Karin Isler

Overall Brain Size, and Not Encephalization Quotient, Best Predicts Cognitive Ability across Non-Human Primates

For over a century, various neuroanatomical measures have been employed as assays of cognitive ability in comparative studies. Nevertheless, it is still unclear whether these measures actually correspond to cognitive ability. A recent meta-analysis of cognitive performance of a broad set of primate species has made it possible to provide a quantitative estimate of general cognitive ability across primates. We find that this estimate is not strongly correlated with neuroanatomical measures that statistically control for a possible effect of body size, such as encephalization quotient or brain size residuals. Instead, absolute brain size measures were the best predictors of primate cognitive ability. Moreover, there was no indication that neocortex-based measures were superior to measures based on the whole brain. The results of previous comparative studies on the evolution of intelligence must be reviewed with this conclusion in mind.

Energetics and the evolution of human brain size

The human brain stands out among mammals by being unusually large. The expensive-tissue hypothesis explains its evolution by proposing a trade-off between the size of the brain and that of the digestive tract, which is smaller than expected for a primate of our body size. Although this hypothesis is widely accepted, empirical support so far has been equivocal. Here we test it in a sample of 100 mammalian species, including 23 primates, by analysing brain size and organ mass data. We found that, controlling for fat-free body mass, brain size is not negatively correlated with the mass of the digestive tract or any other expensive organ, thus refuting the expensive-tissue hypothesis. Nonetheless, consistent with the existence of energy trade-offs with brain size, we find that the size of brains and adipose depots are negatively correlated in mammals, indicating that encephalization and fat storage are compensatory strategies to buffer against starvation. However, these two strategies can be combined if fat storage does not unduly hamper locomotor efficiency. We propose that human encephalization was made possible by a combination of stabilization of energy inputs and a redirection of energy from locomotion, growth and reproduction.

Metabolic costs of brain size evolution

Abstract In the ongoing discussion about brain evolution in vertebrates, the main interest has shifted from theories focusing on energy balance to theories proposing social or ecological benefits of enhanced intellect. With the availability of a wealth of new data on basal metabolic rate (BMR) and brain size and with the aid of reliable techniques of comparative analysis, we are able to show that in fact energetics is an issue in the maintenance of a relatively large brain, and that brain size is positively correlated with the BMR in mammals, controlling for body size effects. We conclude that attempts to explain brain size variation in different taxa must consider the ability to sustain the energy costs alongside cognitive benefits.

Endocranial volumes of primate species: scaling analyses using a comprehensive and reliable data set.

We present a compilation of endocranial volumes (ECV) for 176 non-human primate species based on individual data collected from 3813 museum specimens, at least 88% being wild-caught. In combination with body mass data from wild individuals, strong correlations between endocranial volume and body mass within taxonomic groups were found. Errors attributable to different techniques for measuring cranial capacity were negligible and unbiased. The overall slopes for regressions of log ECV on log body mass in primates are 0.773 for least-squares regression and 0.793 for reduced major axis regression. The least-squares slope is reduced to 0.565 when independent contrasts are substituted for species means (branch lengths from molecular studies). A common slope of 0.646 is obtained with logged species means when grade shifts between major groups are taken into account using ANCOVA. In addition to providing a comprehensive and reliable database for comparative analyses of primate brain size, we show that the scaling relationship between brain mass and ECV does not differ significantly from isometry in primates. We also demonstrate that ECV does not differ substantially between captive and wild samples of the same species. ECV may be a more reliable indicator of brain size than brain mass, because considerably larger samples can be collected to better represent the full range of intraspecific variation. We also provide support for the maternal energy hypothesis by showing that basal metabolic rate (BMR) and gestation period are both positively correlated with brain size in primates, after controlling for the influence of body mass and potential effects of phylogenetic relatedness.

Comparing adult hippocampal neurogenesis in mammalian species and orders: influence of chronological age and life history stage.

Adult hippocampal neurogenesis is a prominent event in rodents. In species with longer life expectancies, newly born cells in the adult dentate gyrus of the hippocampal formation are less abundant or can be completely absent. Several lines of evidence indicate that the regulatory mechanisms of adult neurogenesis differ between short‐ and long‐lived mammals. After a critical appraisal of the factors and problems associated with comparing different species, we provide a quantitative comparison derived from seven laboratory strains of mice (BALB, C57BL/6, CD1, outbred) and rats (F344, Sprague‐Dawley, Wistar), six other rodent species of which four are wild‐derived (wood mouse, vole, spiny mouse and guinea pig), three non‐human primate species (marmoset and two macaque species) and one carnivore (red fox). Normalizing the number of proliferating cells to total granule cell number, we observe an overall exponential decline in proliferation that is chronologically equal between species and orders and independent of early developmental processes and life span. Long‐ and short‐lived mammals differ with regard to major life history stages; at the time points of weaning, age at first reproduction and average life expectancy, long‐lived primates and foxes have significantly fewer proliferating cells than rodents. Although the database for neuronal differentiation is limited, we find indications that the extent of neuronal differentiation is subject to species‐specific selective adaptations. We conclude that absolute age is the critical factor regulating cell genesis in the adult hippocampus of mammals. Ontogenetic and ecological factors primarily influence the regulation of neuronal differentiation rather than the rate of cell proliferation.

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.

Why are there so few smart mammals (but so many smart birds)

The expensive brain hypothesis predicts an interspecific link between relative brain size and life-history pace. Indeed, animals with relatively large brains have reduced rates of growth and reproduction. However, they also have increased total lifespan. Here we show that the reduction in production with increasing brain size is not fully compensated by the increase in lifespan. Consequently, the maximum rate of population increase (rmax) is negatively correlated with brain mass. This result is not due to a confounding effect of body size, indicating that the well-known correlation between rmax and body size is driven by brain size, at least among homeothermic vertebrates. Thus, each lineage faces a ‘grey ceiling’, i.e. a maximum viable brain size, beyond which rmax is so low that the risk of local or species extinction is very high. We found that the steep decline in rmax with brain size is absent in taxa with allomaternal offspring provisioning, such as cooperatively breeding mammals and most altricial birds. These taxa thus do not face a lineage-specific grey ceiling, which explains the far greater number of independent origins of large brain size in birds than mammals. We also predict that (absolute and relative) brain size is an important predictor of macroevolutionary extinction patterns.

Explaining brain size variation: from social to cultural brain

Although the social brain hypothesis has found near-universal acceptance as the best explanation for the evolution of extensive variation in brain size among mammals, it faces two problems. First, it cannot account for grade shifts, where species or complete lineages have a very different brain size than expected based on their social organization. Second, it cannot account for the observation that species with high socio-cognitive abilities also excel in general cognition. These problems may be related. For birds and mammals, we propose to integrate the social brain hypothesis into a broader framework we call cultural intelligence, which stresses the importance of the high costs of brain tissue, general behavioral flexibility and the role of social learning in acquiring cognitive skills.

On Being Small: Brain Allometry in Ants

Comparative neurobiologists have provided ample evidence that in vertebrates small animals have proportionally larger brains: in a double-logarithmic plot of brain weight versus body weight all data points conform quite closely to a straight line with a slope of less than one. Hence vertebrate brains scale allometrically, rather than isometrically, with body size. Here we extend the phylogenetic scope of such studies and the size range of the brains under investigation to the insects, especially ants. We show that the principle of (negative) allometry applies as well, but that ants have considerably smaller brains than any ant-sized vertebrate would have, and that this result holds even if the relatively higher exoskeleton weights of ants (as compared to endoskeleton weights of mammals) are taken into account. Finally, interspecific comparisons within one genus of ants, Cataglyphis, show that species exhibiting small colony sizes (of a few hundred individuals) have significantly smaller brains than species in which colonies are composed of several thousand individuals.

Primate energy expenditure and life history

Significance Measurements of daily energy expenditure indicate that primates, including humans, expend only half of the calories expected for mammals of similar body size. As energy expenditure is central to organismal biology, these results hold important implications for life history, evolutionary biology, and foraging ecology for primates and other mammals. Specifically, we show that primates’ remarkably low metabolic rates account for their distinctively slow rates of growth, reproduction, and aging. Humans and other primates are distinct among placental mammals in having exceptionally slow rates of growth, reproduction, and aging. Primates’ slow life history schedules are generally thought to reflect an evolved strategy of allocating energy away from growth and reproduction and toward somatic investment, particularly to the development and maintenance of large brains. Here we examine an alternative explanation: that primates’ slow life histories reflect low total energy expenditure (TEE) (kilocalories per day) relative to other placental mammals. We compared doubly labeled water measurements of TEE among 17 primate species with similar measures for other placental mammals. We found that primates use remarkably little energy each day, expending on average only 50% of the energy expected for a placental mammal of similar mass. Such large differences in TEE are not easily explained by differences in physical activity, and instead appear to reflect systemic metabolic adaptation for low energy expenditures in primates. Indeed, comparisons of wild and captive primate populations indicate similar levels of energy expenditure. Broad interspecific comparisons of growth, reproduction, and maximum life span indicate that primates’ slow metabolic rates contribute to their characteristically slow life histories.