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.     

Positive genetic correlation between brain size and sexual traits in male guppies artificially selected for brain size

Brain size is an energetically costly trait to develop and maintain. Investments into other costly aspects of an organism's biology may therefore place important constraints on brain size evolution. Sexual traits are often costly and could therefore be traded off against neural investment. However, brain size may itself be under sexual selection through mate choice on cognitive ability. Here, we use guppy (Poecilia reticulata) lines selected for large and small brain size relative to body size to investigate the relationship between brain size, a large suite of male primary and secondary sexual traits, and body condition index. We found no evidence for trade‐offs between brain size and sexual traits. Instead, larger‐brained males had higher expression of several primary and precopulatory sexual traits – they had longer genitalia, were more colourful and developed longer tails than smaller‐brained males. Larger‐brained males were also in better body condition when housed in single‐sex groups. There was no difference in post‐copulatory sexual traits between males from the large‐ and small‐brained lines. Our data do not support the hypothesis that investment into sexual traits is an important limiting factor to brain size evolution, but instead suggest that brain size and several sexual traits are positively genetically correlated.     

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.     

Genome size variation and species diversity in salamanders

Salamanders (Urodela) have among the largest vertebrate genomes, ranging in size from 10 to 120 pg. Although changes in genome size often occur randomly and in the absence of selection pressure, nonrandom patterns of genome size variation are evident among specific vertebrate lineages. Several reports suggest a relationship between species richness and genome size, but the exact nature of that relationship remains unclear both within and across different taxonomic groups. Here, we report (a) a negative relationship between haploid genome size (C‐value) and species richness at the family taxonomic level in salamander clades; (b) a correlation of C‐value and species richness with clade crown age but not with diversification rates; (c) strong associations between C‐value and both geographic area and climatic‐niche rate. Finally, we report a relationship between C‐value diversity and species diversity at both the family‐ and genus‐level clades in urodeles.     

Comparative support for the expensive tissue hypothesis: Big brains are correlated with smaller gut and greater parental investment in Lake Tanganyika cichlids

The brain is one of the most energetically expensive organs in the vertebrate body. Consequently, the energetic requirements of encephalization are suggested to impose considerable constraints on brain size evolution. Three main hypotheses concerning how energetic constraints might affect brain evolution predict covariation between brain investment and (1) investment into other costly tissues, (2) overall metabolic rate, and (3) reproductive investment. To date, these hypotheses have mainly been tested in homeothermic animals and the existing data are inconclusive. However, there are good reasons to believe that energetic limitations might play a role in large-scale patterns of brain size evolution also in ectothermic vertebrates. Here, we test these hypotheses in a group of ectothermic vertebrates, the Lake Tanganyika cichlid fishes. After controlling for the effect of shared ancestry and confounding ecological variables, we find a negative association between brain size and gut size. Furthermore, we find that the evolution of a larger brain is accompanied by increased reproductive investment into egg size and parental care. Our results indicate that the energetic costs of encephalization may be an important general factor involved in the evolution of brain size also in ectothermic vertebrates.     

The effect of brain size evolution on feeding propensity,digestive efficiency,and juvenile growth

One key hypothesis in the study of brain size evolution is the expensive tissue hypothesis; the idea that increased investment into the brain should be compensated by decreased investment into other costly organs, for instance the gut. Although the hypothesis is supported by both comparative and experimental evidence, little is known about the potential changes in energetic requirements or digestive traits following such evolutionary shifts in brain and gut size. Organisms may meet the greater metabolic requirements of larger brains despite smaller guts via increased food intake or better digestion. But increased investment in the brain may also hamper somatic growth. To test these hypotheses we here used guppy (Poecilia reticulata) brain size selection lines with a pronounced negative association between brain and gut size and investigated feeding propensity, digestive efficiency (DE), and juvenile growth rate. We did not find any difference in feeding propensity or DE between large‐ and small‐brained individuals. Instead, we found that large‐brained females had slower growth during the first 10 weeks after birth. Our study provides experimental support that investment into larger brains at the expense of gut tissue carries costs that are not necessarily compensated by a more efficient digestive system.     

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.     

Long life evolves in large-brained bird lineages*

The brain is an energetically costly organ that consumes a disproportionate amount of resources. Species with larger brains relative to their body size have slower life histories, with reduced output per reproductive event and delayed development times that can be offset by increasing behavioral flexibility. The “cognitive buffer” hypothesis maintains that large brain size decreases extrinsic mortality due to greater behavioral flexibility, leading to a longer lifespan. Alternatively, slow life histories, and long lifespan can be a pre-adaptation for the evolution of larger brains. Here, we use phylogenetic path analysis to contrast different evolutionary scenarios and disentangle direct and indirect relationships between brain size, body size, life history, and longevity across 339 altricial and precocial bird species. Our results support both a direct causal link between brain size and lifespan, and an indirect effect via other life history traits. These results indicate that large brain size engenders longer life, as proposed by the “cognitive buffer” hypothesis.     

Brain size affects female but not male survival under predation threat

There is remarkable diversity in brain size among vertebrates, but surprisingly little is known about how ecological species interactions impact the evolution of brain size. Using guppies, artificially selected for large and small brains, we determined how brain size affects survival under predation threat in a naturalistic environment. We cohoused mixed groups of small‐ and large‐brained individuals in six semi‐natural streams with their natural predator, the pike cichlid, and monitored survival in weekly censuses over 5 months. We found that large‐brained females had 13.5% higher survival compared to small‐brained females, whereas the brain size had no discernible effect on male survival. We suggest that large‐brained females have a cognitive advantage that allows them to better evade predation, whereas large‐brained males are more colourful, which may counteract any potential benefits of brain size. Our study provides the first experimental evidence that trophic interactions can affect the evolution of brain size.     

The Expensive Brain: A framework for explaining evolutionary changes in brain size

To explain variation in relative brain size among homoiothermic vertebrates, we propose the Expensive Brain hypothesis as a unifying explanatory framework. It claims that the costs of a relatively large brain must be met by any combination of increased total energy turnover or reduced energy allocation to another expensive function such as digestion, locomotion, or production (growth and reproduction). Focusing on the energetic costs of brain enlargement, a comparative analysis of the largest mammalian sample assembled to date shows that an increase in brain size leads to larger neonates among all mammals and a longer period of immaturity among monotokous precocial species, but not among the polytokous altricial ones, who instead reduce their litter size. Relatively large brained mammals, altricial and precocial, also show reduced annual fertility rates as compared to their smaller brained relatives, but allomaternal energy inputs allow some cooperatively breeding altricial carnivores to produce even more offspring in a shorter time despite having a relatively large brain. Thus, the Expensive Brain framework explains why brain size is linked to life history pace in some, but not all mammalian lineages. This framework encompasses other hypotheses of energetic constraints on brain size variation and is also compatible with the Brain Malnutrition Risk hypothesis, but the absence of a mammal-wide correlation between brain size and immature period argues against the Needing-to-Learn explanation for slower development among large brained mammals.     

Rates of morphological evolution are correlated with species richness in salamanders

The tempo and mode of species diversification and phenotypic evolution vary widely across the tree of life, yet the relationship between these processes is poorly known. Previous tests of the relationship between rates of phenotypic evolution and rates of species diversification have assumed that species richness increases continuously through time. If this assumption is violated, simple phylogenetic estimates of net diversification rate may bear no relationship to processes that influence the distribution of species richness among clades. Here, we demonstrate that the variation in species richness among plethodontid salamander clades is unlikely to have resulted from simple time-dependent processes, leading to fundamentally different conclusions about the relationship between rates of phenotypic evolution and species diversification. Morphological evolutionary rates of both size and shape evolution are correlated with clade species richness, but are uncorrelated with simple estimators of net diversification that assume constancy of rates through time. This coupling between species diversification and phenotypic evolution is consistent with the hypothesis that clades with high rates of morphological trait evolution may diversify more than clades with low rates. Our results indicate that assumptions about underlying processes of diversity regulation have important consequences for interpreting macroevolutionary patterns.     

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

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

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.     

The influence of size on body shape diversification across Indo‐Pacific shore fishes*

Understanding the causes of body shape variability across the tree of life is one of the central issues surrounding the origins of biodiversity. One potential mechanism driving observed patterns of shape disparity is a strongly conserved relationship between size and shape. Conserved allometry has been shown to account for as much as 80% of shape variation in some vertebrate groups. Here, we quantify the amount of body shape disparity attributable to changes in body size across nearly 800 species of Indo‐Pacific shore fishes using a phylogenetic framework to analyze 17 geometric landmarks positioned to capture general body shape and functionally significant features. In marked contrast to other vertebrate lineages, we find that changes in body size only explain 2.9% of the body shape variation across fishes, ranging from 3% to 50% within our 11 sampled families. We also find a slight but significant trend of decreasing rates of shape evolution with increasing size. Our results suggest that the influence of size on fish shape has largely been overwhelmed by lineage‐specific patterns of diversification that have produced the modern landscape of highly diverse forms that we currently observe in nature.     

Evolutionary Divergence in Brain Size between Migratory and Resident Birds

Despite important recent progress in our understanding of brain evolution, controversy remains regarding the evolutionary forces that have driven its enormous diversification in size. Here, we report that in passerine birds, migratory species tend to have brains that are substantially smaller (relative to body size) than those of resident species, confirming and generalizing previous studies. Phylogenetic reconstructions based on Bayesian Markov chain methods suggest an evolutionary scenario in which some large brained tropical passerines that invaded more seasonal regions evolved migratory behavior and migration itself selected for smaller brain size. Selection for smaller brains in migratory birds may arise from the energetic and developmental costs associated with a highly mobile life cycle, a possibility that is supported by a path analysis. Nevertheless, an important fraction (over 68%) of the correlation between brain mass and migratory distance comes from a direct effect of migration on brain size, perhaps reflecting costs associated with cognitive functions that have become less necessary in migratory species. Overall, our results highlight the importance of retrospective analyses in identifying selective pressures that have shaped brain evolution, and indicate that when it comes to the brain, larger is not always better.     

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.     

Sexual selection uncouples the evolution of brain and body size in pinnipeds

The size of the vertebrate brain is shaped by a variety of selective forces. Although larger brains (correcting for body size) are thought to confer fitness advantages, energetic limitations of this costly organ may lead to trade-offs, for example as recently suggested between sexual traits and neural tissue. Here, we examine the patterns of selection on male and female brain size in pinnipeds, a group where the strength of sexual selection differs markedly among species and between the sexes. Relative brain size was negatively associated with the intensity of sexual selection in males but not females. However, analyses of the rates of body and brain size evolution showed that this apparent trade-off between sexual selection and brain mass is driven by selection for increasing body mass rather than by an actual reduction in male brain size. Our results suggest that sexual selection has important effects on the allometric relationships of neural development.     

Within species support for the expensive tissue hypothesis: a negative association between brain size and visceral fat storage in females of the Pacific seaweed pipefish

The brain is one of the most energetically expensive organs in the vertebrate body. Consequently, the high cost of brain development and maintenance is predicted to constrain adaptive brain size evolution (the expensive tissue hypothesis, ETH). Here, we test the ETH in a teleost fish with predominant female mating competition (reversed sex roles) and male pregnancy, the pacific seaweed pipefish Syngnathus schlegeli. The relative size of the brain and other energetically expensive organs (kidney, liver, heart, gut, visceral fat, and ovary/testis) was compared among three groups: pregnant males, nonpregnant males and egg producing females. Brood size in pregnant males was unrelated to brain size or the size of any other organ, whereas positive relationships were found between ovary size, kidney size, and liver size in females. Moreover, we found that the size of energetically expensive organs (brain, heart, gut, kidney, and liver) as well as the amount of visceral fat did not differ between pregnant and nonpregnant males. However, we found marked differences in relative size of the expensive organs between sexes. Females had larger liver and kidney than males, whereas males stored more visceral fat than females. Furthermore, in females we found a negative correlation between brain size and the amount of visceral fat, whereas in males, a positive trend between brain size and both liver and heart size was found. These results suggest that, while the majority of variation in the size of various expensive organs in this species likely reflects that individuals in good condition can afford to allocate resources to several organs, the cost of the expensive brain was visible in the visceral fat content of females, possibly due to the high costs associated with female egg production.     

Body size evolution in Mesozoic birds

The tendency for the mean body size of taxa within a clade to increase through evolution (Cope's Rule) has been demonstrated in a number of terrestrial vertebrate groups. However, because avian body size is strongly constrained by flight, any increase in size during the evolution of this lineage should be limited - there is a maximum size that can be attained by a bird for it to be able to get off the ground. Contrary to previous interpretations of early avian evolution, we demonstrate an overall increase in body size across Jurassic and Cretaceous flying birds: taxon body size increases from the earliest Jurassic through to the end of the Cretaceous, across a time span of 70 Myr. Although evidence is limited that this change is directional, it is certainly nonrandom. Relative size increase occurred presumably as the result of an increase in variance as the avian clade diversified after the origin of flight: a progression towards larger body size is seen clearly within the clades Pygostylia and Ornithothoraces. In contrast, a decrease in body size characterizes the most crownward lineage Ornithuromorpha, the clade that includes all extant taxa, and potentially may explain the survival of these birds across the Cretaceous-Palaeogene boundary. As in all other dinosaurs, counter selection for small size is seen in some clades, whereas body size is increasing overall.     

Shared extremes by ectotherms and endotherms: Body elongation in mustelids is associated with small size and reduced limbs

An elongate body with reduced or absent limbs has evolved independently in many ectothermic vertebrate lineages. While much effort has been spent examining the morphological pathways to elongation in these clades, quantitative investigations into the evolution of elongation in endothermic clades are lacking. We quantified body shape in 61 musteloid mammals (red panda, skunks, raccoons, and weasels) using the head‐body elongation ratio. We also examined the morphological changes that may underlie the evolution toward more extreme body plans. We found that a mustelid clade comprised of the subfamilies Helictidinae, Guloninae, Ictonychinae, Mustelinae, and Lutrinae exhibited an evolutionary transition toward more elongate bodies. Furthermore, we discovered that elongation of the body is associated with the evolution of other key traits such as a reduction in body size and a reduction in forelimb length but not hindlimb length. This relationship between body elongation and forelimb length has not previously been quantitatively established for mammals but is consistent with trends exhibited by ectothermic vertebrates and suggests a common pattern of trait covariance associated with body shape evolution. This study provides the framework for documenting body shapes across a wider range of mammalian clades to better understand the morphological changes influencing shape disparity across all vertebrates.