Adult Brain Size Research Articles

The evolution of human altriciality and brain development in comparative context.

Human newborns are considered altricial compared with other primates because they are relatively underdeveloped at birth. However, in a broader comparative context, other mammals are more altricial than humans. It has been proposed that altricial development evolved secondarily in humans due to obstetrical or metabolic constraints, and in association with increased brain plasticity. To explore this association, we used comparative data from 140 placental mammals to measure how altriciality evolved in humans and other species. We also estimated how changes in brain size and gestation length influenced the timing of neurodevelopment during hominin evolution. Based on our data, humans show the highest evolutionary rate to become more altricial (measured as the proportion of adult brain size at birth) across all placental mammals, but this results primarily from the pronounced postnatal enlargement of brain size rather than neonatal changes. In addition, we show that only a small number of neurodevelopmental events were shifted to the postnatal period during hominin evolution, and that they were primarily related to the myelination of certain brain pathways. These results indicate that the perception of human altriciality is mostly driven by postnatal changes, and they point to a possible association between the timing of myelination and human neuroplasticity.

Parental provisioning drives brain size in birds

Large brains support numerous cognitive adaptations and therefore may appear to be highly beneficial. Nonetheless, the high energetic costs of brain tissue may have prevented the evolution of large brains in many species. This problem may also have a developmental dimension: juveniles, with their immature and therefore poorly performing brains, would face a major energetic hurdle if they were to pay for the construction of their own brain, especially in larger-brained species. Here, we explore the possible role of parental provisioning for the development and evolution of adult brain size in birds. A comparative analysis of 1,176 bird species shows that various measures of parental provisioning (precocial vs. altricial state at hatching, relative egg mass, time spent provisioning the young) strongly predict relative brain size across species. The parental provisioning hypothesis also provides an explanation for the well-documented but so far unexplained pattern that altricial birds have larger brains than precocial ones. We therefore conclude that the evolution of parental provisioning allowed species to overcome the seemingly insurmountable energetic constraint on growing large brains, which in turn enabled bird species to increase survival and population stability. Because including adult eco- and socio-cognitive predictors only marginally improved the explanatory value of our models, these findings also suggest that the traditionally assessed cognitive abilities largely support successful parental provisioning. Our results therefore indicate that the cognitive adaptations underlying successful parental provisioning also provide the behavioral flexibility facilitating reproductive success and survival.

Large-brained birds lay smaller but heavier clutches

The brain is among the most energetically costly organs in vertebrates, and thus trade-offs have been hypothesized to exert constraints on brain size evolution. The energy trade-off hypothesis (ETH) predicts that reducing the energy consumption of reproduction or other costly tissues should compensate for the cost of a large brain. Egg production in birds requires a large proportion of the total energy budget, and a clutch mass in some bird species can outweigh the body mass of the female. To date, this hypothesis has mainly been tested in mammals and ectothermic animals such as anurans and fishes. We collated data on adult brain size, body mass and egg-production traits such as clutch size, egg mass and annual broods from published studies, and conducted a phylogenetic comparative test of the interplay between egg-production investment and brain size evolution across bird species. After controlling for phylogenetic relationships and body size, we find a negative correlation between brain size and clutch size across 1395 species, which favored ETH. However, when egg mass was integrated in models, positive associations were detected between brain size and mass of eggs (via egg mass, clutch mass and annual total egg mass). Our results suggest that brain size trades off against egg-production only via certain aspects (e.g., clutch size). By contrast, a positive relationship between brain size and total egg reproduction (e.g., clutch mass and annual total egg mass) implied increased total energy budget outweighing energy allocation across bird species. Our study shows that there is no general energy trade-off between brain size and egg-reproduction investment, and suggests that brain size evolution follows mixed strategies across bird species.

Postnatal endocranial volume growth in Galago moholi

Our current knowledge of brain growth in non‐human primates is based on comparisons of brain weights in cadaveric newborns compared to adults. Previous work has revealed most strepsirrhine primates (e.g., lemurs and lorises) defer much of their brain growth to the postnatal timeframe. No studies have examined brain growth across postnatal ages, to determine when adult brain size is achieved relative to life history milestones such as weaning or eruption of adult dentition. Micro‐computed tomography via a Scano vivaCT 75 was utilized to scan six specimens, ranging from newborn (day 0) to adult. Amira software was then used to manually segment endocranial contours and generate endocranial volumes from each of the specimens. Preliminary data indicates that the neonatal Galago possesses roughly 44% of the endocranial volume of its adult counterpart. By the late infant stage (30 days), the Galago possesses roughly 70%, and by 60 days postnatal, 99% of the adult endocranial volume. This timeline precedes the weaning period seen at roughly 90 days. Other milestones are also reached at the same age. Galago is reported to be perfecting its signature leaps at 60 days, and in our sample, more than half of replacement teeth have erupted. Results do suggest that Galago, like other strepsirrhines, defers most brain growth to postnatal ages. But here, for the first time, we demonstrate a rapid increase in endocranial volume, well before complete feeding independence.

Growth and development of trabecular structure in the calcaneus of Japanese macaques (Macaca fuscata) reflects locomotor behavior, life history, and neuromuscular development.

Bone structure dynamically adapts to its mechanical environment throughout ontogeny by altering the structure of trabecular bone, the three‐dimensional mesh‐like structure found underneath joint surfaces. Trabecular structure, then, can provide a record of variation in loading directions and magnitude; and in ontogenetic samples, it can potentially be used to track developmental shifts in limb posture. We aim to broaden the analysis of trabecular bone ontogeny by incorporating interactions between ontogenetic variation in locomotor repertoire, neuromuscular maturation, and life history. We examine the associations between these variables and age‐related variation in trabecular structure in the calcaneus of Japanese macaques (Macaca fuscata). We used high‐resolution micro‐computed tomography scanning to image the calcaneus in a cross‐sectional sample of 34 juvenile M. fuscata aged between 0 and 7 years old at the Primate Research Institute, Japan. We calculated whole bone averages of standard trabecular properties and generated whole‐bone morphometric maps of bone volume fraction and Young’s modulus. Trabecular structure becomes increasingly heterogeneous in older individuals. Bone volume fraction (BV/total volume [TV]) decreases during the first month of life and increases afterward, coinciding with the onset of independent locomotion in M. fuscata. At birth, primary Young’s modulus is oriented orthogonal to the ossification center, but after locomotor onset bone structure becomes stiffest in the direction of joint surfaces and muscle attachments. Age‐related variation in bone volume fraction is best predicted by an interaction between the estimated percentage of adult brain size, body mass, and locomotor onset. To explain our findings, we propose a model where interactions between age‐related increases in body weight and maturation of the neuromuscular system alter the loading environment of the calcaneus, to which the internal trabecular structure dynamically adapts. This model cannot be directly tested based on our cross‐sectional data. However, confirmation of the model by longitudinal experiments and in multiple species would show that trabecular structure can be used both to infer behavior from fossil morphology and serve as a valuable proxy for neuromuscular maturation and life history events like locomotor onset and the achievement of an adult‐like gait. This approach could significantly expand our knowledge of the biology and behavior of fossil species.

Decoupling Sleep and Brain Size in Childhood: An Investigation of Genetic Covariation in the Adolescent Brain Cognitive Development Study

BackgroundChildhood sleep problems are common and among the most frequent and impairing comorbidities of childhood psychiatric disorders. In adults, sleep disturbances are heritable and show strong genetic associations with brain morphology; however, little is known about the genetic architecture of childhood sleep and potential etiological links between sleep, brain development, and pediatric-onset psychiatric symptoms. MethodsUsing data from the Adolescent Brain Cognitive Development Study (nPhenotype = 4428 for discovery/replication, nGenetics = 4728; age 9–10 years), we assessed phenotypic relationships, heritability, and genetic correlations between childhood sleep disturbances (insomnia, arousal, breathing, somnolence, hyperhidrosis, sleep-wake transitions), brain size (surface area, cortical thickness, volume), and dimensional psychopathology. ResultsSleep disturbances showed widespread positive associations with multiple domains of childhood psychopathology; however, only insomnia showed replicable associations with smaller brain surface area. Among the sleep disturbances assessed, only insomnia showed significant heritability (h2SNP = 0.15, p < .05) and showed substantial genetic correlations with externalizing and attention-deficit/hyperactivity disorder symptomatology (rGs > 0.80, ps < .05). We found no evidence of genetic correlation between childhood insomnia and brain size. Furthermore, polygenic risk scores calculated from genome-wide association studies of adult insomnia and adult brain size did not predict childhood insomnia; instead, polygenic risk scores trained using attention-deficit/hyperactivity disorder genome-wide association studies predicted decreased surface area at baseline as well as insomnia and externalizing symptoms longitudinally. ConclusionsFindings demonstrate a distinct genetic architecture underlying childhood insomnia and brain size and suggest genetic overlap between childhood insomnia and attention-deficit/hyperactivity disorder symptomatology. Additional research is needed to examine how genetic risk manifests in altered developmental trajectories and comorbid sleep/psychiatric symptoms across adolescence.

Revised estimates of Taung’s brain size growth

Cranial capacity, a proxy for the volume of the brain and associated cranial contents, is an important yardstick used to compare early hominin species because increasing brain size is a key characteristic of our lineage. In 1925, Raymond Dart claimed that a natural endocast found at the Buxton Limeworks near Taung, South Africa (which he named Australopithecus africanus), showed signs of neural reorganisation, but its juvenile status complicated comparison to other hominoid species. In an attempt to put its brain size and reorganisation into a comparative context, subsequent researchers have tried to estimate Taung’s adult cranial capacity by comparison to coarse-grained hominoid growth data. In this study, we simulated brain growth in A. africanus using asymptotic growth models in known-age mountain gorillas, chimpanzees and modern humans, and show that, at just under 4 years old, Taung’s brain had already finished or nearly finished growing according to hominoid developmental schedules. Percentage-growth remaining estimates are lower here than in previous studies using cross-sectional ontogenetic samples of unknown chronological age. Our new adult estimates (between 404 cm3 and 430 cm3 overall and 405–406 cm3 for chimpanzee models) are smaller than previous estimates with a ‘starting’ cranial capacity of 404 cm3, supporting the hypothesis that Taung’s adult brain size would have fallen toward the lower end of the A. africanus range of variation and strengthening the case that Taung was female.&#x0D; Significance:&#x0D; &#x0D; This is one of several recent studies to show that brain growth is completed in African apes and humans earlier than previously appreciated.&#x0D; New adult cranial capacity estimates for Taung are lower than previous estimates, supporting the hypothesis that Taung was female.&#x0D; Cessation of brain growth in hominoids at earlier ages than previously reported suggests that adult cranial capacities for hominin juvenile specimens have been overestimated.&#x0D; &#x0D; Open data set:&#x0D; http://dx.doi.org/10.17632/wyfvwd4s22

The &amp;lt;italic&amp;gt;Australopithecus&amp;lt;/italic&amp;gt; Taun child skull: A fossil that changed human evolution history

The &amp;lt;italic&amp;gt;Australopithecus&amp;lt;/italic&amp;gt; Taun child skull: A fossil that changed human evolution history

Brain size growth in Australopithecus

Postnatal growth is one of the proximate means by which humans attain massive adult brain size. Humans are characterized by the maintenance of prenatal brain growth rates into the first postnatal year, as well as an overall extended period of growth. The evolution of this pattern is difficult to assess due to its relatively brief duration and the underrepresentation of well-preserved fossil individuals who died during this short period. In this study, I use Monte Carlo methods to reconstruct postnatal brain growth rates in Australopithecus afarensis and Australopithecus africanus, based on estimates of neonatal brain size and of likely brain size and age at death of infant specimens (A.L. 333-105, DIK-1-1, and Taung). Neonatal brain size is reconstructed from the empirical scaling relationship among catarrhines which humans follow, and conservative estimates of fossils' chronological ages and brain sizes are drawn from the literature. Simulated distributions of these values are used to calculate average annual rates (ARs) of brain growth and proportional size change from birth (PSC), which are compared to resampled statistics from humans, chimpanzees and gorillas of known age and sex. Simulated ARs and PSCs for A. afarensis are significantly lower than those of chimpanzees and gorillas. Both ARs and PSCs for A. africanus are similar to chimpanzee and gorilla values. These results indicate that although these early hominins were derived in some aspects of brain anatomy, high rates of brain growth did not appear until later in human evolution. Moreover, findings also imply that brain growth rates are not a simple function of adult brain size. This study provides important new information about the evolution of brain growth, despite limitations inherent in fossil samples.

Mammalian brain development and our grandmothering life history

Among mammals, including humans, adult brain size and the relative size of brain components depend precisely on the duration of a highly regular process of neural development. Much wider variation is seen in rates of body growth and the state of neural maturation at life history events like birth and weaning. Large brains result from slow maturation, which in humans is accompanied by weaning early with respect to both neural maturation and longevity. The grandmother hypothesis proposes this distinctive combination of life history features evolved as ancestral populations began to depend on foods that just weaned juveniles couldn't handle. Here we trace possible reciprocal connections between brain development and life history, highlighting the resulting extended neural plasticity in a wider cognitive ecology of allomaternal care that distinguishes human ontogeny with consequences for other peculiarities of our lineage.

Comment on "The growth pattern of Neandertals, reconstructed from a juvenile skeleton from El Sidrón (Spain)".

Rosas et al (Reports, 22 September 2017, p. 1282) calculate El Sidrón J1 to have reached only 87.5% of its adult brain size. This finding is based on an overestimation of Neandertal brain size. Pairwise comparisons with a larger sample of Neandertal fossils reveal that it is unlikely that the brain of El Sidrón would have grown appreciably larger.

Minimal variation in eutherian brain growth rates during fetal neurogenesis.

A central question in the evolution of brain development is whether species differ in rates of brain growth during fetal neurogenesis. Studies of neonatal data have found allometric evidence for brain growth rate differences according to physiological variables such as relative metabolism and placental invasiveness, but these findings have not been tested against fetal data directly. Here, we measure rates of exponential brain growth acceleration in 10 eutherian mammals, two marsupials, and two birds. Eutherian brain acceleration exhibits minimal variation relative to body and visceral organ growth, varies independently of correlated growth patterns in other organs, and is unrelated to proposed physiological constraints such as metabolic rate or placental invasiveness. Brain growth rates in two birds overlap with eutherian variation, while marsupial brain growth is exceptionally slow. Peak brain growth velocity is linked in time with forebrain myelination and eye opening, reliably separates altricial species born before it from precocial species born afterwards, and is an excellent predictor of adult brain size (r2 = 0.98). Species with faster body growth exhibit larger relative brain size in early ontogeny, while brain growth is unrelated to allometric measures. These findings indicate a surprising conservation of brain growth rates during fetal neurogenesis in eutherian mammals, clarify sources of variation in neonatal brain size, and suggest that slow body growth rates cause species to be more encephalized at birth.

Increased juvenile predation is not associated with evolved differences in adult brain size in Trinidadian killifish (Rivulus hartii).

Vertebrates exhibit extensive variation in brain size. The long‐standing assumption is that this variation is driven by ecologically mediated selection. Recent work has shown that an increase in predator‐induced mortality is associated with evolved increases and decreases in brain size. Thus, the manner in which predators induce shifts in brain size remains unclear. Increased predation early in life is a key driver of many adult traits, including life‐history and behavioral traits. Such results foreshadow a connection between age‐specific mortality and selection on adult brain size. Trinidadian killifish, Rivulus hartii, are found in sites with and without guppies, Poecilia reticulata. The densities of Rivulus drop dramatically in sites with guppies because guppies prey upon juvenile Rivulus. Previous work has shown that guppy predation is associated with the evolution of adult life‐history traits in Rivulus. In this study, we compared second‐generation laboratory‐born Rivulus from sites with and without guppies for differences in brain size and associated trade‐offs between brain size and other components of fitness. Despite the large amount of existing research on the importance of early‐life events on the evolution of adult traits, and the role of predation on both behavior and brain size, we did not find an association between the presence of guppies and evolutionary shifts in Rivulus brain size. Such results argue that increased rates of juvenile mortality may not alter selection on adult brain size.

The genetic basis of natural variation in mushroom body size in Drosophila melanogaster.

Genetic variation in brain size may provide the basis for the evolution of the brain and complex behaviours. The genetic substrate and the selective pressures acting on brain size are poorly understood. Here we use the Drosophila Genetic Reference Panel to map polymorphic variants affecting natural variation in mushroom body morphology. We identify 139 genes and 39 transcription factors and confirm effects on development and adult plasticity. We show correlations between morphology and aggression, sleep and lifespan. We propose that natural variation in adult brain size is controlled by interaction of the environment with gene networks controlling development and plasticity.

Transition: changing old habits.

Transitioning patients from pediatric to adult care is an issue of increasing concern, especially when it involves children with chronic conditions that are congenital or complex.1 Care of these children often requires the special expertise of pediatric subspecialists in addition to ongoing primary care. Pediatric specialists and generalists anticipate that patients will age out of their care, yet many adult medicine practitioners do not feel comfortable assuming responsibility for young adults chronically ill with pediatric disorders. A growing array of strategies and interventions are being designed to facilitate this transition, yet they all may not be necessary. The conclusion that a transition to adult care is indicated is generally based on traditional age cutoffs rather than science. Although it would be a significant change, pediatric subspecialists could reframe their services as condition-specific rather than age-specific care and continue to provide care to their aging patients over the life course in conjunction with adult primary care physicians. There is no consensus on the appropriate upper age of pediatricians’ patients or when youths become adults. Adulthood is more a social construct than a developmental stage. It has no readily identifiable markers such as those that define puberty, the beginning of adolescence. As a socially defined stage of life, there exists great variability about who is considered legally an adult. Even the assumption of “adult” responsibilities, that is, responsibility for meeting one’s own basic needs, does not consistently signify adulthood, although perhaps success at that endeavor would count as being an adult. Imaging studies of the brain demonstrate that adult brain size, especially that of the frontal cortex, is attained between the … Address correspondence to Edward L. Schor, MD, The Lucile Packard Foundation for Children’s Health, 400 Hamilton Avenue, Suite 340, Palo Alto, CA 94301. E-mail: edward.schor{at}lpfch.org

Prenatal Exposure to Autism-Specific Maternal Autoantibodies Alters Proliferation of Cortical Neural Precursor Cells, Enlarges Brain, and Increases Neuronal Size in Adult Animals.

Autism spectrum disorders (ASDs) affect up to 1 in 68 children. Autism-specific autoantibodies directed against fetal brain proteins have been found exclusively in a subpopulation of mothers whose children were diagnosed with ASD or maternal autoantibody-related autism. We tested the impact of autoantibodies on brain development in mice by transferring human antigen-specific IgG directly into the cerebral ventricles of embryonic mice during cortical neurogenesis. We show that autoantibodies recognize radial glial cells during development. We also show that prenatal exposure to autism-specific maternal autoantibodies increased stem cell proliferation in the subventricular zone (SVZ) of the embryonic neocortex, increased adult brain size and weight, and increased the size of adult cortical neurons. We propose that prenatal exposure to autism-specific maternal autoantibodies directly affects radial glial cell development and presents a viable pathologic mechanism for the maternal autoantibody-related prenatal ASD risk factor.

Niche partitioning in sympatric Gorilla and Pan from Cameroon: implications for life history strategies and for reconstructing the evolution of hominin life history.

Factors influencing the hominoid life histories are poorly understood, and little is known about how ecological conditions modulate the pace of their development. Yet our limited understanding of these interactions underpins life history interpretations in extinct hominins. Here we determined the synchronisation of dental mineralization/eruption with brain size in a 20th century museum collection of sympatric Gorilla gorilla and Pan troglodytes from Central Cameroon. Using δ13C and δ15N of individuals’ hair, we assessed whether and how differences in diet and habitat use may have impacted on ape development. The results show that, overall, gorilla hair δ13C and δ15N values are more variable than those of chimpanzees, and that gorillas are consistently lower in δ13C and δ15N compared to chimpanzees. Within a restricted, isotopically-constrained area, gorilla brain development appears delayed relative to dental mineralization/eruption [or dental development is accelerated relative to brains]: only about 87.8% of adult brain size is attained by the time first permanent molars come into occlusion, whereas it is 92.3% in chimpanzees. Even when M1s are already in full functional occlusion, gorilla brains lag behind those of chimpanzee (91% versus 96.4%), relative to tooth development. Both bootstrap analyses and stable isotope results confirm that these results are unlikely due to sampling error. Rather, δ15N values imply that gorillas are not fully weaned (physiologically mature) until well after M1 are in full functional occlusion. In chimpanzees the transition from infant to adult feeding appears (a) more gradual and (b) earlier relative to somatic development. Taken together, the findings are consistent with life history theory that predicts delayed development when non-density dependent mortality is low, i.e. in closed habitats, and with the “risk aversion” hypothesis for frugivorous species as a means to avert starvation. Furthermore, the results highlight the complexity and plasticity of hominoid/hominin development.

Modeling Transformations of Neurodevelopmental Sequences across Mammalian Species

A general model of neural development is derived to fit 18 mammalian species, including humans, macaques, several rodent species, and six metatherian (marsupial) mammals. The goal of this work is to describe heterochronic changes in brain evolution within its basic developmental allometry, and provide an empirical basis to recognize equivalent maturational states across animals. The empirical data generating the model comprises 271 developmental events, including measures of initial neurogenesis, axon extension, establishment, and refinement of connectivity, as well as later events such as myelin formation, growth of brain volume, and early behavioral milestones, to the third year of human postnatal life. The progress of neural events across species is sufficiently predictable that a single model can be used to predict the timing of all events in all species, with a correlation of modeled values to empirical data of 0.9929. Each species' rate of progress through the event scale, described by a regression equation predicting duration of development in days, is highly correlated with adult brain size. Neural heterochrony can be seen in selective delay of retinogenesis in the cat, associated with greater numbers of rods in its retina, and delay of corticogenesis in all species but rodents and the rabbit, associated with relatively larger cortices in species with delay. Unexpectedly, precocial mammals (those unusually mature at birth) delay the onset of first neurogenesis but then progress rapidly through remaining developmental events.

Maternal-fetal unit interactions and eutherian neocortical development and evolution

The conserved brain design that primates inherited from early mammals differs from the variable adult brain size and species-specific brain dominances observed across mammals. This variability relies on the emergence of specialized cerebral cortical regions and sub-compartments, triggering an increase in brain size, areal interconnectivity and histological complexity that ultimately lies on the activation of developmental programs. Structural placental features are not well correlated with brain enlargement; however, several endocrine pathways could be tuned with the activation of neuronal progenitors in the proliferative neocortical compartments. In this article, we reviewed some mechanisms of eutherians maternal–fetal unit interactions associated with brain development and evolution. We propose a hypothesis of brain evolution where proliferative compartments in primates become activated by “non-classical” endocrine placental signals participating in different steps of corticogenesis. Changes in the inner placental structure, along with placenta endocrine stimuli over the cortical proliferative activity would allow mammalian brain enlargement with a concomitant shorter gestation span, as an evolutionary strategy to escape from parent-offspring conflict.

How to explain the unusually late age at skill competence among humans

Humans stand out among primates and other mammals in reaching adult-level foraging skills very late in development, well after the onset of reproduction. The aim of this paper is to place this unusual human skill development into a broader comparative context. Among birds and mammals in general, duration of immaturity, indexed by age at first reproduction (AFR), and adult brain size have undergone correlated evolution. This pattern is consistent with two causal processes: AFR is either limited by the time needed to learn adult-level skills (needing to learn) or by the energy needed to grow brain and body to full size (energetic constraints). We tested predictions arising from these two hypotheses with data retrieved from the published literature for 57 mammal and bird species. First, most mammals reach adult-level foraging skills well before the developmental period is completed, implying that energy constraints determine the age at first reproduction, whereas most birds reach adult-level foraging skills around the time of maturity, suggesting time needed for skill acquisition determines the onset of reproduction. Second, within mammals we found that with increasing niche complexity, the age of adult-level skill competence moves closer to the age at first reproduction. Third, when looking at how adult-level skills can be reached later, we found that gregariousness, slow conservative development and post-weaning provisioning allow mammals to reach their skills later. Finally, in species with intense sharing of resources (such as cooperative hunters) competence in foraging skills may even reach peak values after age of first reproduction. We conclude that the human pattern of skill acquisition could arise because our hominin ancestors added cooperative breeding and hunting to the slow development they had as great apes with increasingly complex niches. This result provides a broad biological foundation for the embodied capital model.