Fallacies of progression in theories of brain-size evolution

The tacit assumption that relative enlargement and differentiation of brains reflect a progressive evolutionary trend toward greater intelligence is a major impediment to the study of brain evolution. Theories that purport to establish a linear scale for this presumed correlation between brain size and intelligence are undermined by the absence of an unbiased allometric baseline for estimating differences in encephalization, by the incompatibility of allometric analyses at different taxonomic levels, by the nonlinearity of the criterion of subtraction used to partition the somatic and cognitive components of encephalization, and by the failure to independently demonstrate any cognitive basis for the regularity of brain/body allometry. Analyzing deviations from brain/body allometric trends in terms of encephalization obfuscates the complementarity between brain and body size and ignores selection on body size, which probably determines most deviations. By failing to analyze the effects of allometry at many levels of structure, comparative anatomists have mistaken methodological artifacts for progressive evolutionary trends. Many structural changes, which are assumed to demonstrate progression of brain structure from primitive to advanced forms, are the results of allometric processes. Increased brain size turns out to have some previously unappreciated functional disadvantages.     

Special Issue ofHuman evolution on intelligence and evolutionary biology

This is a Special Issue on intelligence and evolutionary biology, based on selected lectures at a NATO Advanced Study Institute on this topic. The proceedings of the ASI have been published in a separate volume. The papers presented here have been reviewed and updated to reflect information available in 1988.     

Comparative analysis of encephalization in mammals reveals relaxed constraints on anthropoid primate and cetacean brain scaling

There is a well-established allometric relationship between brain and body mass in mammals. Deviation of relatively increased brain size from this pattern appears to coincide with enhanced cognitive abilities. To examine whether there is a phylogenetic structure to such episodes of changes in encephalization across mammals, we used phylogenetic techniques to analyse brain mass, body mass and encephalization quotient (EQ) among 630 extant mammalian species. Among all mammals, anthropoid primates and odontocete cetaceans have significantly greater variance in EQ, suggesting that evolutionary constraints that result in a strict correlation between brain and body mass have independently become relaxed. Moreover, ancestral state reconstructions of absolute brain mass, body mass and EQ revealed patterns of increase and decrease in EQ within anthropoid primates and cetaceans. We propose both neutral drift and selective factors may have played a role in the evolution of brain-body allometry.     

Trajectories and Constraints in Brain Evolution in Primates and Cetaceans

A negative allometric relationship between body mass (BM) and brain size (BS) can be observed for many vertebrate groups. In the past decades, researchers have proposed several hypotheses to explain this finding, but none is definitive and some are possibly not mutually exclusive. Certain species diverge markedly (positively or negatively) from the mean of the ratio BM/BS expected for a particular taxonomic group. It is possible to define encephalization quotient (EQ) as the ratio between the actual BS and the expected brain size. Several cetacean species show higher EQs compared to all primates, except modern humans. The process that led to big brains in primates and cetaceans produced different trajectories, as shown by the organizational differences observed in every encephalic district (e.g., the cortex). However, these two groups both convergently developed complex cognitive abilities. The comparative study on the trajectories through which the encephalization process has independently evolved in primates and cetaceans allows a critical appraisal of the causes, the time and the mode of quantitative and qualitative development of the brain in our species and in the hominid evolutionary lineage.     

Increased brain size in mammals is associated with size variations in gene families with cell signalling,chemotaxis and immune-related functions

Genomic determinants underlying increased encephalization across mammalian lineages are unknown. Whole genome comparisons have revealed large and frequent changes in the size of gene families, and it has been proposed that these variations could play a major role in shaping morphological and physiological differences among species. Using a genome-wide comparative approach, we examined changes in gene family size (GFS) and degree of encephalization in 39 fully sequenced mammalian species and found a significant over-representation of GFS variations in line with increased encephalization in mammals. We found that this relationship is not accounted for by known correlates of brain size such as maximum lifespan or body size and is not explained by phylogenetic relatedness. Genes involved in chemotaxis, immune regulation and cell signalling-related functions are significantly over-represented among those gene families most highly correlated with encephalization. Genes within these families are prominently expressed in the human brain, particularly the cortex, and organized in co-expression modules that display distinct temporal patterns of expression in the developing cortex. Our results suggest that changes in GFS associated with encephalization represent an evolutionary response to the specific functional requirements underlying increased brain size in mammals.     

What can dolphins tell us about primate evolution?

Fifty-five million years ago, a furry, hoofed mammal about the size of a dog ventured into the shallow brackish remnant of the Tethys Sea and set its descendants on a path that would lead to their complete abandonment of the land. These early ancestors of cetaceans (dolphins, porpoises, and whales) thereafter set on an evolutionary course that is arguably the most unusual of any mammal that ever lived. Primates and cetaceans, because of their adaptation to exclusively different physical environments, have had essentially nothing to do with each other throughout their evolution as distinct orders. In fact, the closest phylogenetic relatives of cetaceans are even-toed ungulates.     

Developmental patterns of chimpanzee cerebral tissues provide important clues for understanding the remarkable enlargement of the human brain

Developmental prolongation is thought to contribute to the remarkable brain enlargement observed in modern humans (Homo sapiens). However, the developmental trajectories of cerebral tissues have not been explored in chimpanzees (Pan troglodytes), even though they are our closest living relatives. To address this lack of information, the development of cerebral tissues was tracked in growing chimpanzees during infancy and the juvenile stage, using three-dimensional magnetic resonance imaging and compared with that of humans and rhesus macaques (Macaca mulatta). Overall, cerebral development in chimpanzees demonstrated less maturity and a more protracted course during prepuberty, as observed in humans but not in macaques. However, the rapid increase in cerebral total volume and proportional dynamic change in the cerebral tissue in humans during early infancy, when white matter volume increases dramatically, did not occur in chimpanzees. A dynamic reorganization of cerebral tissues of the brain during early infancy, driven mainly by enhancement of neuronal connectivity, is likely to have emerged in the human lineage after the split between humans and chimpanzees and to have promoted the increase in brain volume in humans. Our findings may lead to powerful insights into the ontogenetic mechanism underlying human brain enlargement.     

Brain evolution and development: adaptation,allometry and constraint

Phenotypic traits are products of two processes: evolution and development. But how do these processes combine to produce integrated phenotypes? Comparative studies identify consistent patterns of covariation, or allometries, between brain and body size, and between brain components, indicating the presence of significant constraints limiting independent evolution of separate parts. These constraints are poorly understood, but in principle could be either developmental or functional. The developmental constraints hypothesis suggests that individual components (brain and body size, or individual brain components) tend to evolve together because natural selection operates on relatively simple developmental mechanisms that affect the growth of all parts in a concerted manner. The functional constraints hypothesis suggests that correlated change reflects the action of selection on distributed functional systems connecting the different sub-components, predicting more complex patterns of mosaic change at the level of the functional systems and more complex genetic and developmental mechanisms. These hypotheses are not mutually exclusive but make different predictions. We review recent genetic and neurodevelopmental evidence, concluding that functional rather than developmental constraints are the main cause of the observed patterns.     

Mapping behavioural evolution onto brain evolution: the strategic roles of conserved organization in individuals and species

The pattern of individual variation in brain component structure in pigs, minks and laboratory mice is very similar to variation across species in the same components, at a reduced scale. This conserved pattern of allometric scaling resembles robotic architectures designed to be robust to changes in computing power and task demands, and may reflect the mechanism by which both growing and evolving brains defend basic sensory, motor and homeostatic functions at multiple scales. Conserved scaling rules also have implications for species-specific sensory and social communication systems, motor competencies and cognitive abilities. The role of relative changes in neuron number in the central nervous system in producing species-specific behaviour is thus highly constrained, while changes in the sensory and motor periphery, and in motivational and attentional systems increase in probability as the principal loci producing important changes in functional neuroanatomy between species. By their nature, these loci require renewed attention to development and life history in the initial organization and production of species-specific behavioural abilities.     

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.     

Evolution of life history parameters in animals with indeterminate growth,particularly fish

Summary Most evolutionary life history theory is developed in terms of the allocation of resources to the competing ends of growth, reproduction, and survivorship. In this paper we show that certain dimensionless numbers may be used to describe the relationship between growth, maturation, and adult mortality; our theory aims to predict these numbers and we are led to aggregate some basic features of life histories, rather than explicitly considering the allocation of a limited resource to different components of fitness. The phenomenology developed here has the convenient property that only parameters describing the shapes of two assumed trade-offs among life history traits appear in the solution of the resulting optimisation problem. Comparative inter- and intraspecific data on fish, lizard, snake and shrimp populations suggest that this approach may help explain some common patterns in the life histories of animals with indeterminate growth.     

Placental invasiveness and brain-body allometry in eutherian mammals

Brain growth is a key trait in the evolution of mammalian life history. Brain development should be mediated by placentation, which determines patterns of resource transfer from mothers to fetal offspring. Eutherian placentation varies in the extent to which a maternal barrier separates fetal tissues from maternal blood. We demonstrate here that more invasive forms of placentation are associated with substantially steeper brain-body allometry, faster prenatal brain growth and slower prenatal body growth. On the basis of the physiological literature we suggest a simple mechanism for these differences: in species with invasive placentation, where the placenta is bathed directly in maternal blood, fatty acids essential for brain development can be readily extracted by the fetus, but in species with less invasive placentation they must be synthesized by the fetus. Hence, with regard to brain-body allometry and prenatal growth patterns, eutherian mammals are structured into distinct groups differing in placental invasiveness.     

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.