Large Relative Brain Size Research Articles

Effects of short‐ and long‐term enrichment on brain and behavior in Trinidadian guppies

AbstractEnvironmental enrichment (EE) often increases positive behavioral and physiological effects on captive animals. Fish are commercially and scientifically important taxa that have been shown to benefit from EE. Here we examined the effects of both short‐ and long‐term EE in Trinidadian guppies (Poecilia reticulata). In the short‐term exposure to EE, female guppies were raised in standard conditions, and after reaching adulthood were moved to either an enriched or a deprived environment for 2 weeks. Long‐term exposure guppies were reared from birth for 12 weeks (until sexual maturity) in either an enriched or deprived environment. We then assessed growth, brain size, and neophobic and exploratory behaviors in standard assays. Guppies given EE were bolder, regardless of timescale, although females showed a more pronounced change in behaviors than males. We further found that guppies reared with EE were smaller yet had larger relative brain sizes than guppies reared under deprived conditions. Here we highlight that EE had influenced growth, brain size, neophobic, and exploratory behaviors in guppies, and behavioral changes were observed after only 2 weeks. Our results highlight the need for assessing the influences of EE in captivity, in particular for researchers studying cognition and behavior.

Seasonal variation of behavior and brain size in a freshwater fish.

Teleost fishes occupy a range of ecosystem, and habitat types subject to large seasonal fluctuations. Temperate fishes, in particular, survive large seasonal shifts in temperature, light availability, and access to certain habitats. Mobile species such as lake trout (Salvelinus namaycush) can behaviorally respond to seasonal variation by shifting their habitat deeper and further offshore in response to warmer surface water temperatures during the summer. During cooler seasons, the use of more structurally complex nearshore zones by lake trout could increase cognitive demands and potentially result in a larger relative brain size during those periods. Yet, there is limited understanding of how such behavioral responses to a seasonally shifting environment might shape, or be shaped by, the nervous system.Here, we quantified variation in relative brain size and the size of five externally visible brain regions in lake trout, across six consecutive seasons in two different lakes. Acoustic telemetry data from one of our study lakes were collected during the study period from a different subset of individuals and used to infer relationships between brain size and seasonal behaviors (habitat use and movement rate).Our results indicated that lake trout relative brain size was larger in the fall and winter compared with the spring and summer in both lakes. Larger brains coincided with increased use of nearshore habitats and increased horizontal movement rates in the fall and winter based on acoustic telemetry. The telencephalon followed the same pattern as whole brain size, while the other brain regions (cerebellum, optic tectum, olfactory bulbs, and hypothalamus) were only smaller in the spring.These findings provide evidence that flexibility in brain size could underpin shifts in behavior, which could potentially subserve functions associated with differential habitat use during cold and warm seasons and allow fish to succeed in seasonally variable environments.

Endocranial volume is variable and heritable, but not related to fitness, in a free-ranging primate

Large relative brain size is a defining characteristic of the order Primates. Arguably, this can be attributed to selection for behavioral aptitudes linked to a larger brain size. In order for selection of a trait to occur, the trait must vary, that variation must be heritable, and enhance fitness. In this study, we use a quantitative genetic approach to investigate the production and maintenance of variation in endocranial volume in a population of free-ranging rhesus macaques. We measured the endocranial volume and body mass proxies of 542 rhesus macaques from Cayo Santiago. We investigated variation in endocranial volume within and between sexes. Using a genetic pedigree, we estimated heritability of absolute and relative endocranial volume, and selection gradients of both traits as well as estimated body mass in the sample. Within this population, both absolute and relative endocranial volume display variation and sexual dimorphism. Both absolute and relative endocranial volume are highly heritable, but we found no evidence of selection on absolute or relative endocranial volume. These findings suggest that endocranial volume is not undergoing selection, or that we did not detect it because selection is neither linear nor quadratic, or that we lacked sufficient sample sizes to detect it.

The link between relative brain size and cognitive ageing in female guppies (Poecilia reticulata) artificially selected for variation in brain size.

Cognitive ageing is the general process when certain mental skills gradually deteriorate with age. Across species, there is a pattern of a slower brain structure degradation rate in large-brained species. Hence, having a larger brain might buffer the impact of cognitive ageing and positively affect survival at older age. However, few studies have investigated the link between relative brain size and cognitive ageing at the intraspecific level. In particular, experimental data on how brain size affects brain function also into higher age is largely missing. We used 288 female guppies (Poecilia reticulata), artificially selected for large and small relative brain size, to investigate variation in colour discrimination and behavioural flexibility, at 4-6, 12 and 24months of age. These ages are particularly interesting since they cover the life span from sexual maturation until maximal life length under natural conditions. We found no evidence for a slower cognitive ageing rate in large-brained females in neither initial colour discrimination nor reversal learning. Behavioural flexibility was predicted by large relative brain size in the youngest group, but the effect of brain size disappeared with increasing age. This result suggests that cognitive ageing rate is faster in large-brained female guppies, potentially due to the faster ageing and shorter lifespan in the large-brained selection lines. It also means that cognition levels align across different brain sizes with older age. We conclude that there are cognitive consequences of ageing that vary with relative brain size in advanced learning abilities, whereas fundamental aspects of learning can be maintained throughout the ecologically relevant life span.

Extended parenting and the evolution of cognition.

Traditional attempts to understand the evolution of human cognition compare humans with other primates. This research showed that relative brain size covaries with cognitive skills, while adaptations that buffer the developmental and energetic costs of large brains (e.g. allomaternal care), and ecological or social benefits of cognitive abilities, are critical for their evolution. To understand the drivers of cognitive adaptations, it is profitable to consider distant lineages with convergently evolved cognitions. Here, we examine the facilitators of cognitive evolution in corvid birds, where some species display cultural learning, with an emphasis on family life. We propose that extended parenting (protracted parent-offspring association) is pivotal in the evolution of cognition: it combines critical life-history, social and ecological conditions allowing for the development and maintenance of cognitive skillsets that confer fitness benefits to individuals. This novel hypothesis complements the extended childhood idea by considering the parents' role in juvenile development. Using phylogenetic comparative analyses, we show that corvids have larger body sizes, longer development times, extended parenting and larger relative brain sizes than other passerines. Case studies from two corvid species with different ecologies and social systems highlight the critical role of life-history features on juveniles' cognitive development: extended parenting provides a safe haven, access to tolerant role models, reliable learning opportunities and food, resulting in higher survival. The benefits of extended juvenile learning periods, over evolutionary time, lead to selection for expanded cognitive skillsets. Similarly, in our ancestors, cooperative breeding and increased group sizes facilitated learning and teaching. Our analyses highlight the critical role of life-history, ecological and social factors that underlie both extended parenting and expanded cognitive skillsets. This article is part of the theme issue 'Life history and learning: how childhood, caregiving and old age shape cognition and culture in humans and other animals'.

Brain Size and Life History Interact to Predict Urban Tolerance in Birds

Urbanization is a major driver of local biodiversity losses, but the traits that determine whether species are able to tolerate urban environments remain poorly understood. Theory suggests that a larger brain should provide higher tolerance to urbanization by enhancing behavioral flexibility to cope with novel challenges. However, assembling empirical evidence for a link between brain size and tolerance to urbanization has proven to be difficult, perhaps because the effect of the brain interacts with life history to influence persistence in urban environments. Here, we provide a global-scale assessment of the role of brain size on urban tolerance, combining quantitative estimations of urban tolerance with detailed information on brain size, life history and ecology for 629 avian species across 27 cities. Our analysis confirms the expected positive association between brain size and urban tolerance, but shows that the relationship is more complex than previously shown. While a large relative brain size generally increases urban tolerance, species with small brains can still attain high success in urban environments if they spread the risk of reproduction in multiple events (i.e. have a low brood value). These alternative strategies, although uncommon in natural conditions, seem to be favored in urban environments, fundamentally restructuring the composition of urban communities. Thus, our results support the notion that brain size mediates tolerance to urbanization, but also shows that there are alternative ways of exploiting urban environments. Our findings reconcile previous conflicting results regarding the effect of brain size on urban tolerance, and provide the basis for improved predictions of the responses of organisms to increasing urbanization over the coming decades.

Brain size does not predict learning strategies in a serial reversal learning test.

ABSTRACTReversal learning assays are commonly used across a wide range of taxa to investigate associative learning and behavioural flexibility. In serial reversal learning, the reward contingency in a binary discrimination is reversed multiple times. Performance during serial reversal learning varies greatly at the interspecific level, as some animals adopt a rule-based strategy that enables them to switch quickly between reward contingencies. A larger relative brain size, generating enhanced learning ability and increased behavioural flexibility, has been proposed to be an important factor underlying this variation. Here, we experimentally tested this hypothesis at the intraspecific level. We used guppies (Poecilia reticulata) artificially selected for small and large relative brain size, with matching differences in neuron number, in a serial reversal learning assay. We tested 96 individuals over 10 serial reversals and found that learning performance and memory were predicted by brain size, whereas differences in efficient learning strategies were not. We conclude that variation in brain size and neuron number is important for variation in learning performance and memory, but these differences are not great enough to cause the larger differences in efficient learning strategies observed at higher taxonomic levels.

Plastic changes in brain morphology in relation to learning and environmental enrichment in the guppy (Poecilia reticulata).

Despite the common assumption that the brain is malleable to surrounding conditions mainly during ontogeny, plastic neural changes can occur also in adulthood. One of the driving forces responsible for alterations in brain morphology is increasing environmental complexity that may demand enhanced cognitive abilities (e.g. attention, memory and learning). However, studies looking at the relationship between brain morphology and learning are scarce. Here, we tested the effects of both learning and environmental enrichment on neural plasticity in guppies (Poecilia reticulata), by means of either a reversal-learning test or a spatial-learning test. Given considerable evidence supporting environmentally induced plastic alterations, two separate control groups that were not subjected to any cognitive test were included to account for potential changes induced by the experimental setup alone. We did not find any effect of learning on any of our brain measurements. However, we found strong evidence for an environmental effect, where fish given access to the spatial-learning environment had larger relative brain size and optic tectum size in relation to those exposed to the reversal-learning environment. Our results demonstrate the plasticity of the adult brain to respond adaptively mainly to environmental conditions, providing support for the environmental enhancement theory.

Observation of tool use in striped skunks: how community science and social media help document rare natural phenomena

AbstractTool use, the manipulation of one object to change the state of another, is found in <1% of animal taxa and most often observed in captivity. Here, we report the observation of tentative tool use in a wild striped skunk (Mephitis mephitis), captured by a trail camera in the front yard of a hobby naturalist who shared the photographs on social media. The skunk is shown manipulating a rock in a manner that strongly suggests the goal of breaking the frozen surface of a water bowl to drink. Skunks join other carnivores that innovated tool use and proto‐tool use in the context of extractive foraging. Their versatile dexterity and manipulative foraging, likely facilitated by their large relative brain size, provide the ideal context for the innovation of novel foraging techniques. We therefore hypothesize that tool use will be observed in other members of the skunk family (Mephitidae), particularly as the broad availability of trail cameras, and the rapid dissemination of interesting observations via social media will increase the discovery rate of rare natural history phenomena. We encourage our colleagues to strengthen this pipeline to discovery, which reverses the information flow of community science projects, to bring amateur and professional naturalists closer together.

On the role of body size, brain size, and eye size in visual acuity

The visual system is highly variable across species, and such variability is a key factor influencing animal behavior. Variation in the visual system, for instance, can influence the outcome of learning tasks when visual stimuli are used. We illustrate this issue in guppies (Poecilia reticulata) artificially selected for large and small relative brain size with pronounced behavioral differences in learning experiments and mate choice tests. We performed a study of the visual system by quantifying eye size and optomotor response of large-brained and small-brained guppies. This represents the first experimental test of the link between brain size evolution and visual acuity. We found that female guppies have larger eyes than male guppies, both in absolute terms and in relation to their body size. Likewise, individuals selected for larger brains had slightly larger eyes but not better visual acuity than small-brained guppies. However, body size was positively associated with visual acuity. We discuss our findings in relation to previous macroevolutionary studies on the evolution of brain morphology, eye morphology, visual acuity, and ecological variables, while stressing the importance of accounting for sensory abilities in behavioral studies.Significance statementPre-existing perceptual biases can be keys for the development of specific behavioral patterns. Hence, potential differences in sensory systems need to be taken into account in the study of animal behavior. We highlight this necessity concentrating on the visual domain and using experimental data on brain size-selected guppies in which we assessed eye size and visual acuity. Behavioral differences between large-brained and small-brained guppies in learning and mate choice predominantly relied on tests using visual cues. Analyses of visual capabilities in this system are therefore necessary. Furthermore, this system offers the unprecedented opportunity to experimentally test the relationship between brain size, eye morphology, and visual capabilities. Our results show similar visual acuities between large-brained and small-brained guppies. However, the differences observed in eye area between the sexes, together with the observed positive relationship between body size and visual acuity, highlight the need to incorporate perceptive differences in the study of animal behavior.

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.

Big brains stabilize populations and facilitate colonization of variable habitats in birds.

The cognitive buffer hypothesis posits that environmental variability can be a major driver of the evolution of cognition because an enhanced ability to produce flexible behavioural responses facilitates coping with the unexpected. Although comparative evidence supports different aspects of this hypothesis, a direct connection between cognition and the ability to survive a variable and unpredictable environment has yet to be demonstrated. Here, we use complementary demographic and evolutionary analyses to show that among birds, the mechanistic premise of this hypothesis is well supported but the implied direction of causality is not. Specifically, we show that although population dynamics are more stable and less affected by environmental variation in birds with larger relative brain sizes, the evolution of larger brains often pre-dated and facilitated the colonization of variable habitats rather than the other way around. Our findings highlight the importance of investigating the timeline of evolutionary events when interpreting patterns of phylogenetic correlation.

Big Cat Coalitions: A Comparative Analysis of Regional Brain Volumes in Felidae.

Broad-based species comparisons across mammalian orders suggest a number of factors that might influence the evolution of large brains. However, the relationship between these factors and total and regional brain size remains unclear. This study investigated the relationship between relative brain size and regional brain volumes and sociality in 13 felid species in hopes of revealing relationships that are not detected in more inclusive comparative studies. In addition, a more detailed analysis was conducted of four focal species: lions (Panthera leo), leopards (Panthera pardus), cougars (Puma concolor), and cheetahs (Acinonyx jubatus). These species differ markedly in sociality and behavioral flexibility, factors hypothesized to contribute to increased relative brain size and/or frontal cortex size. Lions are the only truly social species, living in prides. Although cheetahs are largely solitary, males often form small groups. Both leopards and cougars are solitary. Of the four species, leopards exhibit the most behavioral flexibility, readily adapting to changing circumstances. Regional brain volumes were analyzed using computed tomography. Skulls (n = 75) were scanned to create three-dimensional virtual endocasts, and regional brain volumes were measured using either sulcal or bony landmarks obtained from the endocasts or skulls. Phylogenetic least squares regression analyses found that sociality does not correspond with larger relative brain size in these species. However, the sociality/solitary variable significantly predicted anterior cerebrum (AC) volume, a region that includes frontal cortex. This latter finding is despite the fact that the two social species in our sample, lions and cheetahs, possess the largest and smallest relative AC volumes, respectively. Additionally, an ANOVA comparing regional brain volumes in four focal species revealed that lions and leopards, while not significantly different from one another, have relatively larger AC volumes than are found in cheetahs or cougars. Further, female lions possess a significantly larger AC volume than conspecific males; female lion values were also larger than those of the other three species (regardless of sex). These results may reflect greater complexity in a female lion’s social world, but additional studies are necessary. These data suggest that within family comparisons may reveal variations not easily detected by broad comparative analyses.

Bigger brains may make better problem-solving carnivores.

Benson-Amram, Dantzer, Stricker, Swanson, & Holekamp's (Proceedings of the National Academy of Sciences, 113, 25321-25376, 2016) recent demonstration that larger-brained carnivores were more successful in a single problem-solving task, relative to smaller-brained carnivores, irrespective of social complexity, poses a challenge to proponents of the social intelligence hypothesis (Humphrey, 1976) and provides some support for the idea that larger relative brain sizes have evolved to support greater problem-solving abilities. However, an important question, neglected by the authors, is the extent to which foraging ecology, rather than social environment, more accurately predicts problem solving, and whether this relationship would be observed in noncarnivore, noncaptive animals across a range of tasks.

Selection for brain size impairs innate, but not adaptive immune responses.

Both the brain and the immune system are energetically demanding organs, and when natural selection favours increased investment into one, then the size or performance of the other should be reduced. While comparative analyses have attempted to test this potential evolutionary trade-off, the results remain inconclusive. To test this hypothesis, we compared the tissue graft rejection (an assay for measuring innate and acquired immune responses) in guppies (Poecilia reticulata) artificially selected for large and small relative brain size. Individual scales were transplanted between pairs of fish, creating reciprocal allografts, and the rejection reaction was scored over 8 days (before acquired immunity develops). Acquired immune responses were tested two weeks later, when the same pairs of fish received a second set of allografts and were scored again. Compared with large-brained animals, small-brained animals of both sexes mounted a significantly stronger rejection response to the first allograft. The rejection response to the second set of allografts did not differ between large- and small-brained fish. Our results show that selection for large brain size reduced innate immune responses to an allograft, which supports the hypothesis that there is a selective trade-off between investing into brain size and innate immunity.

Expression change in Angiopoietin-1 underlies change in relative brain size in fish.

Brain size varies substantially across the animal kingdom and is often associated with cognitive ability; however, the genetic architecture underpinning natural variation in these key traits is virtually unknown. In order to identify the genetic architecture and loci underlying variation in brain size, we analysed both coding sequence and expression for all the loci expressed in the telencephalon in replicate populations of guppies (Poecilia reticulata) artificially selected for large and small relative brain size. A single gene, Angiopoietin-1 (Ang-1), a regulator of angiogenesis and suspected driver of neural development, was differentially expressed between large- and small-brain populations. Zebra fish (Danio rerio) morphants showed that mild knock down of Ang-1 produces a small-brained phenotype that could be rescued with Ang-1 mRNA. Translation inhibition of Ang-1 resulted in smaller brains in larvae and increased expression of Notch-1, which regulates differentiation of neural stem cells. In situ analysis of newborn large- and small-brained guppies revealed matching expression patterns of Ang-1 and Notch-1 to those observed in zebrafish larvae. Taken together, our results suggest that the genetic architecture affecting brain size in our population may be surprisingly simple, and Ang-1 may be a potentially important locus in the evolution of vertebrate brain size and cognitive ability.

No association between brain size and male sexual behavior in the guppy

Abstract Animal behavior is remarkably variable at all taxonomic levels. Over the last decades, research on animal behavior has focused on understanding ultimate processes. Yet, it has progressively become more evident that to fully understand behavioral variation, ultimate explanations need to be complemented with proximate ones. In particular, the mechanisms generating variation in sexual behavior remain an open question. Variation in aspects of brain morphology has been suggested as a plausible mechanism underlying this variation. However, our knowledge of this potential association is based almost exclusively on comparative analyses. Experimental studies are needed to establish causality and bridge the gap between microand macroevolutionary mechanisms concerning the link between brain and sexual behavior. We used male guppies that had been artificially selected for large or small relative brain size to study this association. We paired males with females and scored the full known set of male and female sexual behaviors described in guppies. We found several previously demonstrated associations between male traits, male behavior and female behavior. Females responded more strongly towards males that courted more and males with more orange coloration. Also, larger males and males with less conspicuous coloration attempted more coerced copulations. However, courting, frequency of coerced copulation attempts, total intensity of sexual behavior, and female response did not differ between largeand small-brained males. Our data suggest that relative brain size is an unlikely mechanism underlying variation in sexual behavior of the male guppy. We discuss these findings in the context of the conditions under which relative brain size might affect male sexual behavior.

The mating brain: early maturing sneaker males maintain investment into the brain also under fast body growth in Atlantic salmon (Salmo salar).

It has been suggested that mating behaviours require high levels of cognitive ability. However, since investment into mating and the brain both are costly features, their relationship is likely characterized by energetic trade-offs. Empirical data on the subject remains equivocal. We investigated if early sexual maturation was associated with brain development in Atlantic salmon (Salmo salar), in which males can either stay in the river and sexually mature at a small size (sneaker males) or migrate to the sea and delay sexual maturation until they have grown much larger (anadromous males). Specifically, we tested how sexual maturation may induce plastic changes in brain development by rearing juveniles on either natural or ad libitum feeding levels. After their first season we compared brain size and brain region volumes across both types of male mating tactics and females. Body growth increased greatly across both male mating tactics and females during ad libitum feeding as compared to natural feeding levels. However, despite similar relative increases in body size, early maturing sneaker males maintained larger relative brain size during ad libitum feeding levels as compared to anadromous males and females. We also detected several differences in the relative size of separate brain regions across feeding treatments, sexes and mating strategies. For instance, the relative size of the cognitive centre of the brain, the telencephalon, was largest in sneaker males. Our data support that a large relative brain size is maintained in individuals that start reproduction early also during fast body growth. We propose that the cognitive demands during complex mating behaviours maintain a high level of investment into brain development in reproducing individuals.Electronic supplementary materialThe online version of this article (doi:10.1007/s10682-014-9715-x) contains supplementary material, which is available to authorized users.

Primates

Primates

Concept formation in American black bears, Ursus americanus

Despite their large relative brain size, bears have been neglected in studies of comparative cognition in comparison to their fellow carnivores, the social canines and pinnipeds. Here, three captive adult American black bears were presented with a series of natural concept discrimination tasks on a touchscreen computer, in which the discriminations varied in degree of abstraction. The more abstract discriminations could not be performed by attending to perceptual features of the stimuli alone. For instance, at the most abstract level, the bears were required to select images of animals rather than nonanimals, and exemplars within both categories were perceptually diverse. At least one bear performed at above-chance levels with transfer to novel images at each level of abstraction. The bear that began testing with the most abstract problems showed the best transfer on more abstract discriminations, suggesting that the usual practice of overtraining animals on perceptual discriminations may hinder their ability to acquire concepts at more abstract levels. The bears' performance suggests that a generalized diet may be more critical than group living with regard to the evolution of complex cognition in carnivores.