differences in age, experience, reproductive status, or social caste.     

Larger brains spur species diversification in birds

Evidence is accumulating that species traits can spur their evolutionary diversification by influencing niche shifts, range expansions, and extinction risk. Previous work has shown that larger brains (relative to body size) facilitate niche shifts and range expansions by enhancing behavioral plasticity but whether larger brains also promote evolutionary diversification is currently backed by insufficient evidence. We addressed this gap by combining a brain size dataset for >1900 avian species worldwide with estimates of diversification rates based on two conceptually different phylogenetic‐based approaches. We found consistent evidence that lineages with larger brains (relative to body size) have diversified faster than lineages with relatively smaller brains. The best supported trait‐dependent model suggests that brain size primarily affects diversification rates by increasing speciation rather than decreasing extinction rates. In addition, we found that the effect of relatively brain size on species‐level diversification rate is additive to the effect of other intrinsic and extrinsic factors. Altogether, our results highlight the importance of brain size as an important factor in evolution and reinforce the view that intrinsic features of species have the potential to influence the pace of evolution.