Limited effects of culling on the behavior of invasive lionfish (Pterois miles) in the Mediterranean.

Invasive species pose serious threats to ecosystems. To reduce ecological and economic consequences of invasions, efforts are made to control invaders and evaluating the effects of such efforts is paramount. Lionfishes (Pterois volitans and Pterois miles) are native to the Indo-Pacific Ocean and pose a major threat to local ecosystems in the invaded Atlantic and Mediterranean. Culling via spearfishing is a widespread measure to limit lionfish population size in invaded ranges. However, like most hunted fishes, lionfish alter their behavior after repeated culling, potentially decreasing the effectiveness of future culls. Previous studies on lionfish in the Caribbean have shown that lionfish are less bold after repeated culling. However, the impact of culling on lionfish in their newest invasive range, the Mediterranean, remains enigmatic. To determine the behavioral changes in response to culling in this second area of invasion, we tested for effects of culling on the behavior of lionfish in Cyprus, a region heavily impacted by the lionfish invasion in the Mediterranean. We compared the response of lionfish to an approaching free diver holding a metal pole (imitating a spear fisher) between protected areas where spearfishing is restricted and areas where culls are frequently conducted. We also assessed whether activity, hiding pattern, and site fidelity differed between these culled and unculled sites. Overall, we found limited effects of culling on the traits measured, indicating surprising resistance to culling-induced behavioral changes in Mediterranean lionfish. Future studies should monitor invasive lionfish population densities and the effects of culling in more detail to tailor management plans and reduce the negative effects of these fish in specific invaded ranges.

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.

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.

Artificial selection for reversal learning reveals limited repeatability and no heritability of cognitive flexibility in great tits (Parus major).

Cognitive flexibility controls how animals respond to changing environmental conditions. Individuals within species vary considerably in cognitive flexibility but the micro-evolutionary potential in animal populations remains enigmatic. One prerequisite for cognitive flexibility to be able to evolve is consistent and heritable among-individual variation. Here we determine the repeatability and heritability of cognitive flexibility among great tits (Parus major) by performing an artificial selection experiment on reversal learning performance using a spatial learning paradigm over three generations. We found low, yet significant, repeatability (R = 0.15) of reversal learning performance. Our artificial selection experiment showed no evidence for narrow-sense heritability of associative or reversal learning, while we confirmed the heritability of exploratory behaviour. We observed a phenotypic, but no genetic, correlation between associative and reversal learning, showing the importance of prior information on reversal learning. We found no correlation between cognitive and personality traits. Our findings emphasize that cognitive flexibility is a multi-faceted trait that is affected by memory and prior experience, making it challenging to retrieve reliable values of temporal consistency and assess the contribution of additive genetic variation. Future studies need to identify what cognitive components underlie variation in reversal learning and study their between-individual and additive genetic components.

Insights from the judgement bias paradigm: social group and tank size do not affect mental state in female guppies.

Optimal holding conditions are key to animal welfare. How stressful husbandry is perceived by the animal can be determined via an assessment of an animal's mental state - where it is positioned on the continuum between optimistic and pessimistic states - and can be measured using the judgement bias paradigm. In this test, individuals are trained to distinguish a rewarded from an unrewarded cue before being presented an ambiguous, intermediate cue. The response time to the ambiguous cue is then indicative of mental state. A shorter latency suggests a more positive (optimistic) mental state and a longer latency a more negative (pessimistic) mental state. Here, the authors used the judgement bias paradigm to assess the impact of standard laboratory housing conditions on the mental states of female guppies (Poecilia reticulata). As it is debated which holding conditions confer optimal welfare, they tested the impact of husbandry on mental state by keeping animals for 3 weeks in small or large social groups in either small or large tanks. They found that the different standard housing conditions used did not lead to differences in mental state. As an unexpected side result, they found that female guppies seem lateral. Their findings of comparable mental state across housing conditions suggest either that guppies perceive the tested conditions as equally stressful or, alternatively, that guppies are relatively resilient to the combination of group and tank sizes tested in this study. The authors conclude that the judgement bias paradigm can be a useful tool to assess fish welfare.

Predation impacts brain allometry in female guppies (Poecilia reticulata).

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.

Jumping out of trouble: evidence for a cognitive map in guppies (Poecilia reticulata).

Spatial cognitive abilities allow individuals to remember the location of resources such as food patches, predator hide-outs, or shelters. Animals typically incorporate learned spatial information or use external environmental cues to navigate their surroundings. A spectacular example of how some fishes move is through aerial jumping. For instance, fish that are trapped within isolated pools, cut off from the main body of water during dry periods, may jump over obstacles and direct their jumps to return to safe locations. However, what information such re-orientation behavior during jumping is based on remains enigmatic. Here we combine a lab and field experiment to test if guppies (Poecilia reticulata) incorporate learned spatial information and external environmental cues (visual and auditory) to determine where to jump. In a spatial memory assay we found that guppies were more likely to jump towards deeper areas, hence incorporating past spatial information to jump to safety. In a matched versus mismatched spatial cue experiment in the field, we found that animals only showed directed jumping when visual and auditory cues matched. We show that in unfamiliar entrapments guppies direct their jumps by combining visual and auditory cues, whereas in familiar entrapments they use a cognitive map. We hence conclude that jumping behavior is a goal-directed behavior, guided by different sources of information and involving important spatial cognitive skills.

The effect of experimental hybridization on cognition and brain anatomy: Limited phenotypic variation and transgression in Poeciliidae.

Hybridization can promote phenotypic variation and often produces trait combinations distinct from the parental species. This increase in available variation can lead to the manifestation of functional novelty when new phenotypes bear adaptive value under the environmental conditions in which they occur. Although the role of hybridization as a driver of variation and novelty in traits linked to fitness is well recognized, it remains largely unknown whether hybridization can fuel behavioral novelty by promoting phenotypic variation in brain morphology and/or cognitive traits. To address this question, we investigated the effect of hybridization on brain anatomy, learning ability, and cognitive flexibility in first- and second-generation hybrids of two closely related fish species (Poecilia reticulata and Poecilia wingei). Overall, we found that F1 and F2 hybrids showed intermediate brain morphology and cognitive traits compared to parental groups. Moreover, as phenotypic dispersion and transgression were low for both brain and cognitive traits, we suggest that hybridization is not a strong driver of brain anatomical and cognitive diversification in these Poeciliidae. To determine the generality of this conclusion, hybridization experiments with cognitive tests need to be repeated in other families.

Hybridization May Promote Variation in Cognitive Phenotypes in Experimental Guppy Hybrids.

AbstractHybridization 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 remains 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 multidimensional cognitive phenotypes. We found that hybrids showed intermediate learning abilities in both tasks compared with the parentals. 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 hybridization may promote cognitive variation and generate new trait combinations, even when learning performance at the group level is intermediate between parentals.

The expensive-tissue hypothesis may help explain brain-size reduction during domestication.

Morphological traits, such as white patches, floppy ears and curly tails, are ubiquitous in domestic animals and are referred to as the 'domestication syndrome'. A commonly discussed hypothesis that has the potential to provide a unifying explanation for these traits is the 'neural crest/domestication syndrome hypothesis'. Although this hypothesis has the potential to explain most traits of the domestication syndrome, it only has an indirect connection to the reduction of brain size, which is a typical trait of domestic animals. We discuss how the expensive-tissue hypothesis might help explain brain-size reduction in domestication.

Cognition contra camouflage: How the brain mediates predator-driven crypsis evolution.

While crypsis is a prominent antipredator adaptation, the role of the brain in predator-driven evolution remains controversial. Resolving this controversy requires contextualizing the brain with established antipredator traits and predation pressure. We hypothesize that the reduced predation risk through crypsis relaxes predation-driven selection on the brain and provide comparative evidence across 102 Chinese frog species for our hypothesis. Specifically, our phylogenetic path analysis reveals an indirect relationship between predation risk and crypsis that is mediated by brain size. This result suggests that at a low predation risk, frogs can afford to be conspicuous and use their large brain for cognitive predator evasion. This strategy may become less efficient or energetically costlier under higher predation pressure, favoring smaller brains and instead increasing crypsis.

Sex-specific inbreeding depression: A meta-analysis.

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.

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.

Where are they now? Tracking the Mediterranean lionfish invasion via local dive centers.

Invasive species are globally on the rise due to human-induced environmental change and are often a source of harm to their new ecosystems. Tracking the spread of invaders is crucial to better manage invasive species, and citizen science is often used to collect sighting data. However, this can be unreliable due to the general public's limited expertise for accurate identification and a lack of clear absence data. Here, we introduce a refined method of citizen science by tracking the spread of the invasive lionfish (Pterois miles) in the Mediterranean Sea using dive centers' expertise on local marine wildlife. We contacted 1131 dive centers on the Mediterranean coast via email and received 216 responses reporting whether or not lionfish were present in their area and, if present, the year they were first sighted. Currently, lionfish sightings are observed in the eastern half of the Mediterranean, though the front is continuing to move west with the furthest sighting as far as Corfu, Greece (19.939423°E, 39.428017°N). In 2020, lionfish also expanded their invasive range north on the Turkish Aegean coast to Karaburun (26.520657°E, 38.637033°N), showing that the invasion is ongoing. We found that the invasive range is now exceeding previous invasion models, highlighting the need for additional research on lionfish biology to inform management efforts. Continuous monitoring of invasive fronts based on dive center reports and a better understanding of what makes lionfish so invasive is crucial to creating effective management strategies and mitigating their negative impact on native ecosystems.

Fast life-histories are associated with larger brain size in killifishes.

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.

Meta-analytic evidence that animals rarely avoid inbreeding.

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 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.