Comparative analyses of evolutionary rates reveal different pathways to encephalization in bats, carnivorans, and primates

Abstract

Variation in relative brain size is commonly interpreted as the result of selection on neuronal capacity. However, this approach ignores that relative brain size is also linked to another highly adaptive variable: body size. Considering that one-way tradeoff mechanisms are unlikely to provide satisfactory evolutionary explanations, we introduce an analytical framework that describes and quantifies all possible evolutionary scenarios between two traits. To investigate the effects of body mass changes on the interpretation of relative brain size evolution, we analyze three mammalian orders that are expected to be subject to different selective pressures on body size due to differences in locomotor adaptation: bats (powered flight), primates (primarily arboreal), and carnivorans (primarily terrestrial). We quantify rates of brain and body mass changes along individual branches of phylogenetic trees using an adaptive peak model of evolution. We find that the magnitude and variance of the level of integration of brain and body mass rates, and the subsequent relative influence of either brain or body size evolution on the brainbody relationship, differ significantly between orders and subgroups within orders. Importantly, we find that variation in brain-body relationships was driven primarily by variability in body mass. Our approach allows a more detailed interpretation of correlated trait evolution and variation in the underlying evolutionary pathways. Results demonstrate that a principal focus on interpreting relative brain size evolution as selection on neuronal capacity confounds the effects of body mass changes, thereby hiding important aspects that may contribute to explaining animal diversity.L arge brains and advanced cognitive abilities distinguish modern humans from other species, including our closest primate relatives. Consequently, brain size evolution has attracted the attention of generations of scientists (1). However, the human brain is not the largest in absolute mass or volume, but only under consideration of our rather moderate body mass (2-4). Increased "intelligence" is generally attributed to a deviation from a taxonspecific allometric relationship between brain and body (1, 5-7) (Fig. 1). The main interest of studies in the past has thus been to understand which selective forces led to an increase in brain size relative to body size (8)(9)(10)(11)(12)(13)(14).Although the relationship between encephalization and intelligence is intuitive, it is not void of contention (5,6,15). Recent research on measures of "general intelligence" in primates has, for example, found more robust correlations with total brain mass than with encephalization (15). The complex relationship between brain mass, body mass, and intelligence has thus been the subject of considerable debate (5, 6, 16), partly because allometric slopes are taxon-specific (17-19). Regardless of these issues, deviations from the general allometric brain-body relationship continue to be commonly interpreted as a result of ecological, behavior...

A dynamic global equilibrium in carnivoran diversification over 20 million years

“…Recent analyses have resolved many outstanding questions of carnivoran phylogeny, including the monophyly of the aquatic pinnipeds (seals, sea lions and walruses), the sistergroup relationship of pinnipeds and musteloids (weasels, badgers and relatives), the monophyly of a clade containing hyenas, mongooses and the endemic carnivorans of Madagascar, and the polyphyly of the Viverridae (civets and gennets) [27][28][29]. Carnivorans have been used to document macroevolutionary patterns of character evolution and test hypotheses of underlying processes [25,26,[30][31][32][33]. However, knowledge of past diversification patterns for this otherwise well-studied group, and hence potential drivers of that diversity, remains limited.…”

Brain shape convergence in the adaptive radiation of New World monkeys

“…40 and 41). Using this measurement, we have a more structural encephalization definition, avoiding the use of body mass data, which can be subjected to different selective pressures to that experienced by brain size, affecting evolutionary interpretations (42).…”

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

“…principal component analysis [3,18]). Allometric approaches further fail to reveal the temporal origin and rate of evolutionary changes taking place on individual branches of the tree of life covered by the sample and confound the different evolutionary scenarios (in terms of patterns of increase/ decrease between two traits) that underlie allometric residuals [7]. Finally, comparative data on brain structures that are fundamental to neural processing ( prefrontal cortex, frontal motor areas and cerebellar lobules) have not been available until very recently [11,17,19 -21], hampering more in-depth insights on the systemic nature of mosaic brain evolution.…”

“…We address the questions above by combining novel phylogenetic comparative approaches [7,22] with recently collected data on volumes of cytoarchitectonically delineated brain structures (from post-mortem histologically sectioned brains) across species [11,17,[19][20][21]. The novel comparative approach we employ allows inferring the temporal origin, rate and process of evolutionary changes for all individual lineages of the tree of life covering the sample [7].…”

“…In primates, the evolution of brain size (both in terms of absolute size and relative to body size) shows complex patterns of change involving both increases and decreases along different branches of the primate phylogeny [6,7]. The importance of brain size (in association with size-related allometric scaling of individual brain structures) to species' adaptation is demonstrated by a comparative correlation between absolute brain size and cognitive ability in nonhuman primates [8] and between relative brain size and survival in novel environments in different orders across the animal kingdom [2,9,10].…”