No gains for bigger brains: Functional and neuroanatomical consequences of relative brain size in a parasitic wasp

Heritable genetic variation in relative brain size can underlie the relationship between brain performance and the relative size of the brain. We used bidirectional artificial selection to study the consequences of genetic variation in relative brain size on brain morphology, cognition and longevity in Nasonia vitripennis parasitoid wasps. Our results show a robust change in relative brain size after 26 generations of selection and six generations of relaxation. Total average neuropil volume of the brain was 16% larger in wasps selected for relatively large brains than in wasps selected for relatively small brains, whereas the body length of the large‐brained wasps was smaller. Furthermore, the relative volume of the antennal lobes was larger in wasps with relatively large brains. Relative brain size did not influence olfactory memory retention, whereas wasps that were selected for larger relative brain size had a shorter longevity, which was even further reduced after a learning experience. These effects of genetic variation on neuropil composition and memory retention are different from previously described effects of phenotypic plasticity in absolute brain size. In conclusion, having relatively large brains may be costly for N. vitripennis, whereas no cognitive benefits were recorded.     

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.     

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.     

Sex, ecology and the brain: evolutionary correlates of brain structure volumes in Tanganyikan cichlids

Analyses of the macroevolutionary correlates of brain structure volumes allow pinpointing of selective pressures influencing specific structures. Here we use a multiple regression framework, including phylogenetic information, to analyze brain structure evolution in 43 Tanganyikan cichlid species. We analyzed the effect of ecological and sexually selected traits for species averages, the effect of ecological traits for each sex separately and the influence of sexual selection on structure dimorphism. Our results indicate that both ecological and sexually selected traits have influenced brain structure evolution. The patterns observed in males and females generally followed those observed at the species level. Interestingly, our results suggest that strong sexual selection is associated with reduced structure volumes, since all correlations between sexually selected traits and structure volumes were negative and the only statistically significant association between sexual selection and structure dimorphism was also negative. Finally, we previously found that monoparental female care was associated with increased brain size. However, here cerebellum and hypothalamus volumes, after controlling for brain size, associated negatively with female-only care. Thus, in accord with the mosaic model of brain evolution, brain structure volumes may not respond proportionately to changes in brain size. Indeed selection favoring larger brains can simultaneously lead to a reduction in relative structure volumes.     

Evidence for small scale variation in the vertebrate brain: mating strategy and sex affect brain size and structure in wild brown trout (Salmo trutta)

The basis for our knowledge of brain evolution in vertebrates rests heavily on empirical evidence from comparative studies at the species level. However, little is still known about the natural levels of variation and the evolutionary causes of differences in brain size and brain structure within‐species, even though selection at this level is an important initial generator of macroevolutionary patterns across species. Here, we examine how early life‐history decisions and sex are related to brain size and brain structure in wild populations using the existing natural variation in mating strategies among wild brown trout (Salmo trutta). By comparing the brains of precocious fish that remain in the river and sexually mature at a small size with those of migratory fish that migrate to the sea and sexually mature at a much larger size, we show, for the first time in any vertebrate, strong differences in relative brain size and brain structure across mating strategies. Precocious fish have larger brain size (when controlling for body size) but migratory fish have a larger cerebellum, the structure in charge of motor coordination. Moreover, we demonstrate sex‐specific differences in brain structure as female precocious fish have a larger brain than male precocious fish while males of both strategies have a larger telencephalon, the cognitive control centre, than females. The differences in brain size and structure across mating strategies and sexes thus suggest the possibility for fine scale adaptive evolution of the vertebrate brain in relation to different life histories.     

Smart moves: effects of relative brain size on establishment success of invasive amphibians and reptiles

Brain size relative to body size varies considerably among animals, but the ecological consequences of that variation remain poorly understood. Plausibly, larger brains confer increased behavioural flexibility, and an ability to respond to novel challenges. In keeping with that hypothesis, successful invasive species of birds and mammals that flourish after translocation to a new area tend to have larger brains than do unsuccessful invaders. We found the same pattern in ectothermic terrestrial vertebrates. Brain size relative to body size was larger in species of amphibians and reptiles reported to be successful invaders, compared to species that failed to thrive after translocation to new sites. This pattern was found in six of seven global biogeographic realms; the exception (where relatively larger brains did not facilitate invasion success) was Australasia. Establishment success was also higher in amphibian and reptile families with larger relative brain sizes. Future work could usefully explore whether invasion success is differentially associated with enlargement of specific parts of the brain (as predicted by the functional role of the forebrain in promoting behavioural flexibility), or with a general size increase (suggesting that invasion success is facilitated by enhanced perceptual and motor skills, as well as cognitive ability).     

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.     

Sexual selection impacts brain anatomy in frogs and toads

Natural selection is a major force in the evolution of vertebrate brain size, but the role of sexual selection in brain size evolution remains enigmatic. At least two opposing schools of thought predict a relationship between sexual selection and brain size. Sexual selection should facilitate the evolution of larger brains because better cognitive abilities may aid the competition for mates. However, it may also restrict brain size evolution due to energetic trade‐offs between brain tissue and sexually selected traits. Here, we examined the patterns of selection on brain size and brain anatomy in male anurans (frogs and toads), a group where the strength of sexual selection differs markedly among species, using a phylogenetically controlled generalized least‐squared (PGLS) regression analyses. The analysis revealed that in 43 Chinese anuran species, neither mating system, nor type of courtship, or testes mass was significantly associated with relative brain size. While none of those factors related to the relative size of olfactory nerves, optic tecta, telencephalon, and cerebellum, the olfactory bulbs were relatively larger in monogamous species and those using calls during courtship. Our findings support the mosaic model of brain evolution and suggest that while the investigated aspects of sexual selection do not seem to play a prominent role in the evolution of brain size of anurans, they do impact their brain anatomy.     

Artificial selection on brain size leads to matching changes in overall number of neurons

Neurons are the basic computational units of the brain, but brain size is the predominant surrogate measure of brain functional capacity in comparative and cognitive neuroscience. This approach is based on the assumption that larger brains harbor higher numbers of neurons and their connections, and therefore have a higher information‐processing capacity. However, recent studies have shown that brain mass may be less strongly correlated with neuron counts than previously thought. Till now, no experimental test has been conducted to examine the relationship between evolutionary changes in brain size and the number of brain neurons. Here, we provide such a test by comparing neuron number in artificial selection lines of female guppies (Poecilia reticulata) with >15% difference in relative brain mass and numerous previously demonstrated cognitive differences. Using the isotropic fractionator, we demonstrate that large‐brained females have a higher overall number of neurons than small‐brained females, but similar neuronal densities. Importantly, this difference holds also for the telencephalon, a key region for cognition. Our study provides the first direct experimental evidence that selection for brain mass leads to matching changes in number of neurons and shows that brain size evolution is intimately linked to the evolution of neuron number and cognition.     

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

Comparative analyses of primate brain evolution have highlighted changes in size and internal organization as key factors underlying species diversity. It remains, however, unclear (i) how much variation in mosaic brain reorganization versus variation in relative brain size contributes to explaining the structural neural diversity observed across species, (ii) which mosaic changes contribute most to explaining diversity, and (iii) what the temporal origin, rates and processes are that underlie evolutionary shifts in mosaic reorganization for individual branches of the primate tree of life. We address these questions by combining novel comparative methods that allow assessing the temporal origin, rate and process of evolutionary changes on individual branches of the tree of life, with newly available data on volumes of key brain structures (prefrontal cortex, frontal motor areas and cerebrocerebellum) for a sample of 17 species (including humans). We identify patterns of mosaic change in brain evolution that mirror brain systems previously identified by electrophysiological and anatomical tract-tracing studies in non-human primates and functional connectivity MRI studies in humans. Across more than 40 Myr of anthropoid primate evolution, mosaic changes contribute more to explaining neural diversity than changes in relative brain size, and different mosaic patterns are differentially selected for when brains increase or decrease in size. We identify lineage-specific evolutionary specializations for all branches of the tree of life covered by our sample and demonstrate deep evolutionary roots for mosaic patterns associated with motor control and learning.     

Brain organization mirrors caste differences,colony founding and nest architecture in paper wasps (Hymenoptera: Vespidae)

The cognitive challenges that social animals face depend on species differences in social organization and may affect mosaic brain evolution. We asked whether the relative size of functionally distinct brain regions corresponds to species differences in social behaviour among paper wasps (Hymenoptera: Vespidae). We measured the volumes of targeted brain regions in eight species of paper wasps. We found species variation in functionally distinct brain regions, which was especially strong in queens. Queens from species with open-comb nests had larger central processing regions dedicated to vision (mushroom body (MB) calyx collars) than those with enclosed nests. Queens from advanced eusocial species (swarm founders), who rely on pheromones in several contexts, had larger antennal lobes than primitively eusocial independent founders. Queens from species with morphologically distinct castes had augmented central processing regions dedicated to antennal input (MB lips) relative to caste monomorphic species. Intraspecific caste differences also varied with mode of colony founding. Independent-founding queens had larger MB collars than their workers. Conversely, workers in swarm-founding species with decentralized colony regulation had larger MB calyx collars and optic lobes than their queens. Our results suggest that brain organization is affected by evolutionary transitions in social interactions and is related to the environmental stimuli group members face.     

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.     

Sexual selection predicts brain structure in dragon lizards

Phenotypic traits such as ornaments and armaments are generally shaped by sexual selection, which often favours larger and more elaborate males compared to females. But can sexual selection also influence the brain? Previous studies in vertebrates report contradictory results with no consistent pattern between variation in brain structure and the strength of sexual selection. We hypothesize that sexual selection will act in a consistent way on two vertebrate brain regions that directly regulate sexual behaviour: the medial preoptic nucleus (MPON) and the ventromedial hypothalamic nucleus (VMN). The MPON regulates male reproductive behaviour whereas the VMN regulates female reproductive behaviour and is also involved in male aggression. To test our hypothesis, we used high‐resolution magnetic resonance imaging combined with traditional histology of brains in 14 dragon lizard species of the genus Ctenophorus that vary in the strength of precopulatory sexual selection. Males belonging to species that experience greater sexual selection had a larger MPON and a smaller VMN. Conversely, females did not show any patterns of variation in these brain regions. As the volumes of both these regions also correlated with brain volume (BV) in our models, we tested whether they show the same pattern of evolution in response to changes in BV and found that the do. Therefore, we show that the primary brain nuclei underlying reproductive behaviour in vertebrates can evolve in a mosaic fashion, differently between males and females, likely in response to sexual selection, and that these same regions are simultaneously evolving in concert in relation to overall brain size.     

On the evolution of brain size in relation to migratory behaviour in birds

Migratory birds appear to have relatively smaller brain size compared to sedentary species. It has been hypothesized that initial differences in brain size underlying behavioural flexibility drove the evolution of migratory behaviour; birds with relatively large brains evolved sedentary habits and those with relatively small brains evolved migratory behaviour (migratory precursor hypothesis). Alternative hypotheses suggest that changes in brain size might follow different behavioural strategies and that sedentary species might have evolved larger brains because of differences in selection pressures on brain size in migratory and nonmigratory species. Here we present the first evidence arguing against the migratory precursor hypothesis. We compared relative brain volume of three subspecies of the white-crowned sparrow: sedentary Zonotrichia leucophrys nuttalli and migratory Z. l. gambelii and Z. l. oriantha. Within the five subspecies of the white-crowned sparrow, only Z. l. nuttalli is strictly sedentary. The sedentary behaviour of Z. l. nuttalli is probably a derived trait, because Z. l. nuttalli appears to be the most recent subspecies and because all species ancestral to Zonotrichia as well as all older subspecies of Z. leucophrys are migratory. Compared to migratory Z. l. gambelii and Z. l. oriantha, we found that sedentary Z. l. nuttalli had a significantly larger relative brain volume, suggesting that the larger brain of Z. l. nuttalli evolved after a switch to sedentary behaviour. Thus, in this group, brain size does not appear to be a precursor to the evolution of migratory or sedentary behaviour but rather an evolutionary consequence of a change in migratory strategy.     

Multiple determinants of whole and regional brain volume among terrestrial carnivorans

Mammalian brain volumes vary considerably, even after controlling for body size. Although several hypotheses have been proposed to explain this variation, most research in mammals on the evolution of encephalization has focused on primates, leaving the generality of these explanations uncertain. Furthermore, much research still addresses only one hypothesis at a time, despite the demonstrated importance of considering multiple factors simultaneously. We used phylogenetic comparative methods to investigate simultaneously the importance of several factors previously hypothesized to be important in neural evolution among mammalian carnivores, including social complexity, forelimb use, home range size, diet, life history, phylogeny, and recent evolutionary changes in body size. We also tested hypotheses suggesting roles for these variables in determining the relative volume of four brain regions measured using computed tomography. Our data suggest that, in contrast to brain size in primates, carnivoran brain size may lag behind body size over evolutionary time. Moreover, carnivore species that primarily consume vertebrates have the largest brains. Although we found no support for a role of social complexity in overall encephalization, relative cerebrum volume correlated positively with sociality. Finally, our results support negative relationships among different brain regions after accounting for overall endocranial volume, suggesting that increased size of one brain regions is often accompanied by reduced size in other regions rather than overall brain expansion.     

Seasonal variation of behavior and brain size in a freshwater fish

1. 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.
2. 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).
3. 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.
4. 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.

     

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.     

Visual specialization and brain evolution in primates.

Several theories have been proposed to explain the evolution of species differences in brain size, but no consensus has emerged. One unresolved question is whether brain size differences are a result of neural specializations or of biological constraints affecting the whole brain. Here I show that, among primates, brain size variation is associated with visual specialization. Primates with large brains for their body size have relatively expanded visual brain areas, including the primary visual cortex and lateral geniculate nucleus. Within the visual system, it is, in particular, one functionally specialized pathway upon which selection has acted: evolutionary changes in the number of neurons in parvocellular, but not magnocellular, layers of the lateral geniculate nucleus are correlated with changes in both brain size and ecological variables (diet and social group size). Given the known functions of the parvocellular pathway, these results suggest that the relatively large brains of frugivorous species are products of selection on the ability to perceive and select fruits using specific visual cues such as colour. The separate correlation between group size and visual brain evolution, on the other hand, may indicate the visual basis of social information processing in the primate brain.     

Large‐brained birds suffer less oxidative damage

Large brains (relative to body size) might confer fitness benefits to animals. Although the putative costs of well‐developed brains can constrain the majority of species to modest brain sizes, these costs are still poorly understood. Given that the neural tissue is energetically expensive and demands antioxidants, one potential cost of developing and maintaining large brains is increased oxidative stress (‘oxidation exposure’ hypothesis). Alternatively, because large‐brained species exhibit slow‐paced life histories, they are expected to invest more into self‐maintenance such as an efficacious antioxidative defence machinery (‘oxidation avoidance’ hypothesis). We predict decreased antioxidant levels and/or increased oxidative damage in large‐brained species in case of oxidation exposure, and the contrary in case of oxidation avoidance. We address these contrasting hypotheses for the first time by means of a phylogenetic comparative approach based on an unprecedented data set of four redox state markers from 85 European bird species. Large‐brained birds suffered less oxidative damage to lipids (measured as malondialdehyde levels) and exhibited higher total nonenzymatic antioxidant capacity than small‐brained birds, whereas uric acid and glutathione levels were independent of brain size. These results were not altered by potentially confounding variables and did not depend on how relative brain size was quantified. Our findings partially support the ‘oxidation avoidance’ hypothesis and provide a physiological explanation for the linkage of large brains with slow‐paced life histories: reduced oxidative stress of large‐brained birds can secure brain functionality and healthy life span, which are integral to their lifetime fitness and slow‐paced life history.     

Evolution of ASPM is associated with both increases and decreases in brain size in primates

A fundamental trend during primate evolution has been the expansion of brain size. However, this trend was reversed in the Callitrichidae (marmosets and tamarins), which have secondarily evolved smaller brains associated with a reduction in body size. The recent pursuit of the genetic basis of brain size evolution has largely focused on episodes of brain expansion, but new insights may be gained by investigating episodes of brain size reduction. Previous results suggest two genes (ASPM and CDK5RAP2) associated with microcephaly, a human neurodevelopmental disorder, may have an evolutionary function in primate brain expansion. Here we use new sequences encoding key functional domains from 12 species of callitrichids to show that positive selection has acted on ASPM across callitrichid evolution and the rate of ASPM evolution is significantly negatively correlated with callitrichid brain size, whereas the evolution of CDK5RAP2 shows no correlation with brain size. Our findings strongly suggest that ASPM has a previously unsuspected role in the evolution of small brains in primates. ASPM is therefore intimately linked to both evolutionary increases and decreases in brain size in anthropoids and is a key target for natural selection acting on brain size.