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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.

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.

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.

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.

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

In many species, males exhibit phenotypic plasticity in sexually selected traits when exposed to social cues about the intensity of sexual competition. To date, however, few studies have tested how this plasticity affects male reproductive success. We initially tested whether male mosquitofish,Gambusia holbrooki(Poeciliidae), change their investment in traits under pre- and postcopulatory sexual selection depending on the social environment. For a full spermatogenesis cycle, focal males were exposed to visual and chemical cues of rivals that were either present (competitive treatment) or absent (control). Males from the competitive treatment had significantly slower-swimming sperm but did not differ in sperm count from control males. When two males competed for a female, competitive treatment males also made significantly fewer copulation attempts and courtship displays than control males. Further, paternity analysis of 708 offspring from 148 potential sires, testing whether these changes in reproductive traits affected male reproductive success, showed that males previously exposed to cues about the presence of rivals sired significantly fewer offspring when competing with a control male. We discuss several possible explanations for these unusual findings.

Predation is a near ubiquitous factor of nature and a powerful selective force on prey. Moreover, it has recently emerged as an important driver in the evolution of brain anatomy, though population comparisons show ambiguous results with considerable unexplained variation. Here, we test the reproducibility of reduced predation on evolutionary trajectories of brain evolution. We make use of an introduction experiment, whereby guppies (Poecilia reticulata) from a single high predation stream were introduced to four low predation streams. After 8-9 years of natural selection in the wild and two generations of common garden conditions in the laboratory, we quantified brain anatomy. Relative brain region sizes did not differ between populations. However, we found a general increase and striking variation in relative brain size of introduced populations, which varied from no change to a 12.5% increase in relative brain weight, relative to the ancestral high predation population. We interpret this as evidence for non-parallel evolution, which implies a weak or inconsistent association of relative brain size with fitness in low predation sites. The evolution of brain anatomy appears sensitive to unknown environmental factors, or contingent on either chance events or historical legacies of environmental change.

Many animals undergo complete metamorphosis, where larval forms change abruptly in adulthood. Color change during ontogeny is common, but there is little understanding of evolutionary patterns in these changes. Here, we use data on larval and adult color for 246 butterfly species (61% of all species in Australia) to test whether the evolution of color is coupled between life stages. We show that adults are more variable in color across species than caterpillars and that male adult color has lower phylogenetic signal. These results suggest that sexual selection is driving color diversity in male adult butterflies at a broad scale. Moreover, color similarities between species at the larval stage do not predict color similarities at the adult stage, indicating that color evolution is decoupled between young and adult forms. Most species transition from cryptic coloration as caterpillars to conspicuous coloration as adults, but even species with conspicuous caterpillars change to different conspicuous colors as adults. The use of high-contrast coloration is correlated with body size in caterpillars but not adults. Taken together, our results suggest a change in the relative importance of different selective pressures at different life stages, resulting in the evolutionary decoupling of coloration through ontogeny.

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.

Many studies investigate the benefits of polyandry, but repeated interactions with males can lower female reproductive success. Interacting with males might even decrease offspring performance if it reduces a female's ability to transfer maternal resources. Male presence can be detrimental for females in two ways: by forcing females to mate at a higher rate and through costs associated with resisting male mating attempts. Teasing apart the relative costs of elevated mating rates from those of greater male harassment is critical to understand the evolution of mating strategies. Furthermore, it is important to test whether a male's phenotype, notably body size, has differential effects on female reproductive success versus the performance of offspring, and whether this is due to male body size affecting the costs of harassment or the actual mating rate. In the eastern mosquitofish Gambusia holbrooki, males vary greatly in body size and continually attempt to inseminate females. We experimentally manipulated male presence (i.e., harassment), male body size and whether males could copulate. Exposure to males had strong detrimental effects on female reproductive output, growth and immune response, independent of male size or whether males could copulate. In contrast, there was a little evidence of a cross-generational effect of male harassment or mating rate on offspring performance. Our results suggest that females housed with males pay direct costs due to reduced condition and offspring production and that these costs are not a consequence of increased mating rates. Furthermore, exposure to males does not affect offspring reproductive traits.

Predation is a near ubiquitous factor of nature and a powerful selective force on prey. Moreover, it has recently emerged as an important driver in the evolution of brain anatomy, though population comparisons show ambiguous results with considerable unexplained variation. Here, we test the reproducibility of reduced predation on evolutionary trajectories on brain evolution. We make use of an introduction experiment, whereby guppies (Poecilia reticulata) from a single high predation stream were introduced to four low predation streams. After 8–9 years of natural selection in the wild and two generations of common garden conditions in the laboratory, we quantified brain anatomy. Relative brain region sizes did not differ between populations. However, we found a general increase and striking variation in relative brain size of introduced populations, which varied from no change to a 12.5% increase in relative brain weight, relative to the ancestral high predation population. We interpret this as evidence for non-parallel evolution, which implies a weak or inconsistent association of relative brain size with fitness in low predation sites. The evolution of brain anatomy appears sensitive to unknown environmental factors, or contingent on either chance events or historical legacies of environmental change., Predation is a near ubiquitous factor of nature and a powerful selective force on prey. Moreover, it has recently emerged as an important driver in the evolution of brain anatomy, though population comparisons show ambiguous results with considerable unexplained variation. Here, we test the reproducibility of reduced predation on evolutionary trajectories on brain evolution. We make use of an introduction experiment, whereby guppies (Poecilia reticulata) from a single high predation stream were introduced to four low predation streams. After 8–9 years of natural selection in the wild and two generations of common garden conditions in the laboratory, we quantified brain anatomy. Relative brain region sizes did not differ between populations. However, we found a general increase and striking variation in relative brain size of introduced populations, which varied from no change to a 12.5% increase in relative brain weight, relative to the ancestral high predation population. We interpret this as evidence for non-parallel evolution, which implies a weak or inconsistent association of relative brain size with fitness in low predation sites. The evolution of brain anatomy appears sensitive to unknown environmental factors, or contingent on either chance events or historical legacies of environmental change.

Parental effects on offspring performance have been attributed to many factors such as parental age, size and condition. However, we know little about how these different parental characteristics interact to determine parental effects, or the extent to which their effect on offspring depends on either the sex of the parent or that of the offspring. Here we experimentally tested for effects of variation in parents' early diet and inbreeding levels, as well as effects of parental age, and for potential interactive effects of these three factors on key aspects of offspring development in the mosquitofish (Gambusia holbrooki). Older mothers produced offspring that were significantly smaller at birth. This negative effect of maternal age on offspring size was still evident at maturation as older mothers had smaller daughters, but not smaller sons. The daughters of older mothers did, however, reach maturity sooner. Paternal age did not affect offspring body size, but it had a complex effect on their sons' relative genital size. When initially raised on a food-restricted diet, older fathers sired sons with relatively smaller genitalia, but when fathers were initially raised on a control diet their sons had relatively larger genitalia. The inbreeding status of mothers and fathers had no significant effects on any of the measured offspring traits. Our results indicate that the manifestation of parental effects can be complex. It can vary with both parent and offspring sex; can change over an offspring's life; and is sometimes evident as an interaction between different parental traits. Understanding this complexity will be important to predict the role of parental effects in adaptation.

Mating with relatives has often been shown to negatively affect offspring fitness (inbreeding depression). There is considerable evidence for inbreeding depression due to effects on naturally selected traits, particularly those expressed early in life, but there is less evidence of it for sexually selected traits. This is surprising because sexually selected traits are expected to exhibit strong inbreeding depression. Here, we experimentally created inbred and outbred male mosquitofish (Gambusia holbrooki). Inbred males were the offspring of matings between full siblings. We then investigated how inbreeding influenced a number of sexually selected male traits, specifically: attractiveness, sperm number and velocity, as well as sperm competitiveness based on a male's share of paternity. We found no inbreeding depression for male attractiveness or sperm traits. There was, however, evidence that lower heterozygosity decreased paternity due to reduced sperm competitiveness. Our results add to the growing evidence that competitive interactions exacerbate the negative effects of the increased homozygosity that arises when there is inbreeding.

The detrimental effects of matings between relatives are well known. However, few studies determine the extent to which inbreeding depression in males is due to natural or sexual selection. Importantly, measuring fitness or key fitness components, rather than phenotypic traits allows more accurate estimation of inbreeding depression. We investigate how differences in inbreeding and juvenile diet (i.e. early stressful environment) influence a key component of male fitness, namely their reproductive success. We experimentally created inbred and outbred male mosquitofish (Gambusia holbrooki) by mating full-sibs (f = 0·25). We show that this led to a 23% reduction in genome-wide heterozygosity based on SNPs. Males were raised on different diets early in life to create high-stress and low-stress rearing environments. We then allowed adult males to compete freely for females to test if inbreeding, early diet and their interaction affect a male's share of paternity. Early diet had no effect on paternity, but outbred males sired almost twice as many offspring as inbred males (n = 628 offspring from 122 potential sires). Using artificial insemination methods we determined that this was unlikely to be due to early embryo mortality of eggs fertilised by inbred males: there was no evidence that male inbreeding status affects the realised fecundity of females (n = 288). Given there was no difference in male mortality in our competitive mating experiment, the lower reproductive success of inbred males can most parsimoniously be attributed to inbreeding negatively affecting sexually selected traits that affect male mating success and/or sperm competitiveness. We discuss which sexually selected traits might be involved.

BACKGROUND: Inbreeding is often associated with a decrease in offspring fitness (‘inbreeding depression’). Moreover, it is generally assumed that the negative effects of inbreeding are exacerbated in stressful environments. This G × E interaction has been explored in many taxa under different environmental conditions. These studies usually manipulate environmental conditions either in adulthood or throughout an individual’s entire life. Far fewer studies have tested how stressful environments only experienced during development subsequently influence the effects of inbreeding on adult traits. RESULTS: We experimentally manipulated the diet (control versus low food) of inbred and outbred juvenile Eastern mosquitofish (Gambusia holbrooki) for three weeks (days 7-28) to test whether experiencing a presumably stressful environment early in life influences their subsequent growth and adult phenotypes. The control diet was a standard laboratory food regime, while fish on the low food diet received less than 25 % of this amount of food. Unexpectedly, despite a large sample size (237 families, 908 offspring) and a quantified 23 % reduction in genome-wide heterozygosity in inbred offspring from matings between full-siblings (f = 0.25), neither inbreeding nor its interaction with early diet affected growth trajectories, juvenile survival or adult size. Individuals did not mitigate a poor start in life by showing ‘compensatory growth’ (i.e. faster growth once the low food treatment ended), but they showed ‘catch-up growth’ by delaying maturation. There was, however, no effect of inbreeding on the extent of catch-up growth. CONCLUSIONS: There were no detectable effects of inbreeding on growth or adult size, even on a low food diet that should elevate inbreeding depression. Thus, the long-term costs of inbreeding due to lower male reproductive success we have shown in another study appear to be unrelated to inbreeding depression for adult male size or the growth rates that are r

It is often assumed that mating with close relatives reduces offspring fitness. In such cases, reduced offspring fitness may arise from inbreeding depression (i.e., genetic effects of elevated homozygosity) or from post-mating maternal investment. This can be due to a reduction in female investment after mating with genetically incompatible males ("differential allocation") or compensation for incompatibility ("reproductive compensation"). Here, we looked at the effects of mating with relatives on offspring fitness in mosquitofish, Gambusia holbrooki. In this species, females are assumed to be nonplacental and to allocate resources to eggs before fertilization, limiting differential allocation. We looked at the effects of mating with a brother or with an unrelated male on brood size, offspring size, gestation period, and early offspring growth. Mating with a relative reduced the number of offspring at birth, but there was no difference in the likelihood of breeding, gestation time, nor in the size or growth of these offspring. We suggest that due to limited potential for maternal effects to influence these traits that any reduction in offspring fitness, or lack thereof, can be explained by inbreeding depression rather than by maternal effects. We highlight the importance of considering the potential role of maternal effects when studying inbreeding depression and encourage further studies in other Poeciliid species with different degrees of placentation to test whether maternal effects mask or amplify any genetic effects of mating with relatives.