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.

Hybridization is an important mechanism of evolution. While hybrids often express inferior traits and are selected against, hybridization can promote phenotypic variation and produce trait combinations distinct from the parentals, generating novel adaptive potential. Among other traits, hybridization can impact behavior and cognition and may reinforce species boundaries when hybrids show decreased cognitive abilities. However, the hypothesized role of hybridization in the diversification of cognitive phenotypes re-mains enigmatic. To test this idea, we compare the performance of female guppies (Poecilia reticulata), Endler’s guppies (Poecilia wingei), and their experimental hybrids in color association and reversal learning. In addition, we introduce a new approach to compare mul-tidimensional cognitive phenotypes. We found that hybrids showed intermediate learning abilities in both tasks compared with the pa-rentals. Moreover, hybrids had slightly higher phenotypic dispersion, new trait combinations occurred in some hybrid individuals, and the mean phenotype of one hybrid group deviated away from the axis of variation of the parentals. Our method should hence be useful in further exploring how hybridization and other evolutionary processes impact behavioral and cognitive traits. Our results suggest that hy-bridization may promote cognitive variation and generate new trait combinations, even when learning performance at the group level is intermediate between parentals. 

Cognitive and sensory abilities are vital in affecting survival under predation risk, leading to selection on brain anatomy. However, how exactly predation and brain evolution are linked has not yet been resolved, as current empirical evidence is inconclusive. This may be due to predation pressure having different effects across life stages and/or due to confounding factors in ecological comparisons of predation pressure. Here, we used adult guppies (Poecilia reticulata) to experimentally test how direct predation during adulthood would impact the relative brain size and brain anatomy of surviving individuals to examine if predators selectively remove individuals with specific brain morphology. To this end, we compared fish surviving predation to control fish, which were exposed to visual and olfactory predator cues but could not be predated on. We found that predation impacted the relative size of female brains. However, this effect was dependent on body size, as larger female survivors showed relatively larger brains, while smaller survivors showed relatively smaller brains when compared to control females. We found no differences in male relative brain size between survivors and controls, nor for any specific relative brain region sizes for either sex. Our results corroborate the important, yet complex, role of predation as an important driver of variation in brain size. 

Inbreeding depression, the reduced fitness of the offspring of related individuals, can affect males and females differently. Although a comprehensive theoretical framework describing the causes of sex-specific inbreeding depression is lacking, empirical evidence suggests that often one sex tends to be more vulnerable than the other. However, the generality, direction, and degree of sex-specific difference in inbreeding depression remains enigmatic as studies on this topic have reported conflicting results. Here, we conduct a meta-analysis to test for sex-specific differences in the magnitude of inbreeding depression. We synthetised 321 effect sizes of experimental studies across 47 species and found a small difference in inbreeding depression between the sexes: females suffered slightly higher inbreeding depression than males. Furthermore, a higher inbreeding coefficient was correlated with higher inbreeding depression. However, there was a large amount of heterogeneity that remained unexplained, even when considering different factors that could affect inbreeding between the sexes, such as sexual size dimorphism, heterogamety, the type of trait measured and whether animals were tested in a stressful environment. As such, we highlight the need to further explore inbreeding depression across different species to determine the occurrence and causes of sex differences to increase our understanding of the evolutionary consequences of sex-specific inbreeding depression.

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.

Predation risk during early ontogeny can impact developmental trajectories and permanently alter adult phenotypes. Such phenotypic plasticity often leads to adaptive changes in traits involved in anti-predator responses. While plastic changes in cognition may increase survival, it remains unclear whether early predation experience shapes cognitive investment and drives developmental plasticity in cognitive abilities. Here, we show that predation risk during early ontogeny induces developmental plasticity in two cognitive domains. We reared female guppies Poecilia reticulata with and without predator cues and tested their adult cognitive abilities. We found that females reared under simulated predation took longer to learn a simple association task, yet outperformed animals reared without predation threat in a reversal learning task testing cognitive flexibility. These results show that predation pressure during ontogeny shapes adult cognitive abilities, which we argue is likely to be adaptive. Our study highlights the important role of predator-mediated developmental plasticity on cognitive investment in natural populations and the general role of plasticity in cognitive performance.

The high energetic demands associated with the vertebrate brain are proposed to result in a trade-off between the pace of life-history and relative brain size. However, because both life-history and brain size also have a strong relationship with body size, any associations between the pace of life-history and relative brain size may be confounded by coevolution with body size. Studies on systems where contrasts in the pace of life-history occur without concordant contrasts in body size could therefore add to our understanding of the potential coevolution between relative brain size and life-history. Using one such system - 21 species of killifish - we employed a common garden design across two ontogenetic stages to investigate the association between relative brain size and the pace of life-history. Contrary to predictions, we found that relative brain size was larger in adult fast-living killifishes, compared to slow-living species. Although we found no differences in relative brain size between juvenile killifishes. Our results suggest that fast- and slow-living killifishes do not exhibit the predicted trade-off between brain size and life-history. Instead, fast and slow-living killifishes could differ in the ontogenetic timing of somatic versus neural growth or inhabit environments that differ considerably in cognitive demands.

Animals are usually expected to avoid mating with relatives (kin avoidance) as incestuous mating can lead to the expression of inbreeding depression. Yet, theoretical models predict that unbiased mating with regards to kinship should be common, and that under some conditions, the inclusive fitness benefits associated with inbreeding can even lead to a preference for mating with kin. This mismatch between empirical and theoretical expectations generates uncertainty as to the prevalence of inbreeding avoidance in animals. Here, we synthesized 677 effect sizes from 139 experimental studies of mate choice for kin versus non-kin in diploid animals, representing 40 years of research, using a meta-analytical approach. Our meta-analysis revealed little support for the widely held view that animals avoid mating with kin, despite clear evidence of publication bias. Instead, unbiased mating with regards to kinship appears widespread across animals and experimental conditions. The significance of a variety of moderators was explored using meta-regressions, revealing that the degree of relatedness and prior experience with kin explained some variation in the effect sizes. Yet, we found no difference in kin avoidance between males and females, choice and no-choice experiments, mated and virgin animals or between humans and animals. Our findings highlight the need to rethink the widely held view that inbreeding avoidance is a given in experimental studies.

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.