Gregariousness increases brain size in ungulates

The brain’s main function is to organise the physiological and behavioural responses to environmental and social challenges in order to keep the organism alive. Here, we studied the effects that gregariousness (as a measurement of sociality), dietary habits, gestation length and sex have on brain size of extant ungulates. The analysis controlled for the effects of phylogeny and for random variability implicit in the data set. We tested the following groups of hypotheses: (1) Social brain hypothesis—gregarious species are more likely to have larger brains than non-gregarious species because the former are subjected to demanding and complex social interactions; (2) Ecological hypothesis—dietary habits impose challenging cognitive tasks associated with finding and manipulating food (foraging strategy); (3) Developmental hypotheses (a) energy strategy: selection for larger brains operates, primarily, on maternal metabolic turnover (i.e. gestation length) in relation to food quality because the majority of the brain’s growth takes place in utero, and finally (b) sex hypothesis: females are expected to have larger brains than males, relative to body size, because of the differential growth rates of the soma and brain between the sexes. We found that, after adjusting for body mass, gregariousness and gestation length explained most of the variation in brain mass across the ungulate species studied. Larger species had larger brains; gregarious species and those with longer gestation lengths, relative to body mass, had larger brains than non-gregarious species and those with shorter gestation lengths. The effect of diet was negligible and subrogated by gestation length, and sex had no significant effect on brain size. The ultimate cause that could have triggered the co-evolution between gestation length and brain size remains unclear.     

Thermogenic capacity of three species of fruit-eating phyllostomid bats

This study evaluated the thermogenic capacity of three species of fruit-eating phyllostomid bats (Carollia perspicillata, Sturnira lilium and Artibeus lituratus) during the dry-cool and wet-warm seasons, by measuring changes in body mass, basal metabolic rate (BMR), maximal metabolic rate (MMR), nonshivering thermogenesis and shivering thermogenesis. Body mass was lower, on average, during the dry-cool season and all species of fruit-eating bats showed an increase in oxygen consumption after noradrenaline injection and after exposure to a He-O₂ atmosphere. However, the magnitude of this increase was similar in both seasons. BMR also did not vary between seasons. Although, our results showed for the first time that all three species studied were able to increase thermogenesis by both nonshivering and shivering thermogenesis, we did not find significant differences in any thermoregulatory variable measured when comparing data from the two different seasons. Probably the difference in the mean and variance of the temperature profile between seasons were not strong enough to alter the thermogenic capacity of these species. Furthermore, the use of alternative physiological (torpor) or behavioral (huddling) strategies might have alleviated the need to trigger energetic-costly thermogenic responses.     

Are Megabats Big?

Traditionally, bats (Order Chiroptera) are divided into two suborders, Megachiroptera (“megabats”) and Microchiroptera, and this nomenclature suggests a consistent difference in body size. To test whether megabats are, in fact, significantly larger than other bats, we compared them with respect to average body mass (log transformed), using both conventional and phylogenetic statistics. Because bat phylogeny is controversial, including the position of megabats, we employed several analyses. First, we derived two generic-level topologies for 101 genera, one with megabats as the sister of all other bats (“morphological” tree), the other with megabats as the sister of one specific group of microbats, the Rhinolophoidea (“molecular” tree). Second, we used a recently published “supertree” that allowed us to analyze body mass data for 656 species. In addition, because the way body mass has evolved is generally unknown, we employed several sets of arbitrary branch lengths on both topologies, as well as transformations of the branches intended to mimic particular models of character evolution. Irrespective of the topology or branch lengths used, log body mass showed highly significant phylogenetic signal for both generic and species-level analyses (all P≤ 0.001). Conventional statistics indicated that megabats were indeed larger than other bats (P ? 0.001). Phylogenetic analyses supported this difference only when performed with certain branch lengths, thus demonstrating that careful consideration of the branch lengths used in a comparative analysis can enhance statistical power. A conventional Levene's test indicated that log body mass was more variable in megabats as compared with other bats (P=0.075 for generic-level data set, P ? 0.001 for species-level). A phylogenetic equivalent, which gauges the amount of morphospace occupied (or average minimum rate of evolution) relative to topology and branch lengths specified, indicated no significant difference for the generic analyses, but did indicate a difference for some of the species-level analyses. The ancestral bat is estimated to have been approximately 20–23 g in body mass (95% confidence interval approximately 9–51 g).     

Renal form and function in relation to the ecology of bats (Chiroptera)from Malawi, Central Africa

The ratio of the medulla to the cortex (M/C ratio) was determined for three species of Megachiroptera, and the ratio of the inner medulla to the cortex (IM/C ratio) was determined for 28 species of insect-eating Microchiroptera from diverse savanna and montane habitats within Malawi. Although all these species occur in the southern savanna biotic zone of Africa, each varies in its ability to exploit the African rainforest, arid and desert biotic zones. The kidneys of the Megachiroptera were very different to those of the insect-eating Microchiroptera, and these differences were related to the need of fruit-bats to excrete the surplus water associated with their diet. The urine concentrating capacity of each species of Microchiroptera was predicted from the IM/C ratio. Family characteristics were examined, and the urine concentrating capacities of the Malawian bats were compared with bats from elsewhere, and with some rodents. The insect- eating Microchiroptera exemplified a very diverse range of IM/C ratios. The IM/C ratio of each species was compared with its drinking behaviour in captivity, diet, foraging strategy, flight, aspect ratio, domicile, roosting behaviour and habitat. It was hypothesized that the ability of insect-eating Microchiroptera to conserve urinary water would be an advantage to species: (a) living in xeric habitats; (b) adapted for sustained high-speed flight; (c) roosting in hot dry domiciles; (d) roosting in solitude; and (e) living at high altitudes where seasonal low temperatures induce torpidity. These hypotheses were tested, and it was concluded that, while the ability to conserve urinary water may have been an advantage in most of these situations, it was not essential.     

Delphinid brain development from neonate to adulthood with comparisons to other cetaceans and artiodactyls

Why do neonatal and adult delphinids have much larger brains than artiodactyls when they have common ancestors? We explore relationships between neonatal brain size, gestation duration, maternal body mass, and body growth. Cetacean brains grow fast in the womb and longer gestation results in a larger brain. Allometry shows that the larger the mother's body mass, the larger the neonatal brain. After birth, delphinid bodies grow much faster than brains, and the index of encephalization decreases even as brains grow beyond maturity. Delphinids’ larger brain growth during life at sea may be explained by at least three differences from artiodactyls’ life on land. First, the sea offers high calorie prey to support growth of a large brain. Second, life in water offers relief from gravity, allowing for a large head to contain a large brain. Third, sound in water may pass through an immersed body. This allows sounds from the water to reach the fetus, driving early development of delphinoid auditory brain parts. As an example of this, the dolphin ear bone is very large at birth. Furthermore, the auditory nervous system appears mature well before birth. Compared with artiodactyls, these three differences likely result in a larger delphinid brain.     

Light enough to travel: migratory bats have smaller brains,but not larger hippocampi,than sedentary species

Migratory bird species have smaller brains than non-migratory species. The behavioural flexibility/migratory precursor hypothesis suggests that sedentary birds have larger brains to allow the behavioural flexibility required in a seasonally variable habitat. The energy trade-off hypothesis proposes that brains are heavy, energetically expensive and therefore, incompatible with migration. Here, we compared relative brain, neocortex and hippocampus volume between migratory and sedentary bats at the species-level and using phylogenetically independent contrasts. We found that migratory bats had relatively smaller brains and neocortices than sedentary species. Our results support the energy trade-off hypothesis because bats do not exhibit the same degree of flexibility in diet selection as sedentary birds. Our results also suggest that bat brain size differences are subtler than those found in birds, perhaps owing to bats'' shorter migration distances. Conversely, we found no difference in relative hippocampus volume between migratory and sedentary species, underscoring our limited understanding of the role of the hippocampus in bats.     

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.     

HOW MAMMALS PRODUCE LARGE-BRAINED OFFSPRING

Two explanations for species differences in neonatal brain size in eutherian mammals relate the size of the brain at birth to maternal metabolic rate. Martin (1981, 1983) argued that maternal basal metabolic rate puts an upper bound on the mother's ability to supply energy to the fetus, thereby limiting neonatal brain size. Hofman (1983) proposed that gestation length in mammals is constrained by maternal metabolic rate, implying an indirect constraint on neonatal brain size. Since individuals of precocial species have much larger neonatal brain sizes and are gestated longer for a given maternal body size than individuals of altricial species, Martin's and Hofman's ideas also require that mothers of precocial offspring have higher metabolic rates for their body sizes than mothers of altricial offspring. Data on 116 mammal species from 13 orders show that neither neonatal brain size nor gestation length is correlated with maternal metabolic rate when maternal body-size effects are removed. For a given maternal size, there is no difference in metabolic rates between precocial and altricial species, despite a two-fold difference between them in average neonatal brain size. However, neonatal brain size is strongly correlated with gestation length and litter size, independently of maternal size and metabolic rate. Analyses conducted within orders replicated the findings for gestation length and suggested that neonatal brain size may be at best only weakly related to metabolic rate. Differences in neonatal brain size appear to have evolved primarily with species differences in gestation length and litter size but not with differences in metabolic rate; large-brained offspring are typically produced from litters of one that have been gestated for a long time relative to maternal size. We conclude that species differences in relative neonatal brain size reflect different life-history tactics rather than constraints imposed by metabolic rate.     

Adaptation of brain regions to habitat complexity: a comparative analysis in bats (Chiroptera)

Vertebrate brains are organized in modules which process information from sensory inputs selectively. Therefore they are probably under different evolutionary pressures. We investigated the impact of environmental influences on specific brain centres in bats. We showed in a phylogenetically independent contrast analysis that the wing area of a species corrected for body size correlated with estimates of habitat complexity. We subsequently compared wing area, as an indirect measure of habitat complexity, with the size of regions associated with hearing, olfaction and spatial memory, while controlling for phylogeny and body mass. The inferior colliculi, the largest sub-cortical auditory centre, showed a strong positive correlation with wing area in echolocating bats. The size of the main olfactory bulb did not increase with wing area, suggesting that the need for olfaction may not increase during the localization of food and orientation in denser habitat. As expected, a larger wing area was linked to a larger hippocampus in all bats. Our results suggest that morphological adaptations related to flight and neuronal capabilities as reflected by the sizes of brain regions coevolved under similar ecological pressures. Thus, habitat complexity presumably influenced and shaped sensory abilities in this mammalian order independently of each other.     

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.     

Seed-mass effects in four Mediterranean Quercus species (Fagaceae) growing in contrasting light environments

Three hypotheses have been proposed to explain the functional relationship between seed mass and seedling performance: the reserve effect (larger seeds retain a larger proportion of reserves after germinating), the metabolic effect (seedlings from larger seeds have slower relative growth rates), and the seedling-size effect (larger seeds produce larger seedlings). We tested these hypotheses by growing four Mediterranean Quercus species under different light conditions (3, 27, and 100% of available radiation). We found evidence for two of the three hypotheses, but none of the four species complied with all three hypotheses at the same time. The reserve effect was not found in any species, the metabolic effect was found in three species (Q. ilex, Q. pyrenaica, and Q. suber), and the seedling-size effect in all species. Light availability significantly affected the relationships between seed size and seedling traits. For Q. ilex and Q. canariensis, a seedling-size effect was found under all three light conditions, but only under the lowest light (3%) for Q. suber and Q. pyrenaica. In all species, the correlation between seed mass and seedling mass increased with a decrease in light, suggesting that seedlings growing in low light depend more upon their seed reserves. A causal model integrates the three hypotheses, suggesting that larger seeds generally produced larger seedlings.     

THE EVOLUTIONARY HISTORY OF CETACEAN BRAIN AND BODY SIZE

Cetaceans rival primates in brain size relative to body size and include species with the largest brains and biggest bodies to have ever evolved. Cetaceans are remarkably diverse, varying in both phenotypes by several orders of magnitude, with notable differences between the two extant suborders, Mysticeti and Odontoceti. We analyzed the evolutionary history of brain and body mass, and relative brain size measured by the encephalization quotient (EQ), using a data set of extinct and extant taxa to capture temporal variation in the mode and direction of evolution. Our results suggest that cetacean brain and body mass evolved under strong directional trends to increase through time, but decreases in EQ were widespread. Mysticetes have significantly lower EQs than odontocetes due to a shift in brain:body allometry following the divergence of the suborders, caused by rapid increases in body mass in Mysticeti and a period of body mass reduction in Odontoceti. The pattern in Cetacea contrasts with that in primates, which experienced strong trends to increase brain mass and relative brain size, but not body mass. We discuss what these analyses reveal about the convergent evolution of large brains, and highlight that until recently the most encephalized mammals were odontocetes, not primates.     

Investment in higher order central processing regions is not constrained by brain size in social insects

The extent to which size constrains the evolution of brain organization and the genesis of complex behaviour is a central, unanswered question in evolutionary neuroscience. Advanced cognition has long been linked to the expansion of specific brain compartments, such as the neocortex in vertebrates and the mushroom bodies in insects. Scaling constraints that limit the size of these brain regions in small animals may therefore be particularly significant to behavioural evolution. Recent findings from studies of paper wasps suggest miniaturization constrains the size of central sensory processing brain centres (mushroom body calyces) in favour of peripheral, sensory input centres (antennal and optic lobes). We tested the generality of this hypothesis in diverse eusocial hymenopteran species (ants, bees and wasps) exhibiting striking variation in body size and thus brain size. Combining multiple neuroanatomical datasets from these three taxa, we found no universal size constraint on brain organization within or among species. In fact, small-bodied ants with miniscule brains had mushroom body calyces proportionally as large as or larger than those of wasps and bees with brains orders of magnitude larger. Our comparative analyses suggest that brain organization in ants is shaped more by natural selection imposed by visual demands than intrinsic design limitations.     

Larger brains spur species diversification in birds

Evidence is accumulating that species traits can spur their evolutionary diversification by influencing niche shifts, range expansions, and extinction risk. Previous work has shown that larger brains (relative to body size) facilitate niche shifts and range expansions by enhancing behavioral plasticity but whether larger brains also promote evolutionary diversification is currently backed by insufficient evidence. We addressed this gap by combining a brain size dataset for >1900 avian species worldwide with estimates of diversification rates based on two conceptually different phylogenetic‐based approaches. We found consistent evidence that lineages with larger brains (relative to body size) have diversified faster than lineages with relatively smaller brains. The best supported trait‐dependent model suggests that brain size primarily affects diversification rates by increasing speciation rather than decreasing extinction rates. In addition, we found that the effect of relatively brain size on species‐level diversification rate is additive to the effect of other intrinsic and extrinsic factors. Altogether, our results highlight the importance of brain size as an important factor in evolution and reinforce the view that intrinsic features of species have the potential to influence the pace of evolution.     

Metabolic correlates of hominid brain evolution

Large brain sizes in humans have important metabolic consequences as humans expend a relatively larger proportion of their resting energy budget on brain metabolism than other primates or non-primate mammals. The high costs of large human brains are supported, in part, by diets that are relatively rich in energy and other nutrients. Among living primates, the relative proportion of metabolic energy allocated to the brain is positively correlated with dietary quality. Humans fall at the positive end of this relationship, having both a very high quality diet and a large brain size. Greater encephalization also appears to have consequences for aspects of body composition. Comparative primate data indicate that humans are 'under-muscled', having relatively lower levels of skeletal muscle than other primate species of similar size. Conversely, levels of body fatness are relatively high in humans, particularly in infancy. These greater levels of body fatness and reduced levels of muscle mass allow human infants to accommodate the growth of their large brains in two important ways: (1) by having a ready supply of stored energy to 'feed the brain', when intake is limited and (2) by reducing the total energy costs of the rest of the body. Paleontological evidence indicates that the rapid brain evolution observed with the emergence of Homo erectus at approximately 1.8 million years ago was likely associated with important changes in diet and body composition.     

Nervous and sensory system correlates of an epibenthic evolutionary radiation in antarctic notothenioid fishes, genus Trematomus (Perciformes; Nototheniidae)

The perciform suborder Notothenioidei consists of 120 species, with 94 confined to the Antarctic Region of the Southern Ocean. On the Antarctic shelf, this phyletic radiation has been accompanied by a substantial morphological and ecological diversification towards a pelagic existence. For example, the primarily benthic genus Trematomus contains an epibenthic radiation that includes T. loennbergii, T. lepidorhinus, and T. eulepidotus. By comparing these epibenthic species with three congeneric benthic species (T. scotti, T. pennellii, and T. bernacchii) we tested three null hypotheses regarding brain variation in Antarctic trematomids: 1) that there is no difference in brain morphology among the six species; 2) that phylogenetic and ecological factors do not influence brain morphology; and 3) that peripheral sensory structures do not influence brain morphology. We rejected each of these hypotheses, leading us to conclude that Trematomus brains vary interspecifically, between benthic and epibenthic species, and with a species' depth distribution. Further, we conclude that brain variation is correlated with differences in peripheral sensory systems and motor activity. Specifically, epibenthic Trematomus have larger percentages of their brain volume devoted to lateral line mechanoreceptive and motor (cerebellar) structures. Species living at greater depths have low ratios of cones:rods in the retina and larger olfactory structures.     

Roles of Birds and Bats in Early Tropical-Forest Restoration

Restoration of tropical forest depended in large part on seed dispersal by fruit-eating animals that transported seeds into planted forest patches. We tested effectiveness of dispersal agents as revealed by established recruits of tree and shrub species that bore seeds dispersed by birds, bats, or both. We documented restoration of dispersal processes over the first 76 months of experimental restoration in southern Mexico. Mixed-model repeated-measures randomized-block ANOVAs of seedlings recruited into experimental controls and mixed-species plantings from late-secondary and mature forest indicated that bats and birds played different roles in the first years of a restoration process. Bats dispersed pioneer tree and shrub species to slowly regenerating grassy areas, while birds mediated recruitment of later-successional species into planted stands of trees and to a lesser extent into controls. Of species of pioneer trees and shrubs established in plots, seven were primarily dispersed by birds, three by bats and four by both birds and bats. Of later-successional species recruited past the seedling stage, 13 were of species primarily dispersed by birds, and six were of species dispersed by both birds and bats. No later-successional species primarily dispersed by bats established in control or planted plots. Establishment of recruited seedlings was ten-fold higher under cover of planted trees than in grassy controls. Even pre-reproductive trees drew fruit-eating birds and the seeds that they carried from nearby forest, and provided conditions for establishment of shade-tolerant tree species. Overall, after 76 months of cattle exclusion, 94% of the recruited shrubs and trees in experimental plots were of species that we did not plant.     

A phylogenetic supertree of the bats (Mammalia: Chiroptera)

We present the first estimate of the phylogenetic relationships among all 916 extant and nine recently extinct species of bats Mammalia: Chiroptera), a group that accounts for almost one-quarter of extant mammalian diversity. This phylogeny was derived by combining 105 estimates of bat phylogenetic relationships published since 1970 using the supertree construction technique of Matrix Representation with Parsimony (MRP). Despite the explosive growth in the number of phylogenetic studies of bats since 1990, phylogenetic relationships in the order have been studied non-randomly. For example, over one-third of all bat systematic studies to date have locused on relationships within Phyllostomidae, whereas relationships within clades such as Kerivoulinae and Murinae have never been studied using cladistic methods. Resolution in the supertree similarly differs among clades: overall resolution is poor (46.4%, of a fully bifurcating solution) but reaches 100% in some groups (e.g. relationships within Mormoopidae). The supertree analysis does not support a recent proposal that Microchiroptera is paraphyletic with respect to Megachiroptera, as the majority of source topologies support microbat monophyly. Although it is not a substitute for comprehensive phylogenetic analyses of primary molecular and morphological data, the bat supertree provides a useful tool for future phylogenetic comparative and macroevolutionary studies. Additionally, it identifies clades that have been little studied, highlights groups within which relationships are controversial, and like all phylogenetic studies, provides preliminary hypotheses that can form starting points for future phylogenetic studies of bats.     

Mating system and brain size in bats

The contribution of sexual selection to brain evolution has been little investigated. Through comparative analyses of bats, we show that multiple mating by males, in the absence of multiple mating by females, has no evolutionary impact on relative brain dimension. In contrast, bat species with promiscuous females have relatively smaller brains than do species with females exhibiting mate fidelity. This pattern may be a consequence of the demonstrated negative evolutionary relationship between investment in testes and investment in brains, both metabolically expensive tissues. These results have implications for understanding the correlated evolution of brains, behaviour and extravagant sexually selected traits.     

A phylogenetic analysis of sleep architecture in mammals: the integration of anatomy, physiology, and ecology

Among mammalian species, the time spent in the two main "architectural" states of sleep--slow-wave sleep (SWS) and rapid-eye-movement (REM) sleep--varies greatly. Previous comparative studies of sleep architecture found that larger mammals, those with bigger brains, and those with higher absolute basal metabolic rates (BMR) tended to engage in less SWS and REM sleep. Species experiencing a greater risk of predation also exhibited less SWS and REM sleep. In all cases, however, these studies lacked a formal phylogenetic and theoretical framework and used mainly correlational analyses. Using independent contrasts and an updated data set, we extended existing approaches with path analysis to examine the integrated influence of anatomy, physiology, and ecology on sleep architecture. Path model structure was determined by nonmutually exclusive hypotheses for the function of sleep. We found that species with higher relative BMRs engage in less SWS, whereas species with larger relative brain masses engage in more REM sleep. REM sleep was the only sleep variable strongly influenced by predation risk; mammals sleeping in riskier environments engage in less REM sleep. Overall, we found support for some hypotheses for the function of sleep, such as facilitating memory consolidation or learning, but not others, such as energy conservation.