Evolution of brain region volumes during artificial selection for relative brain size

The vertebrate brain shows an extremely conserved layout across taxa. Still, the relative sizes of separate brain regions vary markedly between species. One interesting pattern is that larger brains seem associated with increased relative sizes only of certain brain regions, for instance telencephalon and cerebellum. Till now, the evolutionary association between separate brain regions and overall brain size is based on comparative evidence and remains experimentally untested. Here, we test the evolutionary response of brain regions to directional selection on brain size in guppies (Poecilia reticulata) selected for large and small relative brain size. In these animals, artificial selection led to a fast response in relative brain size, while body size remained unchanged. We use microcomputer tomography to investigate how the volumes of 11 main brain regions respond to selection for larger versus smaller brains. We found no differences in relative brain region volumes between large‐ and small‐brained animals and only minor sex‐specific variation. Also, selection did not change allometric scaling between brain and brain region sizes. Our results suggest that brain regions respond similarly to strong directional selection on relative brain size, which indicates that brain anatomy variation in contemporary species most likely stem from direct selection on key regions.     

The allometric approach to species differences in brain size

Allometric methods can be used to test quantitative theories of the relationship between brain size and body size across species, and to search for ecological, behavioural, life history, and ontogenetic correlates of brain size. Brain size scales with an allometric exponent of around 0.75 against body size across mammals, but is closer to 0.56 for birds and for reptiles. The slope of the allometric line often varies depending upon the taxonomic level of analysis. However, this phenomenon, at least in mammals, may be a statistical artifact. Brain size for a given body size (relative brain size) varies among orders in birds and mammals, and some dietary associations with relative brain size have been found in particular taxa. Developmental status at birth is the most consistent correlate of relative brain size: precocial neonates have larger brains for a given maternal size than altricial neonates in both birds and mammals. Altricial neonates, however, have more brain growth following birth, and in birds also have larger relative adult brain sizes. Energetic explanations for differences in neonatal brain growth, although attractive on theoretical grounds, have largely failed to stand up to empirical tests.     

Incisor size and diet revisited: The view from a platyrrhine perspective

Allometric relationships between incisor size and body size were determined for 26 species of New World primates. While previous studies have suggested that the incisors of Old World primates, and anthropoids in general, scale isometrically with body size, the data presented here indicate a negative allometric relationship between incisor size and body size among New World species. This negative allometry was exhibited by platyrrhines when either upper or lower incisor row length was regressed against body weight, and when either least-squares or bivariate principal axis equations were used. When upper incisor length was plotted against skull length, negative allometry could be sustained using both statistical techniques only when the full sample of 26 species was plotted. The choice of variables to represent incisor size and body size, and the choice of a statistical technique to effect the allometric equation, had a more pronounced impact on the location of individual species with regard to lines of best fit. Platyrrhines as a group have smaller incisors relative to body size than do catarrhines, regardless of diet. Among New World primates, small incisors represent a plausible primitive condition; species with relatively large incisors manifest a phyletic change associated with a dietary shift to foods that require increased incisal preparation. The opposite trend characterizes Old World primates. In spite of the taxonomic differences in relative incisor size between platyrrhine and catarrhine primates, inferences about diet derived from an allometric equation for all anthropoids should prove reliable as long as the species with unknown diet does not lie at the upper end of the body size range for platyrrhines or catarrhines.     

Relative brain size,stratification, and social structure in anthropoids

The relationships between relative brain size and both stratification and social structure were examined in a total of 82 species of anthropoids. The species were divided into a total of 42 congeneric groups which consisted of congeneric species with similar ecologies and social structures. The relative brain size (RBS) was calculated for each congeneric group in each superfamily, based on an allometric equation describing the relationship between brain weight and body weight for each superfamily. Among congeneric groups with a common category of diet, RBS was significantly greater for terrestrial groups than for arboreal groups, and for polygynous (i.e. multi-female) groups than for monogynous (single-female) groups. Furthermore, RBS was significantly and positively correlated with the size of the home range per individual for the Cercopithecoidea, and with troop size for frugivorous groups of the Ceboidea. The results obtained suggest that factors associated with terrestriality and polygyny have been involved in the increases in relative brain size of anthropoids.     

Evolution of brain–body allometry in Lake Tanganyika cichlids

Brain size is strongly associated with body size in all vertebrates. This relationship has been hypothesized to be an important constraint on adaptive brain size evolution. The essential assumption behind this idea is that static (i.e., within species) brain–body allometry has low ability to evolve. However, recent studies have reported mixed support for this view. Here, we examine brain–body static allometry in Lake Tanganyika cichlids using a phylogenetic comparative framework. We found considerable variation in the static allometric intercept, which explained the majority of variation in absolute and relative brain size. In contrast, the slope of the brain–body static allometry had relatively low variation, which explained less variation in absolute and relative brain size compared to the intercept and body size. Further examination of the tempo and mode of evolution of static allometric parameters confirmed these observations. Moreover, the estimated evolutionary parameters indicate that the limited observed variation in the static allometric slope could be a result of strong stabilizing selection. Overall, our findings suggest that the brain–body static allometric slope may represent an evolutionary constraint in Lake Tanganyika cichlids.     

Competition, niche specialization and the evolution of brain size in the genus Peromyscus

Previous studies of relative brain size in mammals have suggested an association with complex habitats and with low reproductive rate. In order to examine the causal relationships more thoroughly, a detailed examination of relative brain size variation in the genus Peromyscus was undertaken. Endocranial volumes were used to estimate brain weight for 32 species including 161 subspecies, and relative brain size calculated as the species deviation from the allometric relationship between brain and body size. The intrageneric allometric coefficient was higher than most values previously reported from low taxonomic levels, but intraspecific coefficients were generally lower than this.
Island species, and relict species isolated on mountain tops, which may be ecological 'islands', had consistently small relative brain sizes, but peninsular species were large brained. Among the remaining species there were significant correlations between litter size and relative brain size, and between the number of competitor species and relative brain size. Species with many competitor species have relatively large brains and small litters. It is concluded that the nature of the geographical distribution, the pattern of species formation and habitat complexity all influence relative brain size in existing forms.     

Intertemporal choice in lemurs

Different species vary in their ability to wait for delayed rewards in intertemporal choice tasks. Models of rate maximization account for part of this variation, but other factors such as social structure and feeding ecology seem to underly some species differences. Though studies have evaluated intertemporal choice in several primate species, including Old World monkeys, New World monkeys, and apes, prosimians have not been tested. This study investigated intertemporal choices in three species of lemur (black-and-white ruffed lemurs, Varecia variegata, red ruffed lemurs, Varecia rubra, and black lemurs, Eulemur macaco) to assess how they compare to other primate species and whether their choices are consistent with rate maximization. We offered lemurs a choice between two food items available immediately and six food items available after a delay. We found that by adjusting the delay to the larger reward, the lemurs were indifferent between the two options at a mean delay of 17 s, ranging from 9 to 25 s. These data are comparable to data collected from common marmosets (Callithrix jacchus). The lemur data were not consistent with models of rate maximization. The addition of lemurs to the list of species tested in these tasks will help uncover the role of life history and socio-ecological factors influencing intertemporal choices.     

Competition,niche specialization and the evolution of brain size in the genus Peromyscus

Previous studies of relative brain size in mammals have suggested an association with complex habitats and with low reproductive rate. In order to examine the causal relationships more thoroughly, a detailed examination of relative brain size variation in the genus Peromyscus was undertaken. Endocranial volumes were used to estimate brain weight for 32 species including 161 subspecies, and relative brain size calculated as the species deviation from the allometric relationship between brain and body size. The intrageneric allometric coefficient was higher than most values previously reported from low taxonomic levels, but intraspecific coefficients were generally lower than this. Island species, and relict species isolated on mountain tops, which may be ecological ‘islands’, had consistently small relative brain sizes, but peninsular species were large brained. Among the remaining species there were significant correlations between litter size and relative brain size, and between the number of competitor species and relative brain size. Species with many competitor species have relatively large brains and small litters. It is concluded that the nature of the geographical distribution, the pattern of species formation and habitat complexity all influence relative brain size in existing forms.     

Sociality, ecology, and relative brain size in lemurs

The social brain hypothesis proposes that haplorhine primates have evolved relatively large brains for their body size primarily as an adaptation for living in complex social groups. Studies that support this hypothesis have shown a strong relationship between relative brain size and group size in these taxa. Recent reports suggest that this pattern is unique to haplorhine primates; many nonprimate taxa do not show a relationship between group size and relative brain size. Rather, pairbonded social monogamy appears to be a better predictor of a large relative brain size in many nonprimate taxa. It has been suggested that haplorhine primates may have expanded the pairbonded relationship beyond simple dyads towards the evolution of complex social groups. We examined the relationship between group size, pairbonding, and relative brain size in a sample of 19 lemurs; strepsirrhine primates that last share a common ancestor with monkeys and apes approximately 75 Ma. First, we evaluated the social brain hypothesis, which predicts that species with larger social groups will have relatively larger brains. Secondly, we tested the pairbonded hypothesis, which predicts that species with a pairbonded social organization will have relatively larger brains than non-pairbonded species. We found no relationship between group size or pairbonding and relative brain size in lemurs. We conducted two further analyses to test for possible relationships between two nonsocial variables, activity pattern and diet, and relative brain size. Both diet and activity pattern are significantly associated with relative brain size in our sample. Specifically, frugivorous species have relatively larger brains than folivorous species, and cathemeral species have relatively larger brains than diurnal, but not nocturnal species. These findings highlight meaningful differences between Malagasy strepsirrhines and haplorhines, and between Malagasy strepsirrhines and nonprimate taxa, regarding the social and ecological factors associated with increases in relative brain size. The results suggest that factors such as foraging complexity and flexibility of activity patterns may have driven selection for increases in brain size in lemurs.     

Lack of support for Rensch's rule in an intraspecific test using red flour beetle (Tribolium castaneum) populations

Rensch's rule proposes a universal allometric scaling phenomenon across species where sexual size dimorphism (SSD) has evolved: in taxa with male‐biased dimorphism, degree of SSD should increase with overall body size, and in taxa with female‐biased dimorphism, degree of SSD should decrease with increasing average body size. Rensch's rule appears to hold widely across taxa where SSD is male‐biased, but not consistently when SSD is female‐biased. Furthermore, studies addressing this question within species are rare, so it remains unclear whether this rule applies at the intraspecific level. We assess body size and SSD within Tribolium castaneum (Herbst), a species where females are larger than males, using 21 populations derived from separate locations across the world, and maintained in isolated laboratory culture for at least 20 years. Body size, and hence SSD patterns, are highly susceptible to variations in temperature, diet quality and other environmental factors. Crucially, here we nullify interference of such confounds as all populations were maintained under identical conditions (similar densities, standard diet and exposed to identical temperature, relative humidity and photoperiod). We measured thirty beetles of each sex for all populations, and found body size variation across populations, and (as expected) female‐biased SSD in all populations. We test whether Rensch's rule holds for our populations, but find isometry, i.e. no allometry for SSD. Our results thus show that Rensch's rule does not hold across populations within this species. Our intraspecific test matches previous interspecific studies showing that Rensch's rule fails in species with female‐biased SSD.     

Skills,division of labour and economies of scale among Amazonian hunters and South Indian honey collectors

In foraging and other productive activities, individuals make choices regarding whether and with whom to cooperate, and in what capacities. The size and composition of cooperative groups can be understood as a self-organized outcome of these choices, which are made under local ecological and social constraints. This article describes a theoretical framework for explaining the size and composition of foraging groups based on three principles: (i) the sexual division of labour; (ii) the intergenerational division of labour; and (iii) economies of scale in production. We test predictions from the theory with data from two field contexts: Tsimane'' game hunters of lowland Bolivia, and Jenu Kuruba honey collectors of South India. In each case, we estimate the impacts of group size and individual group members'' effort on group success. We characterize differences in the skill requirements of different foraging activities and show that individuals participate more frequently in activities in which they are more efficient. We evaluate returns to scale across different resource types and observe higher returns at larger group sizes in foraging activities (such as hunting large game) that benefit from coordinated and complementary roles. These results inform us that the foraging group size and composition are guided by the motivated choice of individuals on the basis of relative efficiency, benefits of cooperation, opportunity costs and other social considerations.     

Ecogeographical and phylogenetic effects on craniofacial variation in macaques

The widespread and complex ecogeographical diversity of macaques may have caused adaptive morphological convergence among four phylogenetic subgroups, making their phylogenetic relationships unclear. We used geometric morphometrics and multivariate analyses to test the null hypothesis that craniofacial morphology does not vary with ecogeographical and phylogenetic factors. As predicted by Bergmann's rule, size was larger for the fascicularis and sinica groups in colder environments. No clear size cline was observed in the silenus and sylvanus groups. An allometric pattern was observed across macaques, indicating that as size increases, rounded faces become more elongated. However, the elevation was differentiated within each of the former two groups and between the silenus and sylvanus groups, and the slope decreased in each of the two northern species of the fascicularis group. All allometric changes resulted in the similar situation of the face being more rounded in animals inhabiting colder zones and/or in animals having a larger body size than that predicted from the overarching allometric pattern. For non‐allometric components, variations in prognathism were significantly correlated with dietary differences; variations in localized shape components in zygomatics and muzzles were significantly correlated with phylogenetic differences among the subgroups. The common allometric pattern was probably influenced directly or indirectly by climate‐related factors, which are pressures favoring a more rounded face in colder environments and/or a more elongated face in warmer environments. Allometric dissociation could have occurred several times in Macaca even within a subgroup because of their wide latitudinal distributions, critically impairing the taxonomic utility of craniofacial elongation. Am J Phys Anthropol 154:27–41, 2014. © 2014 Wiley Periodicals, Inc.     

Gill surface area provides a clue for the respiratory basis of brain size in the blacktip shark (Carcharhinus limbatus)

Brain size varies dramatically, both within and across species, and this variation is often believed to be the result of trade-offs between the cognitive benefits of having a large brain for a given body size and the energetic cost of sustaining neural tissue. One potential consequence of having a large brain is that organisms must also meet the associated high energetic demands. Thus, a key question is whether metabolic rate correlates with brain size. However, using metabolic rate to measure energetic demand yields a relatively instantaneous and dynamic measure of energy turnover, which is incompatible with the longer evolutionary timescale of changes in brain size within and across species. Morphological traits associated with oxygen consumption, specifically gill surface area, have been shown to be correlates of oxygen demand and energy use, and thus may serve as integrated correlates of these processes, allowing us to assess whether evolutionary changes in brain size correlate with changes in longer-term oxygen demand and energy use. We tested how brain size relates to gill surface area in the blacktip shark Carcharhinus limbatus. First, we examined whether the allometric slope of brain mass (i.e., the rate that brain mass changes with body mass) is lower than the allometric slope of gill surface area across ontogeny. Second, we tested whether gill surface area explains variation in brain mass, after accounting for the effects of body mass on brain mass. We found that brain mass and gill surface area both had positive allometric slopes, with larger individuals having both larger brains and larger gill surface areas compared to smaller individuals. However, the allometric slope of brain mass was lower than the allometric slope of gill surface area, consistent with our prediction that the allometric slope of gill surface area could pose an upper limit to the allometric slope of brain mass. Finally, after accounting for body mass, individuals with larger brains tended to have larger gill surface areas. Together, our results provide clues as to how fishes may evolve and maintain large brains despite their high energetic cost, suggesting that C. limbatus individuals with a large gill surface area for their body mass may be able to support a higher energetic turnover, and, in turn, a larger brain for their body mass.     

Allometry and prediction in hominoids: a solution to the problem of intervening variables.

To avoid misinterpretation of allometric exponents determined from interspecific allometric comparisons, specific conditions must be met with respect to the common reference variable. Body weight is considered to be the best general indication of overall size and is hence widely acknowledged to be the most suitable reference variable. However, because of the paucity of recorded body weights for museum specimens, various comparative studies have used other size indicators as intervening variables, although the allometric relationships to body size/weight were often unknown and possibly differed between species. Because of differences in the scaling properties of alternative intervening variables across the species investigated, conflicting conclusions may be drawn if different variables are chosen as substitutes for overall size. This is illustrated with two examples. In this study, series of skeletons with associated body weights of Gorilla, Pan, Pongo, and Homo were investigated. Both ontogenetic and static adult allometric relationships between several widely used reference variables and body weight were determined. Neither these variables nor additional estimators investigated in this study displayed allometric exponents and coefficients similar enough across species to justify direct interspecific comparison. To generate an alternative size estimator for both ontogenetic and static interspecific investigations, equations for combined sexes were derived to predict body weight from various long bone dimensions for individual hominoid species. From a total of 25 predictors, 12 prediction equations per species (six for nonadults and six for adults) were selected according to their relative suitability for reliable prediction of body weight. It is shown that the derived reference variable "predicted body weight" avoids problems of intervening variables, is valid for any interspecific ontogenetic and static allometric comparison, and displays less fluctuation in comparison to actual body weight.     

Sociality,ecology and developmental constraints predict variation in brain size across birds

Conflicting theories have been proposed to explain variation in relative brain size across the animal kingdom. Ecological theories argue that the cognitive demands of seasonal or unpredictable environments have selected for increases in relative brain size, whereas the ‘social brain hypothesis’ argues that social complexity is the primary driver of brain size evolution. Here, we use a comparative approach to test the relative importance of ecology (diet, foraging niche and migration), sociality (social bond, cooperative breeding and territoriality) and developmental mode in shaping brain size across 1886 bird species. Across all birds, we find a highly significant effect of developmental mode and foraging niche on brain size, suggesting that developmental constraints and selection for complex motor skills whilst foraging generally imposes important selection on brain size in birds. We also find effects of social bonding and territoriality on brain size, but the direction of these effects do not support the social brain hypothesis. At the same time, we find extensive heterogeneity among major avian clades in the relative importance of different variables, implying that the significance of particular ecological and social factors for driving brain size evolution is often clade- and context-specific. Overall, our results reveal the important and complex ways in which ecological and social selection pressures and developmental constraints shape brain size evolution across birds.     

Conspecific attraction and shelter selection in gregarious insects

During habitat selection, the presence of conspecifics can frequently drive a nonuniform distribution of animals across habitats of equivalent quality. In group-living species, subgroups of individuals might display mutual attraction while differing in their preferences for environmental resources. The final decision to settle requires individuals to integrate both environmental and social cues. This raises the question of the relative importance of sociality and resources preferences in determining habitat choice. In this study, we examined the interactive influence of conspecific attraction on individual resource preferences on refuge choice in groups of cockroaches. Shelters scaled to the sizes of nymphs and adult males were offered to groups of only nymphs and only males and to mixed groups. The choices of males were consistent across social conditions. Conversely, the preferences of nymphs shifted depending on the social context; the presence of males overrode the affinity nymphs had for scaled-size shelters. We developed a numerical model implementing parameters derived from these experiments to test whether the final spatial distribution of individuals originated from a differential attraction between nymphs and males that was associated with their relative body size. Finally, we propose a general framework for understanding how similar mechanisms can promote the skewed distribution of organisms at different spatial scales.     

DISTINCT EVOLUTIONARY PATTERNS OF BRAIN AND BODY SIZE DURING ADAPTIVE RADIATION

Morphological traits are often genetically and/or phenotypically correlated with each other and such covariation can have an important influence on the evolution of individual traits. The strong positive relationship between brain size and body size in vertebrates has attracted a lot of interest, and much debate has surrounded the study of the factors responsible for the allometric relationship between these two traits. Here, we use comparative analyses of the Tanganyikan cichlid adaptive radiation to investigate the patterns of evolution for brain size and body size separately. We found that body size exhibited recent bursts of rapid evolution, a pattern that is consistent with divergence linked to ecological specialization. Brain weight on the other hand, showed no bursts of divergence but rather evolved in a gradual manner. Our results thus show that even highly genetically correlated traits can present markedly different patterns of evolution, hence interpreting patterns of evolution of traits from correlations in extant taxa can be misleading. Furthermore, our results suggest, contrary to expectations from theory, that brain size does not play a key role during adaptive radiation.     

Social complexity and the fractal structure of group size in primate social evolution

Compared to most other mammals and birds, anthropoid primates have unusually complex societies characterised by bonded social groups. Among primates, this effect is encapsulated in the social brain hypothesis: the robust correlation between various indices of social complexity (social group size, grooming clique size, tactical behaviour, coalition formation) and brain size. Hitherto, this has always been interpreted as a simple, unitary relationship. Using data for five different indices of brain volume from four independent brain databases, we show that the distribution of group size plotted against brain size is best described as a set of four distinct, very narrowly defined grades which are unrelated to phylogeny. The allocation of genera to these grades is highly consistent across the different data sets and brain indices. We show that these grades correspond to the progressive evolution of bonded social groups. In addition, we show, for those species that live in multilevel social systems, that the typical sizes of the different grouping levels in each case coincide with different grades. This suggests that the grades correspond to demographic attractors that are especially stable. Using five different cognitive indices, we show that the grades correlate with increasing social cognitive skills, suggesting that the cognitive demands of managing group cohesion increase progressively across grades. We argue that the grades themselves represent glass ceilings on animals' capacity to maintain social and spatial coherence during foraging and that, in order to evolve more highly bonded groups, species have to be able to invest in costly forms of cognition.     

Cross-country relationships between life expectancy,intertemporal choice and age at first birth

Humans, like other animals, typically discount the value of delayed rewards relative to those available in the present. From an evolutionary perspective, prioritising immediate rewards is a predictable response to high local mortality rates, as is an acceleration of reproductive scheduling. In a sample of 46 countries, we explored the cross-country relationships between average life expectancy, intertemporal choice, and women's age at first birth. We find that, across countries, lower life expectancy is associated with both a smaller percentage of people willing to wait for a larger but delayed reward, as well as a younger age at first birth. These results, which hold when controlling for region and economic pressure (GDP-per capita), dovetail with findings at the individual level to suggest that life expectancy is an important ecological predictor of both intertemporal and reproductive decision-making.