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Domestication is a well-known example of the relaxation of environmentally based cognitive selection that leads to reductions in brain size. However, little is known about how brain size evolves after domestication and whether subsequent directional/artificial selection can compensate for domestication effects. The first animal to be domesticated was the dog, and recent directional breeding generated the extensive phenotypic variation among breeds we observe today. Here we use a novel endocranial dataset based on high-resolution CT scans to estimate brain size in 159 dog breeds and analyze how relative brain size varies across breeds in relation to functional selection, longevity, and litter size. In our analyses, we controlled for potential confounding factors such as common descent, gene flow, body size, and skull shape. We found that dogs have consistently smaller relative brain size than wolves supporting the domestication effect, but breeds that are more distantly related to wolves have relatively larger brains than breeds that are more closely related to wolves. Neither functional category, skull shape, longevity, nor litter size was associated with relative brain size, which implies that selection for performing specific tasks, morphology, and life history does not necessarily influence brain size evolution in domesticated species.

The organization and coordination of fish schools provide a valuable model to investigate the genetic architecture of affiliative behaviors and dissect the mechanisms underlying social behaviors and personalities. We used quantitative genetic methods in replicate guppy selection lines that vary in group alignment and schooling propensity to investigate the genetic basis of sociability phenotypes. Alignment and attraction, the two major traits forming the sociability personality axis in this species, showed heritability estimates at the upper end of the range previously described for social behaviors, with important variation across sexes. Consistent with findings in collective motion patterns, experimental evolution of schooling propensity increases the sociability of female, but not male, guppies when swimming with unfamiliar conspecifics, a highly relevant trait in a species with fission-fusion social systems in natural populations. Our results from PoolSeq and RNASeq convergently identify genes involved in neuron migration and synaptic function, highlighting a crucial role of glutamatergic synaptic function and calcium-dependent signaling processes in the evolution of schooling.

Mosaic brain evolution, the change in the size of separate brain regions in response to selection on cognitive performance, is an important idea in the field of cognitive evolution. However, untill now, most of the data on how separate brain regions respond to selection and their cognitive consequences stem from comparative studies. To experimentally investigate the influence of mosaic brain evolution on cognitive ability, we used male guppies artificially selected for large and small telencephalons relative to the rest of the brain. Here, we tested an important aspect of executive cognitive ability using a detour task. We found that males with larger telencephalons outperformed males with smaller telencephalons. Fish with larger telencephalons showed faster improvement in performance during detour training and were more successful in reaching the food reward without touching the transparent barrier (i.e., through correct detouring) during the test phase. Together, our findings provide the first experimental evidence showing that evolutionary enlargement of relative telencephalon size confers cognitive benefits, supporting an important role for mosaic brain evolution during cognitive evolution.

Determining how variation in brain morphology affects cognitive abilities is important to understand inter-individual variation in cognition and, ultimately, cognitive evolution. Yet, despite many decades of research in this area, there is surprisingly little experimental data available from assays that quantify cognitive abilities and brain morphology in the same individuals. Here, we tested female guppies (

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.

Determining how variation in brain morphology affects cognitive abilities is important to understand inter-individual variation in cognition and, ultimately, cognitive evolution. Yet, despite many decades of research in this area, there is surprisingly little experimental data available from assays that quantify cognitive abilities and brain morphology in the same individuals. Here, we tested female guppies ( Poecilia reticulata ) in two tasks, colour discrimination and reversal learning, to evaluate their learning abilities and cognitive flexibility. We then estimated the size of five brain regions (telencephalon, optic tectum, hypothalamus, cerebellum and dorsal medulla), in addition to relative brain size. We found that optic tectum relative size, in relation to the rest of the brain, correlated positively with discrimination learning performance, while relative telencephalon size correlated positively with reversal learning performance. The other brain measures were not associated with performance in either task. By evaluating how fast learning occurs and how fast an animal adjusts its learning rules to changing conditions, we find support for that different brain regions have distinct functional correlations at the individual level. Importantly, telencephalon size emerges as an important neural correlate of higher executive functions such as cognitive flexibility. This is rare evidence supporting the theory that more neural tissue in key brain regions confers cognitive benefits.

Among-population variance of phenotypic traits is of high relevance for understanding evolutionary mechanisms that operate in relatively short timescales, but various sources of nonindependence, such as common ancestry and gene flow, can hamper the interpretations. In this comparative analysis of 138 dog breeds, we demonstrate how such confounders can independently shape the evolution of a behavioural trait (human-directed play behaviour from the Dog Mentality Assessment project). We combined information on genetic relatedness and haplotype sharing to reflect common ancestry and gene flow, respectively, and entered these into a phylogenetic mixed model to partition the among-breed variance of human-directed play behaviour while also accounting for within-breed variance. We found that 75% of the among-breed variance was explained by overall genetic relatedness among breeds, whereas 15% could be attributed to haplotype sharing that arises from gene flow. Therefore, most of the differences in human-directed play behaviour among breeds have likely been caused by constraints of common ancestry as a likely consequence of past selection regimes. On the other hand, gene flow caused by crosses among breeds has played a minor, but not negligible role. Our study serves as an example of an analytical approach that can be applied to comparative situations where the effects of shared origin and gene flow require quantification and appropriate statistical control in a within-species/among-population framework. Altogether, our results suggest that the evolutionary history of dog breeds has left remarkable signatures on the among-breed variation of a behavioural phenotype.

Despite ongoing advances in sexual selection theory, the evolution of mating decisions remains enigmatic. Cognitive processes often require simultaneous processing of multiple sources of information from environmental and social cues. However, little experimental data exist on how cognitive ability affects such fitness-associated aspects of behaviour. Using advanced tracking techniques, we studied mating behaviours of guppies artificially selected for divergence in relative brain size, with known differences in cognitive ability, when predation threat and sex ratio was varied. In females, we found a general increase in copulation behaviour in when the sex ratio was female biased, but only large-brained females responded with greater willingness to copulate under a low predation threat. In males, we found that small-brained individuals courted more intensively and displayed more aggressive behaviours than large-brained individuals. However, there were no differences in female response to males with different brain size. These results provide further evidence of a role for female brain size in optimal decision-making in a mating context. In addition, our results indicate that brain size may affect mating display skill in male guppies. We suggest that it is important to consider the association between brain size, cognitive ability and sexual behaviour when studying how morphological and behavioural traits evolve in wild populations.

The telencephalon is a brain region believed to have played an essential role during cognitive evolution in vertebrates. However, till now, all the evidence on the evolutionary association between telencephalon size and cognition stem from comparative studies. To experimentally investigate the potential evolutionary association between cognitive abilities and telencephalon size, we used male guppies artificially selected for large and small telencephalon relative to the rest of the brain. In a detour task, we tested a functionally important aspect of executive cognitive ability; inhibitory control abilities. We found that males with larger telencephalon outperformed males with smaller telencephalon. They showed faster improvement in performance during detour training and were more successful in reaching the food reward without touching the transparent barrier. Together, our findings provide the first experimental evidence showing that evolutionary enlargements of relative telencephalon size confer cognitive benefits, supporting an important role for mosaic brain evolution during cognitive evolution.

Description, Experimental evidence shows that mosaic evolution can drive brain morphology variation and potentially cognitive evolution., The mosaic brain evolution hypothesis, stating that brain regions can evolve relatively independently during cognitive evolution, is an important idea to understand how brains evolve with potential implications even for human brain evolution. Here, we provide the first experimental evidence for this hypothesis through an artificial selection experiment in the guppy (Poecilia reticulata). After four generations of selection on relative telencephalon volume (relative to brain size), we found substantial changes in telencephalon size but no changes in other regions. Further comparisons revealed that up-selected lines had larger telencephalon, while down-selected lines had smaller telencephalon than wild Trinidadian populations. Our results support that independent evolutionary changes in specific brain regions through mosaic brain evolution can be important facilitators of cognitive evolution.

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 24 months 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.

Choosing a mate is one of the most important decisions in an animal’s lifetime. Female mate choice is often guided by the presence or intensity of male sexual ornaments, which must be integrated and compared among potential mates. Individuals with greater cognitive abilities may be better at evaluating and comparing sexual ornaments, even when the difference in ornaments is small. While brain size is often used as a proxy for cognitive ability, its effect on mate choice has rarely been investigated. Here, we investigate the effect of brain size on mate preferences in the pygmy halfbeak Dermogenys collettei, a small freshwater fish that forms mixed-sex shoals where mating takes place. Pygmy halfbeaks are ideal models as their semi-transparent heads allow for external brain measurements. After validating the use of external measurements as a proxy for internal brain size, we presented females with large or small brains (relative to body length) with two males that had either a large or small difference in sexual ornamentation (measured by the total area of red coloration). Unexpectedly, neither total relative brain size nor relative telencephalon size affected any measured aspect of mate preference. However, the difference in male sexual ornamentation did affect preference, with females preferring males with a smaller area of red coloration when the difference in ornaments was large. This study highlights the complexities of mate choice and the importance of considering a range of stimuli when examining mate preferences., Does a bigger brain make you better at choosing a good mate? Using a small fish called a pygmy halfbeak, we show that females with bigger brains are not better at choosing mates compared to females with smaller brains. However, we discovered that female preference depends on how different males are—females prefer males with less red coloration on their bodies when there is a big difference between the two males.

The rules of interaction that animals use to coordinate their movements are heritable and can evolve rapidly., Collective motion occurs when individuals use social interaction rules to respond to the movements and positions of their neighbors. How readily these social decisions are shaped by selection remains unknown. Through artificial selection on fish (guppies, Poecilia reticulata) for increased group polarization, we demonstrate rapid evolution in how individuals use social interaction rules. Within only three generations, groups of polarization-selected females showed a 15% increase in polarization, coupled with increased cohesiveness, compared to fish from control lines. Although lines did not differ in their physical swimming ability or exploratory behavior, polarization-selected fish adopted faster speeds, particularly in social contexts, and showed stronger alignment and attraction responses to multiple neighbors. Our results reveal the social interaction rules that change when collective behavior evolves.

Understanding the basis of behavior requires dissecting the complex waves of gene expression that underlie how the brain processes stimuli and produces an appropriate response. In order to determine the dynamic nature of the neurogenomic network underlying mate choice, we use transcriptome sequencing to capture the female neurogenomic response in two brain regions involved in sensory processing and decision-making under different mating and social contexts. We use differential coexpression (DC) analysis to evaluate how gene networks in the brain are rewired when a female evaluates attractive and nonattractive males, greatly extending current single-gene approaches to assess changes in the broader gene regulatory network. We find the brain experiences a remarkable amount of network rewiring in the different mating and social contexts we tested. Further analysis indicates the network differences across contexts are associated with behaviorally relevant functions and pathways, particularly learning, memory and other cognitive functions. Finally, we identify the loci that display social context-dependent connections, revealing the basis of how relevant neurological and metabolic pathways are differentially recruited in distinct social contexts. More broadly, our findings contribute to our understanding of the genetics of mating and social behavior by identifying gene drivers behind behavioral neural processes, illustrating the utility of DC analysis in neurosciences and behavior.

Reversal 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., Summary: Relative brain size affects differences in advanced learning ability in small- and large-brained female guppies; however, regardless of brain size, they do not learn a generalized rule from earlier experience.

Collective movement is achieved when individuals adopt local rules to interact with their neighbours. How the brain processes information about neighbours’ positions and movements may affect how individuals interact in groups. As brain size can determine such information processing it should impact collective animal movement. Here we investigate whether brain size affects the structure and organisation of newly forming fish shoals by quantifying the collective movement of guppies (Poecilia reticulata) from large- and small-brained selection lines, with known differences in learning and memory. We used automated tracking software to determine shoaling behaviour of single-sex groups of eight or two fish and found no evidence that brain size affected the speed, group size, or spatial and directional organisation of fish shoals. Our results suggest that brain size does not play an important role in how fish interact with each other in these types of moving groups of unfamiliar individuals. Based on these results, we propose that shoal dynamics are likely to be governed by relatively basic cognitive processes that do not differ in these brain size selected lines of guppies.

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.

1. In social contexts, animal behaviour is often studied in terms of group-level characteristics. One clear example of this is the collective motion of animals in decentralized structures, such as ...

The evolution of collective behaviour has been proposed to have important effects on individual cognitive abilities. Yet, in what way they are related remains enigmatic. In this context, the ‘distributed cognition’ hypothesis suggests that reliance on other group members relaxes selection for individual cognitive abilities. Here, we test how cognitive processes respond to evolutionary changes in collective motion using replicate lines of guppies (Poecilia reticulata) artificially selected for the degree of schooling behaviour (group polarization) with >15% difference in schooling propensity. We assessed associative learning in females of these selection lines in a series of cognitive assays: colour associative learning, reversal-learning, social associative learning, and individual and collective spatial associative learning. We found that control females were faster than polarization selected females at fulfilling a learning criterion only in the colour associative learning assay, but they were also less likely to reach a learning criterion in the individual spatial associative learning assay. Hence, although testing several cognitive domains, we found weak support for the distributed cognition hypothesis. We propose that any cognitive implications of selection for collective behaviour lie outside of the cognitive abilities included in food-motivated associative learning for visual and spatial cues.

We read with great interest the recent work in PNAS by Bergero et al. (1) describing differences in male and female recombination patterns on the guppy ( Poecilia reticulata ) sex chromosome. We fully agree that recombination in males is largely confined to the ends of the sex chromosome. Bergero et al. interpret these results to suggest that our previous findings of population-level variation in the degree of sex chromosome differentiation in this species (2) are incorrect. However, we suggest that their results are entirely consistent with our previous report, and that their interpretation presents a false controversy. Our population genomic results indicate that crossing over between the X and Y is rare across most of … [↵][1]1To whom correspondence may be addressed. Email: a.e.wright{at}sheffield.ac.uk. [1]: #xref-corresp-1-1

Brain size varies greatly at all taxonomic levels. Feeding ecology, life history and sexual selection have been proposed as key components in generating contemporary diversity in brain size across vertebrates. Analyses of brain size evolution have, however, been limited to lineages where males predominantly compete for mating and females choose mates. Here, we present the first original data set of brain sizes in pipefishes and seahorses (Syngnathidae) a group in which intense female mating competition occurs in many species. After controlling for the effect of shared ancestry and overall body size, brain size was positively correlated with relative snout length. Moreover, we found that females, on average, had 4.3% heavier brains than males and that polyandrous species demonstrated more pronounced (11.7%) female-biased brain size dimorphism. Our results suggest that adaptations for feeding on mobile prey items and sexual selection in females are important factors in brain size evolution of pipefishes and seahorses. Most importantly, our study supports the idea that sexual selection plays a major role in brain size evolution, regardless of on which sex sexual selection acts stronger.

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

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 (

Despite the common assumption that the brain is mainly malleable to surrounding conditions 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 for 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.

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.

We published a study recently testing the link between brain size and behavioural plasticity using brain size selected guppy (Poecilia reticulata) lines (2019, Journal of Evolutionary Biology, 32, 218-226). Only large-brained fish showed habituation to a new, but actually harmless environment perceived as risky, by increasing movement activity over the 20-day observation period. We concluded that "Our results suggest that brain size likely explains some of the variation in behavioural plasticity found at the intraspecific level". In a commentary published in the same journal, Haave-Audet et al. challenged the main message of our study, stating that (a) relative brain size is not a suitable proxy for cognitive ability and (b) habituation measured by us is likely not adaptive and costly. In our response, we first show that a decade's work has proven repeatedly that relative brain size is indeed positively linked to cognitive performance in our model system. Second, we discuss how switching from stressed to unstressed behaviour in stressful situations without real risk is likely adaptive. Finally, we point out that the main cost of behavioural plasticity in our case is the development and maintenance of the neural system needed for information processing, and not the expression of plasticity. We hope that our discussion with Haave-Audet et al. helps clarifying some central issues in this emerging research field.

Snapshot analyses have demonstrated dramatic intraspecific variation in the degree of brain sexual size dimorphism (SSD). Although brain SSD is believed to be generated by the sex-specific cognitive demands of reproduction, the relative roles of developmental and population specific contributions to variation in brain SSD remain little studied. Using a common garden experiment, we tested for sex-specific changes in brain anatomy over the breeding cycle in three-spined stickleback (Gasterosteus aculeatus) sampled from four locations in Northern Europe. We found that the male brain increased in size (ca. 24%) significantly more than the female brain towards breeding, and that the resulting brain SSD was similar (ca. 20%) for all populations over the breeding cycle. Our findings support the notion that the stickleback brain is highly plastic and changes over the breeding cycle, especially in males, likely as an adaptive response to the cognitive demands of reproduction (e.g. nest construction and parental care). The results also provide evidence to suggest that breeding-related changes in brain size may be the reason for the widely varying estimates of brain SSD across studies of this species, cautioning against interpreting brain size measurements from a single time-point as fixed/static.

Understanding how animal personality (consistent between-individual behavioural differences) arises has become a central topic in behavioural sciences. This endeavour is complicated by the fact that not only the mean behaviour of individuals (behavioural type) but also the strength of their reaction to environmental change (behavioural plasticity) varies consistently. Personality and cognitive abilities are linked, and we suggest that behavioural plasticity could also be explained by differences in brain size (a proxy for cognitive abilities), since accurate decisions are likely essential to make behavioural plasticity beneficial. We test this idea in guppies (Poecilia reticulata), artificially selected for large and small brain size, which show clear cognitive differences between selection lines. To test whether those lines differed in behavioural plasticity, we reared them in groups in structurally enriched environments and then placed adults individually into empty tanks, where we presented them daily with visual predator cues and monitored their behaviour for 20 days with video-aided motion tracking. We found that individuals differed consistently in activity and risk-taking, as well as in behavioural plasticity. In activity, only the large-brained lines demonstrated habituation (increased activity) to the new environment, whereas in risk-taking, we found sensitization (decreased risk-taking) in both brain size lines. We conclude that brain size, potentially via increasing cognitive abilities, may increase behavioural plasticity, which in turn can improve habituation to novel environments. However, the effects seem to be behaviour-specific. Our results suggest that brain size likely explains some of the variation in behavioural plasticity found at the intraspecific level.

Animals living in groups can show substantial variation in social traits and this affects their social organization. However, as the specific mechanisms driving this organization are difficult to identify in already organized groups typically found in the wild, the contribution of interindividual variation to group level behaviour remains enigmatic. Here, we present results of an experiment to create and compare groups that vary in social organization, and study how individual behaviour varies between these groups. We iteratively sorted individuals between groups of guppies, Poecilia reticulata, by ranking the groups according to their directional alignment and then mixing similar groups. Over the rounds of sorting the consistency of the group rankings increased, producing groups that varied significantly in key social behaviours such as collective activity and group cohesion. The repeatability of the underlying individual behaviour was then estimated by comparing the experimental data to simulations. At the level of basic locomotion, individuals in more coordinated groups displayed stronger interactions with the centre of the group, and weaker interactions with their nearest neighbours. We propose that this provides the basis for a passive phenotypic assortment mechanism that may explain the structures of social networks in the wild.

BackgroundBrain size is expected to evolve by a balance between cognitive benefits and energetic costs. Several influential hypotheses have suggested that large brains may be especially beneficial in social contexts. Group living and competition may pose unique cognitive challenges to individuals and favor the evolution of increased cognitive ability. Evidence comes from comparative studies on the link between social complexity and brain morphology, but the strength of empirical support has recently been challenged. In addition, the behavioral mechanisms that would link cognitive ability to sociality are rarely studied. Here we take an alternative approach and investigate experimentally how brain size can relate to the social competence of individuals within species, a problem that so far has remained unresolved. We use the unique guppy brain size selection line model system to evaluate whether large brains are advantageous by allowing individuals to better assess their performance in a social contest situation. Based on theoretical literature, we predict that contest duration should depend on the brain size of the loser, as it is the capitulation of the losing individual that ends the fight.ResultsFirst, we show that studying the movement of competitors during contests allows for precise estimation of the dominance timeline in guppies, even when overt aggression is typically one-sided and delayed. Second, we staged contests between pairs of male that had been artificially selected for large and small relative brain size, with demonstrated differences in cognitive ability. We show that dominance was established much earlier in contests with large-brained losers, whereas the brain size of the winner had no effect. Following our prediction, large-brained individuals gave up more quickly when they were going to lose.ConclusionsThese results suggest that large-brained individuals assess their performance in contests better and that social competence indeed can depend on brain size. Conflict resolution may therefore be an important behavioral mechanism behind macro-evolutionary patterns between sociality and brain size. Since conflict is ubiquitous among group-living animals, the possible effects of the social environment on the evolution of cognition may be more broadly applicable than previously thought.

The allometric relationship between brain and body size among vertebrates is often considered a manifestation of evolutionary constraints. However, birds and mammals have undergone remarkable encephalization, in which brain size has increased without corresponding changes in body size. Here, we explore the hypothesis that a reduction of phenotypic integration between brain and body size has facilitated encephalization in birds and mammals. Using a large dataset comprising 20,213 specimens across 4,587 species of jawed vertebrates, we show that the among-species (evolutionary) brain-body allometries are remarkably constant, both across vertebrate classes and across taxonomic levels. Birds and mammals, however, are exceptional in that their within-species (static) allometries are shallower and more variable than in other vertebrates. These patterns are consistent with the idea that birds and mammals have reduced allometric constraints that are otherwise ubiquitous across jawed vertebrates. Further exploration of ontogenetic allometries in selected taxa of birds, fishes and mammals reveals that birds and mammals have extended the period of fetal brain growth compared to fishes. Based on these findings, we propose that avian and mammalian encephalization has been contingent on increased variability in brain growth patterns.

In the courtship process, multiple signals are often used between the signaller and the receiver. Here we describe female response to multiple male visual morphological and behavioural signals in the swordtail characin, Corynopoma riisei. The swordtail characin is a species in which males display several morphological ornaments as well as a rich courtship repertoire. Our results show that high courtship intensity was associated with an increased female response towards the male ornament, increased number of mating attempts and a reduction in female aggression. The morphological aspects investigated here did not seem to correlate with female response. This may indicate that, when both behaviour and morphology are considered simultaneously, courtship behaviour may have priority over morphological cues in this species.

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.

Understanding the evolution of mate choice requires dissecting the mechanisms of female preference, particularly how these differ among social contexts and preference phenotypes. Here, we studied the female neurogenomic response after only 10 min of mate exposure in both a sensory component (optic tectum) and a decision-making component (telencephalon) of the brain. By comparing the transcriptional response between females with and without preferences for colourful males, we identified unique neurogenomic elements associated with the female preference phenotype that are not present in females without preference. A network analysis revealed different properties for this response at the sensory-processing and the decision-making levels, and we show that this response is highly centralized in the telencephalon. Furthermore, we identified an additional set of genes that vary in expression across social contexts, beyond mate evaluation. We show that transcription factors among these loci are predicted to regulate the transcriptional response of the genes we found to be associated with female preference.

Many genes are subject to contradictory selection pressures in males and females, and balancing selection resulting from sexual conflict has the potential to substantially increase standing genetic diversity in populations and thereby act as an important force in adaptation. However, the underlying causes of sexual conflict, and the potential for resolution, remains hotly debated. Using transcriptome-resequencing data from male and female guppies, we use a novel approach, combining patterns of genetic diversity and intersexual divergence in allele frequency, to distinguish the different scenarios that give rise to sexual conflict, and how this conflict may be resolved through regulatory evolution. We show that reproductive fitness is the main source of sexual conflict, and this is resolved via the evolution of male-biased expression. Furthermore, resolution of sexual conflict produces significant differences in genetic architecture between males and females, which in turn lead to specific alleles influencing sex-specific viability. Together, our findings suggest an important role for sexual conflict in shaping broad patterns of genome diversity, and show that regulatory evolution is a rapid and efficient route to the resolution of conflict.

Understanding what drives animal decisions is fundamental in evolutionary biology, and mate choice decisions are arguably some of the most important decisions in any individual's life. As cognitive ability can impact decision-making, elucidating the link between mate choice and cognitive ability is necessary to fully understand mate choice. To experimentally study this link, we used guppies (Poecilia reticulata) artificially selected for divergence in relative brain size and with previously demonstrated differences in cognitive ability. A previous test in our female guppy selection lines demonstrated the impact of brain size and cognitive ability on information processing during female mate choice decisions. Here we evaluated the effect of brain size and cognitive ability on male mate choice decisions. Specifically, we investigated the preferences of large-brained, small-brained, and non-selected guppy males for female body size, a key indicator of female fecundity in this species. For this, male preferences were quantified in dichotomous choice tests when presented to dyads of females with small, medium and large body size differences. All types of males showed preference for larger females but no effect of brain size was found in the ability to discriminate between differently sized females. However, we found that non-selected and large-brained males, but not small-brained males, showed context-dependent preferences for larger females depending on the difference in female size. Our results have two important implications. First, they provide further evidence that male mate choice occurs also in a species in which secondary sexual ornamentation occurs only in males. Second, they show that brain size and cognitive ability have important effects on individual variation in mating preferences and sexually selected traits.

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 statement Pre-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. Electronic supplementary material The online version of this article (10.1007/s00265-017-2408-z) contains supplementary material, which is available to authorized users.

It has become increasingly clear that a larger brain can confer cognitive benefits. Yet not all of the numerous aspects of cognition seem to be affected by brain size. Recent evidence suggests that some more basic forms of cognition, for instance colour vision, are not influenced by brain size. We therefore hypothesize that a larger brain is especially beneficial for distinct and gradually more complex aspects of cognition. To test this hypothesis, we assessed the performance of brain size selected female guppies ( Poecilia reticulata ) in two distinct aspects of cognition that differ in cognitive complexity. In a standard reversal-learning test we first investigated basic learning ability with a colour discrimination test, then reversed the reward contingency to specifically test for cognitive flexibility. We found that large-brained females outperformed small-brained females in the reversed-learning part of the test but not in the colour discrimination part of the test. Large-brained individuals are hence cognitively more flexible, which probably yields fitness benefits, as they may adapt more quickly to social and/or ecological cognitive challenges. Our results also suggest that a larger brain becomes especially advantageous with increasing cognitive complexity. These findings corroborate the significance of brain size for cognitive evolution.

The predation pressure data were collected by AEM and AED as part of an ERC-funded project (BioTIME 250189), AEM was supported by the Royal Society, AK and NK were supported by the Knut and Alice Wallenberg Foundation (KAW2013.0072 to NK). There is remarkable diversity in brain anatomy among vertebrates and evidence is accumulating that predatory interactions are crucially important for this diversity. To test this hypothesis, we collected female guppies (Poecilia reticulata) from 16 wild populations and related their brain anatomy to several aspects of predation pressure in this ecosystem, such as the biomass of the four major predators of guppies (one prawn and three fish species), and predator diversity (number of predatory fish species in each site). We found that populations from localities with higher prawn biomass had relatively larger telencephalon size as well as larger brains. Optic tectum size was positively associated with one of the fish predator’s biomass and with overall predator diversity. However, both olfactory bulb and hypothalamus size were negatively associated with the biomass of another of the fish predators. Hence, while fish predator occurrence is associated with variation in brain anatomy, prawn occurrence is associated with variation in brain size. Our results suggest that cognitive challenges posed by local differences in predator communities may lead to changes in prey brain anatomy in the wild. Publisher PDF

Pheromones constitute an important cue used by both males and females during courtship. Here, we investigate the effect of male pheromones on female behaviour in the swordtail characin (Corynopoma ...

Female response to various aspects of male trait morphology and the effect of female feeding motivation were investigated in the swordtail characin Corynopoma riisei, a species where males are equipped with a flag-like food-mimicking ornament that grows from the operculum. Unfed females responded more strongly to the male ornament and showed a stronger preference for larger ornaments than did fed females. Females were shown not to discriminate between artificial male ornaments of either undamaged or damaged shape.