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 effect of brain size evolution on feeding propensity,digestive efficiency,and juvenile growth

One key hypothesis in the study of brain size evolution is the expensive tissue hypothesis; the idea that increased investment into the brain should be compensated by decreased investment into other costly organs, for instance the gut. Although the hypothesis is supported by both comparative and experimental evidence, little is known about the potential changes in energetic requirements or digestive traits following such evolutionary shifts in brain and gut size. Organisms may meet the greater metabolic requirements of larger brains despite smaller guts via increased food intake or better digestion. But increased investment in the brain may also hamper somatic growth. To test these hypotheses we here used guppy (Poecilia reticulata) brain size selection lines with a pronounced negative association between brain and gut size and investigated feeding propensity, digestive efficiency (DE), and juvenile growth rate. We did not find any difference in feeding propensity or DE between large‐ and small‐brained individuals. Instead, we found that large‐brained females had slower growth during the first 10 weeks after birth. Our study provides experimental support that investment into larger brains at the expense of gut tissue carries costs that are not necessarily compensated by a more efficient digestive system.     

A further cost for the sicker sex? Evidence for male‐biased parasite‐induced vulnerability to predation

Males are typically the sicker sex. Data from multiple taxa indicate that they are more likely to be infected with parasites, and are less “tolerant,” or less able to mitigate the fitness costs of a given infection, than females. One cost of infection for many animals is an increased probability of being captured by a predator. A clear, hitherto untested, prediction is therefore that this parasite‐induced vulnerability to predation is more pronounced among males than females. We tested this prediction in the sexually size dimorphic guppy, Poecilia reticulata, in which females are typically larger than males. We either sham or experimentally infected guppies with Gyrodactylus turnbulli, elicited their escape response using an established protocol and measured the distance they covered during 60 ms. To discriminate between the effects of body size and those of other inherent sex differences, we size‐matched fish across treatment groups. Infection with G. turnbulli reduced the distance covered during the escape response of small adults by 20.1%, whereas that of large fish was unaffected. This result implies that parasite‐induced vulnerability to predation is male‐biased in the wild: although there was no difference in escape response between our experimentally size‐matched groups of males and females, males are significantly smaller across natural guppy populations. These results are consistent with Bateman's principle for immunity: Natural selection for larger body sizes and longevity in females seems to have resulted in the evolution of increased infection tolerance. We discuss the potential implications of sex‐ and size‐biased parasite‐induced vulnerability to predation for the evolutionary ecology of this host–parasite interaction in natural communities.     

Positive genetic correlation between brain size and sexual traits in male guppies artificially selected for brain size

Brain size is an energetically costly trait to develop and maintain. Investments into other costly aspects of an organism's biology may therefore place important constraints on brain size evolution. Sexual traits are often costly and could therefore be traded off against neural investment. However, brain size may itself be under sexual selection through mate choice on cognitive ability. Here, we use guppy (Poecilia reticulata) lines selected for large and small brain size relative to body size to investigate the relationship between brain size, a large suite of male primary and secondary sexual traits, and body condition index. We found no evidence for trade‐offs between brain size and sexual traits. Instead, larger‐brained males had higher expression of several primary and precopulatory sexual traits – they had longer genitalia, were more colourful and developed longer tails than smaller‐brained males. Larger‐brained males were also in better body condition when housed in single‐sex groups. There was no difference in post‐copulatory sexual traits between males from the large‐ and small‐brained lines. Our data do not support the hypothesis that investment into sexual traits is an important limiting factor to brain size evolution, but instead suggest that brain size and several sexual traits are positively genetically correlated.     

No gains for bigger brains: Functional and neuroanatomical consequences of relative brain size in a parasitic wasp

Heritable genetic variation in relative brain size can underlie the relationship between brain performance and the relative size of the brain. We used bidirectional artificial selection to study the consequences of genetic variation in relative brain size on brain morphology, cognition and longevity in Nasonia vitripennis parasitoid wasps. Our results show a robust change in relative brain size after 26 generations of selection and six generations of relaxation. Total average neuropil volume of the brain was 16% larger in wasps selected for relatively large brains than in wasps selected for relatively small brains, whereas the body length of the large‐brained wasps was smaller. Furthermore, the relative volume of the antennal lobes was larger in wasps with relatively large brains. Relative brain size did not influence olfactory memory retention, whereas wasps that were selected for larger relative brain size had a shorter longevity, which was even further reduced after a learning experience. These effects of genetic variation on neuropil composition and memory retention are different from previously described effects of phenotypic plasticity in absolute brain size. In conclusion, having relatively large brains may be costly for N. vitripennis, whereas no cognitive benefits were recorded.     

Size selection by a gape‐limited predator of a marine snail: Insights into magic traits for speciation

The intertidal snail Littorina saxatilis has repeatedly evolved two parallel ecotypes assumed to be wave adapted and predatory shore crab adapted, but the magnitude and targets of predator‐driven selection are unknown. In Spain, a small, wave ecotype with a large aperture from the lower shore and a large, thick‐shelled crab ecotype from the upper shore meet in the mid‐shore and show partial size‐assortative mating. We performed complementary field tethering and laboratory predation experiments; the first set compared the survival of two different size‐classes of the crab ecotype while the second compared the same size‐class of the two ecotypes. In the first set, the large size‐class of the crab ecotype survived significantly better than the small size‐class both on the upper shore and in the laboratory. In the second set, the small size‐class of the crab ecotype survived substantially better than that of the wave ecotype both on the upper shore and in the laboratory. Shell‐breaking predation on tethered snails was almost absent within the lower shore. In the laboratory shore crabs (Pachygrapsus marmoratus) with larger claw heights selected most strongly against the small size‐class of the crab ecotype, whereas those with medium claw heights selected most strongly against the thin‐shelled wave ecotype. Sexual maturity occurred at a much larger size in the crab ecotype than in the wave ecotype. Our results showed that selection on the upper shore for rapid attainment of a size refuge from this gape‐limited predator favors large size, thick shells, and late maturity. Model parameterization showed that size‐selective predation restricted to the upper shore resulted in the evolution of the crab ecotype despite gene flow from the wave ecotype snails living on the lower shore. These results on gape‐limited predation and previous ones showing size‐assortative mating between ecotypes suggest that size may represent a magic trait for the thick‐shelled ecotype.     

ARTIFICIAL SELECTION ON RELATIVE BRAIN SIZE REVEALS A POSITIVE GENETIC CORRELATION BETWEEN BRAIN SIZE AND PROACTIVE PERSONALITY IN THE GUPPY

Animal personalities range from individuals that are shy, cautious, and easily stressed (a “reactive” personality type) to individuals that are bold, innovative, and quick to learn novel tasks, but also prone to routine formation (a “proactive” personality type). Although personality differences should have important consequences for fitness, their underlying mechanisms remain poorly understood. Here, we investigated how genetic variation in brain size affects personality. We put selection lines of large‐ and small‐brained guppies (Poecilia reticulata), with known differences in cognitive ability, through three standard personality assays. First, we found that large‐brained animals were faster to habituate to, and more exploratory in, open field tests. Large‐brained females were also bolder. Second, large‐brained animals excreted less cortisol in a stressful situation (confinement). Third, large‐brained animals were slower to feed from a novel food source, which we interpret as being caused by reduced behavioral flexibility rather than lack of innovation in the large‐brained lines. Overall, the results point toward a more proactive personality type in large‐brained animals. Thus, this study provides the first experimental evidence linking brain size and personality, an interaction that may affect important fitness‐related aspects of ecology such as dispersal and niche exploration.     

Predicting Predatory Outcomes in the Context of Carryover Effects: Interactions between Juvenile Frogs and Spider Predators

As representatives of organisms with complex life histories, frogs provide an ideal system to study predator‐induced carryover effects: how the risk of predation in one life stage can impact predator–prey interactions in a later stage. Invertebrate predation on frogs has been widely reported, although studies of the behavioral mechanisms underlying their interactions in the terrestrial stage have been lacking. We made detailed observations of interactions between a wolf spider (Tigrosa helluo) and Blanchard's cricket frog (Acris blanchardi) to determine factors that predict capture success and to evaluate potential carryover effects from aquatic predation risk. Juvenile frogs, reared with or without dragonfly predator cues, were placed in an arena with or without spider cues and allowed to interact with a spider. Spiders captured frogs, and an interaction between frog size and activity predicted frog survival. We found no evidence that either aquatic or terrestrial cues altered frog behavior or survival. By preying upon a demographically important life stage, spiders may contribute to population dynamics in frogs.     

Artificial selection on brain size leads to matching changes in overall number of neurons

Neurons are the basic computational units of the brain, but brain size is the predominant surrogate measure of brain functional capacity in comparative and cognitive neuroscience. This approach is based on the assumption that larger brains harbor higher numbers of neurons and their connections, and therefore have a higher information‐processing capacity. However, recent studies have shown that brain mass may be less strongly correlated with neuron counts than previously thought. Till now, no experimental test has been conducted to examine the relationship between evolutionary changes in brain size and the number of brain neurons. Here, we provide such a test by comparing neuron number in artificial selection lines of female guppies (Poecilia reticulata) with >15% difference in relative brain mass and numerous previously demonstrated cognitive differences. Using the isotropic fractionator, we demonstrate that large‐brained females have a higher overall number of neurons than small‐brained females, but similar neuronal densities. Importantly, this difference holds also for the telencephalon, a key region for cognition. Our study provides the first direct experimental evidence that selection for brain mass leads to matching changes in number of neurons and shows that brain size evolution is intimately linked to the evolution of neuron number and cognition.     

Large‐brained birds suffer less oxidative damage

Large brains (relative to body size) might confer fitness benefits to animals. Although the putative costs of well‐developed brains can constrain the majority of species to modest brain sizes, these costs are still poorly understood. Given that the neural tissue is energetically expensive and demands antioxidants, one potential cost of developing and maintaining large brains is increased oxidative stress (‘oxidation exposure’ hypothesis). Alternatively, because large‐brained species exhibit slow‐paced life histories, they are expected to invest more into self‐maintenance such as an efficacious antioxidative defence machinery (‘oxidation avoidance’ hypothesis). We predict decreased antioxidant levels and/or increased oxidative damage in large‐brained species in case of oxidation exposure, and the contrary in case of oxidation avoidance. We address these contrasting hypotheses for the first time by means of a phylogenetic comparative approach based on an unprecedented data set of four redox state markers from 85 European bird species. Large‐brained birds suffered less oxidative damage to lipids (measured as malondialdehyde levels) and exhibited higher total nonenzymatic antioxidant capacity than small‐brained birds, whereas uric acid and glutathione levels were independent of brain size. These results were not altered by potentially confounding variables and did not depend on how relative brain size was quantified. Our findings partially support the ‘oxidation avoidance’ hypothesis and provide a physiological explanation for the linkage of large brains with slow‐paced life histories: reduced oxidative stress of large‐brained birds can secure brain functionality and healthy life span, which are integral to their lifetime fitness and slow‐paced life history.     

Predators can influence the host‐parasite dynamics of their prey via nonconsumptive effects

Ecological communities are partly structured by indirect interactions, where one species can indirectly affect another by altering its interactions with a third species. In the absence of direct predation, nonconsumptive effects of predators on prey have important implications for subsequent community interactions. To better understand these interactions, we used a Daphnia‐parasite‐predator cue system to evaluate if predation risk affects Daphnia responses to a parasite. We investigated the effects of predator cues on two aspects of host–parasite interactions (susceptibility to infection and infection intensity), and whether or not these effects differed between sexes. Our results show that changes in response to predator cues caused an increase in the prevalence and intensity of parasite infections in female predator‐exposed Daphnia. Importantly, the magnitude of infection risk depended on how long Daphnia were exposed to the cues. Additionally, heavily infected Daphnia that were constantly exposed to cues produced relatively more offspring. While males were ~5× less likely to become infected compared to females, we were unable to detect effects of predator cues on male Daphnia–parasite interactions. In sum, predators, prey, and their parasites can form complex subnetworks in food webs, necessitating a nuanced understanding of how nonconsumptive effects may mediate these interactions.     

Population genomics of natural and experimental populations of guppies (Poecilia reticulata)

Convergent evolution represents one of the best lines of evidence for adaptation, but few cases of phenotypic convergence are understood at the genetic level. Guppies inhabiting the Northern Mountain Range of Trinidad provide a classic example of phenotypic convergent evolution, where adaptation to low or high predation environments has been found for a variety of traits. A major advantage of this system is the possibility of long‐term experimental studies in nature, including transplantation from high to low predation sites. We used genome scans of guppies from three natural high and low predation populations and from two experimentally established populations and their sources to examine whether phenotypic convergent evolution leaves footprints at the genome level. We used population‐genetic modelling approaches to reconstruct the demographic history and migration among sampled populations. Naturally colonized low predation populations had signatures of increased effective population size since colonization, while introduction populations had signatures of decreased effective population size. Only a small number of regions across the genome had signatures of selection in all natural populations. However, the two experimental populations shared many genomic regions under apparent selection, more than expected by chance. This overlap coupled with a population decrease since introduction provides evidence for convergent selection occurring in the two introduced populations. The lack of genetic convergence in the natural populations suggests that convergent evolution is lacking in these populations or that the effects of selection become difficult to detect after a long‐time period.     

Strategies of zooplanktivory shape the dynamics and diversity of littoral plankton communities: a mesocosm approach

Planktivorous fish can exert strong top‐down control on zooplankton communities. By incorporating different feeding strategies, from selective particulate feeding to cruising filter feeding, fish species target distinct prey. In this study, we investigated the effects of two species with different feeding strategies, the three‐spined stickleback (Gasterosteus aculeatus (L.)) and roach (Rutilus rutilus (L.)), on a low‐diversity brackish water zooplankton community using a 16‐day mesocosm experiment. The experiment was conducted on a small‐bodied spring zooplankton community in high‐nutrient conditions, as well as a large‐bodied summer community in low‐nutrient conditions. Effects were highly dependent on the initial zooplankton community structure and hence seasonal variation. In a small‐bodied community with high predation pressure and no dispersal or migration, the selective particulate‐feeding stickleback depleted the zooplankton community and decreased its diversity more radically than the cruising filter‐feeding roach. Cladocerans rather than copepods were efficiently removed by predation, and their removal caused altered patterns in rotifer abundance. In a large‐bodied summer community with initial high taxonomic and functional diversity, predation pressure was lower and resource availability was high for omnivorous crustaceans preying on other zooplankton. In this community, predation maintained diversity, regardless of predator species. During both experimental periods, predation influenced the competitive relationship between the dominant calanoid copepods, and altered species composition and size structure of the zooplankton community. Changes also occurred to an extent at the level of nontarget prey, such as microzooplankton and rotifers, emphasizing the importance of subtle predation effects. We discuss our results in the context of the adaptive foraging mechanism and relate them to the natural littoral community.     

Yes,correct context is indeed the key: An answer to Haave‐Audet et al. 2019

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

Selection on fruit traits is mediated by the interplay between frugivorous birds,fruit flies,parasitoid wasps and seed‐dispersing ants

Every organism on Earth must cope with a multitude of species interactions both directly and indirectly throughout its life cycle. However, how selection from multiple species occupying different trophic levels affects diffuse mutualisms has received little attention. As a result, how a given species amalgamates the combined effects of selection from multiple mutualists and antagonists to enhance its own fitness remains little understood. We investigated how multispecies interactions (frugivorous birds, ants, fruit flies and parasitoid wasps) generate selection on fruit traits in a seed dispersal mutualism. We used structural equation models to assess whether seed dispersers (frugivorous birds and ants) exerted phenotypic selection on fruit and seed traits in the spiny hackberry (Celtis ehrenbergiana), a fleshy‐fruited tree, and how these selection regimes were influenced by fruit fly infestation and wasp parasitoidism levels. Birds exerted negative correlational selection on the combination of fruit crop size and mean seed weight, favouring either large crops with small seeds or small crops with large seeds. Parasitoids selected plants with higher fruit fly infestation levels, and fruit flies exerted positive directional selection on fruit size, which was positively correlated with seed weight. Therefore, higher parasitoidism indirectly correlated with higher plant fitness through increased bird fruit removal. In addition, ants exerted negative directional selection on mean seed weight. Our results show that strong selection on phenotypic traits may still arise in perceived diffuse species interactions. Overall, we emphasize the need to consider diverse direct and indirect partners to achieve a better understanding of the mechanisms driving phenotypic trait evolution in multispecies interactions.     

Parting ways: parasite release in nature leads to sex‐specific evolution of defence

We evaluated the extent to which males and females evolve along similar or different trajectories in response to the same environmental shift. Specifically, we used replicate experimental introductions in nature to consider how release from a key parasite (Gyrodactylus) generates similar or different defence evolution in male vs. female guppies (Poecilia reticulata). After 4–8 generations of evolution, guppies were collected from the ancestral (parasite still present) and derived (parasite now absent) populations and bred for two generations in the laboratory to control for nongenetic effects. These F2 guppies were then individually infected with Gyrodactylus, and infection dynamics were monitored on each fish. We found that parasite release in nature led to sex‐specific evolutionary responses: males did not show much evolution of resistance, whereas females showed the evolution of increased resistance. Given that male guppies in the ancestral population had greater resistance to Gyrodactylus than did females, evolution in the derived populations led to reduction of sexual dimorphism in resistance. We argue that previous selection for high resistance in males constrained (relative to females) further evolution of the trait. We advocate more experiments considering sex‐specific evolutionary responses to environmental change.     

Reproductive trade‐offs in a long‐lived bird species: condition‐dependent reproductive allocation maintains female survival and offspring quality

Life history theory is an essential framework to understand the evolution of reproductive allocation. It predicts that individuals of long‐lived species favour their own survival over current reproduction, leading individuals to refrain from reproducing under harsh conditions. Here we test this prediction in a long‐lived bird species, the Siberian jay Perisoreus infaustus. Long‐term data revealed that females rarely refrain from breeding, but lay smaller clutches in unfavourable years. Neither offspring body size, female survival nor offspring survival until the next year was influenced by annual condition, habitat quality, clutch size, female age or female phenotype. Given that many nests failed due to nest predation, the variance in the number of fledglings was higher than the variance in the number of eggs and female survival. An experimental challenge with a novel pathogen before egg laying largely replicated these patterns in two consecutive years with contrasting conditions. Challenged females refrained from breeding only in the unfavourable year, but no downstream effects were found in either year. Taken together, these findings demonstrate that condition‐dependent reproductive allocation may serve to maintain female survival and offspring quality, supporting patterns found in long‐lived mammals. We discuss avenues to develop life history theory concerning strategies to offset reproductive costs.     

Do trade‐offs between predation pressures on females versus nests drive nest‐site choice in painted turtles?

Predation strongly influences reproductive behaviours because reproducing individuals must balance mortality risks to themselves and to their offspring. In many freshwater turtles, the nest predation risk decreases with nest distance from water, whereas the predation risk to females increases farther from water. To determine whether predation pressure influences the distance from water at which female turtles nest, we measured predation pressure on nesting females and on nests, as well as the distances of nests to water, in two populations of painted turtles. Using models, we found that female survival in both populations was high and did not vary with distance from water. Nest survival was also uncorrelated with nest distance to water, although it was significantly lower than adult survival in both populations and was only 1.2% in one population. Our results suggest that nest sites are not predictably safe from predators. Instead, turtles may hedge their bets by nesting over a wide range of distances from water because any distance is risky for nests and no distance is particularly risky for the nesting female. We suggest that other factors, such as suitable incubation conditions and/or post‐emergence hatchling survival, probably play a larger role than predation in driving nest‐site choice in painted turtles.     

Material affects attack rates on dummy caterpillars in tropical forest where arthropod predators dominate: an experiment using clay and dough dummies with green colourants on various plant species

Predation can be one of the key factors that determine abundance in insect herbivore communities, and drive evolution of body size, and anti‐predator traits, including crypsis. Population dynamics and selection pressures will depend on the identity of dominant predators in the system, and these may vary substantially among habitats. Arthropods emerge as chief predators on caterpillars in the understorey of non‐montane tropical forest, whereas birds dominate elsewhere. In a tropical forest in Uganda, Africa, we evaluated marks on dummy caterpillars that differed in size, material (clay vs. dough), colourant, and plant species on which dummy caterpillars were exposed. We included live caterpillars to estimate the extent to which studies using artificial caterpillars reflect actual levels of predation. Ants and wasps were the most important damagers of dummy caterpillars, whereas bug and beetle damage was very rare, and no bird or small mammal damage was observed. Daily attack rates did not differ significantly from apparent mortality of live caterpillars (daily mortality = 12.1%), but dummy caterpillars made from dough were attacked more frequently (daily attack rate = 18.4%) than those from clay (daily attack rate = 6.9%). Caterpillars of different colour and size, and caterpillars exposed on different plant species had the same chances to be predated. This is in contrast to results from temperate area studies where birds dominate and are not affected by dummy caterpillar material, but prefer larger caterpillars. Our results are consistent with dominant predators on tropical forest caterpillars being invertebrates that are more chemically than visually oriented, so that: (1) material used for dummy caterpillars is important, (2) background matching is relatively unimportant, and (3) being large may have less of a cost. These patterns in predation might facilitate polyphagy and evolution of large body size in tropical Lepidoptera.     

Body size evolution of a shell‐brooding cichlid fish from Lake Tanganyika

The substrate‐brooding cichlid fish Telmatochromis temporalis in Lake Tanganyika demonstrates a simple example of ecological speciation between normal and dwarf morphs through divergent natural selection on body size. The dwarf morph most likely evolved from the ancestral normal morph; therefore, elucidating the evolution of its small body size is a key to understanding this ecological speciation event. Previous studies suggest that the small body size of the dwarf morph is an adaptation to the use of empty snail shells as shelters (males) and spawning sites (females), but this idea has not been fully evaluated. Combining original and previously published information, this study compared likelihood values to determine the primary factor that would be responsible for regulating the body size of the dwarf morph. Male body size is most likely regulated by the ability to turn within shells, which may influence the predation avoidance of adult fish. Females are smaller than males, and their body size is most likely regulated by the ability to lay eggs in the small spaces within shells close to the shell apices where predation risk on eggs is lower. This study provides new evidence supporting the hypothesis that different natural selection factors affected body size of the different sexes of the dwarf morph, which has not been reported in other animal species.