Relative telencephalon size does not affect collective motion in the guppy (Poecilia reticulata).

Collective motion is common across all animal taxa, from swarming insects to schools of fish. The collective motion requires intricate behavioral integration among individuals, yet little is known about how evolutionary changes in brain morphology influence the ability for individuals to coordinate behavior in groups. In this study, we utilized guppies that were selectively bred for relative telencephalon size, an aspect of brain morphology that is normally associated with advanced cognitive functions, to examine its role in collective motion using an open-field assay. We analyzed high-resolution tracking data of same-sex shoals consisting of 8 individuals to assess different aspects of collective motion, such as alignment, attraction to nearby shoal members, and swimming speed. Our findings indicate that variation in collective motion in guppy shoals might not be strongly affected by variation in relative telencephalon size. Our study suggests that group dynamics in collectively moving animals are likely not driven by advanced cognitive functions but rather by fundamental cognitive processes stemming from relatively simple rules among neighboring individuals.

Social complexity affects cognitive abilities but not brain structure in a Poeciliid fish.

Some cognitive abilities are suggested to be the result of a complex social life, allowing individuals to achieve higher fitness through advanced strategies. However, most evidence is correlative. Here, we provide an experimental investigation of how group size and composition affect brain and cognitive development in the guppy (Poecilia reticulata). For 6 months, we reared sexually mature females in one of 3 social treatments: a small conspecific group of 3 guppies, a large heterospecific group of 3 guppies and 3 splash tetras (Copella arnoldi)-a species that co-occurs with the guppy in the wild, and a large conspecific group of 6 guppies. We then tested the guppies' performance in self-control (inhibitory control), operant conditioning (associative learning), and cognitive flexibility (reversal learning) tasks. Using X-ray imaging, we measured their brain size and major brain regions. Larger groups of 6 individuals, both conspecific and heterospecific groups, showed better cognitive flexibility than smaller groups but no difference in self-control and operant conditioning tests. Interestingly, while social manipulation had no significant effect on brain morphology, relatively larger telencephalons were associated with better cognitive flexibility. This suggests alternative mechanisms beyond brain region size enabled greater cognitive flexibility in individuals from larger groups. Although there is no clear evidence for the impact on brain morphology, our research shows that living in larger social groups can enhance cognitive flexibility. This indicates that the social environment plays a role in the cognitive development of guppies.

Functional convergence of genomic and transcriptomic architecture underlies schooling behaviour in a live-bearing fish.

The organization and coordination of fish schools provide a valuable model to investigate the genetic architecture of affiliative behaviours and dissect the mechanisms underlying social behaviours and personalities. Here we used replicate guppy selection lines that vary in schooling propensity and combine quantitative genetics with genomic and transcriptomic analyses to investigate the genetic basis of sociability phenotypes. We show that consistent with findings in collective motion patterns, experimental evolution of schooling propensity increased the sociability of female, but not male, guppies when swimming with unfamiliar conspecifics. This finding highlights a relevant link between coordinated motion and sociability for species forming fission-fusion societies in which both group size and the type of social interactions are dynamic across space and time. We further show that 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 behaviours, with important variation across sexes. The results from both Pool-seq and RNA-seq data indicated that genes involved in neuron migration and synaptic function were instrumental in the evolution of sociability, highlighting a crucial role of glutamatergic synaptic function and calcium-dependent signalling processes in the evolution of schooling.

Genetic and context-specific effects on individual inhibitory control performance in the guppy (Poecilia reticulata).

Among-individual variation in cognitive traits, widely assumed to have evolved under adaptive processes, is increasingly being demonstrated across animal taxa. As variation among individuals is required for natural selection, characterizing individual differences and their heritability is important to understand how cognitive traits evolve. Here, we use a quantitative genetic study of wild-type guppies repeatedly exposed to a 'detour task' to test for genetic variance in the cognitive trait of inhibitory control. We also test for genotype-by-environment interactions (GxE) by testing related fish under alternative experimental treatments (transparent vs. semi-transparent barrier in the detour-task). We find among-individual variation in detour task performance, consistent with differences in inhibitory control. However, analysis of GxE reveals that heritable factors only contribute to performance variation in one treatment. This suggests that the adaptive evolutionary potential of inhibitory control (and/or other latent variables contributing to task performance) may be highly sensitive to environmental conditions. The presence of GxE also implies that the plastic response of detour task performance to treatment environment is genetically variable. Our results are consistent with a scenario where variation in individual inhibitory control stems from complex interactions between heritable and plastic components.

Evolution of schooling drives changes in neuroanatomy and motion characteristics across predation contexts in guppies.

One of the most spectacular displays of social behavior is the synchronized movements that many animal groups perform to travel, forage and escape from predators. However, elucidating the neural mechanisms underlying the evolution of collective behaviors, as well as their fitness effects, remains challenging. Here, we study collective motion patterns with and without predation threat and predator inspection behavior in guppies experimentally selected for divergence in polarization, an important ecological driver of coordinated movement in fish. We find that groups from artificially selected lines remain more polarized than control groups in the presence of a threat. Neuroanatomical measurements of polarization-selected individuals indicate changes in brain regions previously suggested to be important regulators of perception, fear and attention, and motor response. Additional visual acuity and temporal resolution tests performed in polarization-selected and control individuals indicate that observed differences in predator inspection and schooling behavior should not be attributable to changes in visual perception, but rather are more likely the result of the more efficient relay of sensory input in the brain of polarization-selected fish. Our findings highlight that brain morphology may play a fundamental role in the evolution of coordinated movement and anti-predator behavior.

Experimental expansion of relative telencephalon size improves the main executive function abilities in guppy.

Executive functions are a set of cognitive control processes required for optimizing goal-directed behavior. Despite more than two centuries of research on executive functions, mostly in humans and nonhuman primates, there is still a knowledge gap in what constitutes the mechanistic basis of evolutionary variation in executive function abilities. Here, we show experimentally that size changes in a forebrain structure (i.e. telencephalon) underlie individual variation in executive function capacities in a fish. For this, we used male guppies (Poecilia reticulata) issued from artificial selection lines with substantial differences in telencephalon size relative to the rest of the brain. We tested fish from the up- and down-selected lines not only in three tasks for the main core executive functions: cognitive flexibility, inhibitory control, and working memory, but also in a basic conditioning test that does not require executive functions. Individuals with relatively larger telencephalons outperformed individuals with smaller telencephalons in all three executive function assays but not in the conditioning assay. Based on our findings, we propose that the telencephalon is the executive brain in teleost fish. Together, it suggests that selective enlargement of key brain structures with distinct functions, like the fish telencephalon, is a potent evolutionary pathway toward evolutionary enhancement of advanced cognitive abilities in vertebrates.

Evolution of relative brain size in dogs-no effects of selection for breed function, litter size, or longevity.

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.

Brain morphology correlates of learning and cognitive flexibility in a fish species (Poecilia reticulata).

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.

Artificial mosaic brain evolution of relative telencephalon size improves inhibitory control abilities in the guppy (Poecilia reticulata).

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.

Does brain size affect mate choice? An experimental examination in pygmy halfbeaks.

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.

Rapid mosaic brain evolution under artificial selection for relative telencephalon size in the guppy (Poecilia reticulata).

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.

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

Cognitive ageing is the general process when certain mental skills gradually deteriorate with age. Across species, there is a pattern of a slower brain structure degradation rate in large-brained species. Hence, having a larger brain might buffer the impact of cognitive ageing and positively affect survival at older age. However, few studies have investigated the link between relative brain size and cognitive ageing at the intraspecific level. In particular, experimental data on how brain size affects brain function also into higher age is largely missing. We used 288 female guppies (Poecilia reticulata), artificially selected for large and small relative brain size, to investigate variation in colour discrimination and behavioural flexibility, at 4-6, 12 and 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.

Different mating contexts lead to extensive rewiring of female brain coexpression networks in the guppy.

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.

Rapid evolution of coordinated and collective movement in response to artificial selection.

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.

Artificial selection for schooling behaviour and its effects on associative learning abilities.

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 tested 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.

The link between selection for function and human-directed play behaviour in dogs.

Human-directed play behaviour is a distinct behavioural feature of domestic dogs. But the role that artificial selection for contemporary dog breeds has played for human-directed play behaviour remains elusive. Here, we investigate how human-directed play behaviour has evolved in relation to the selection for different functions, considering processes of shared ancestry and gene flow among the different breeds. We use the American Kennel Club (AKC) breed group categorization to reflect the major functional differences and combine this with observational data on human-directed play behaviour for over 132 breeds across 89 352 individuals from the Swedish Dog Mentality Assessment project. Our analyses demonstrate that ancestor dogs already showed intermediate levels of human-directed play behaviour, levels that are shared with several modern breed types. Herding and Sporting breeds display higher levels of human-directed play behaviour, statistically distinguishable from Non-sporting and Toy breeds. Our results suggest that human-directed play behaviour played a role in the early domestication of dogs and that subsequent artificial selection for function has been important for contemporary variation in a behavioural phenotype mediating the social bond with humans.

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

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.

Brain size affects responsiveness in mating behaviour to variation in predation pressure and sex ratio.

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 role of common ancestry and gene flow in the evolution of human-directed play behaviour in dogs.

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.