Selection for small body size favours contrasting sex-specific life histories, boldness and feeding in medaka, Oryzias latipes.
ABSTRACT: BACKGROUND:Studying variation in life-history traits and correlated behaviours, such as boldness and foraging (i.e., pace-of-life syndrome), allows us to better understand how these traits evolve in a changing environment. In fish, it is particularly relevant studying the interplay of resource abundance and size-selection. These are two environmental stressors affecting fish in natural conditions, but also associated with human-induced environmental change. For instance, fishing, one of the most important threats for freshwater and marine populations, results in both higher mortality on large-sized fish and reduced population density. RESULTS:Medaka, Oryzias latipes, from lines selected for large or small size over ten generations, were exposed individually to high or low food availability from birth to adulthood. Maturation schedules, reproductive investment, growth, boldness and feeding were assessed to evaluate the effect of size-selection on the pace of life, and whether it differed between food contexts (high and low). Different food abundance and size-selection resulted in diverse life histories associated with different feeding and boldness behaviour, thus showing different pace-of-life-syndromes. High availability of food favoured faster growth, earlier maturation and increased shyness. Selection for small size led to slower growth in both males and females. But, the life-history trajectory to reach such growth was sex- and food-specific. Under low food conditions, females selected for small size showed earlier maturation, which led to slower adult growth and subsequent low willingness to feed, compared to females selected for large size. No line differences were found in females at high food conditions. In contrast, males exposed to selection for small size grew slower both as juvenile and adult, and were bolder under both feeding regimes. Therefore, the response to size-selection was more sensitive to food availability in females than in males. CONCLUSIONS:We showed that size-selection (over ten generations) and resource abundance (over developmental time) led to changes in life history and behaviour. However, the effect of size-selection was sex- and context-specific, calling for precaution when drawing general conclusions on the population-level effects (or lack of them) of size-selective fishing. Conservation and management plans should consider this sex- and context-specificity.
Project description:Intraspecific trait variation has large effects on the ecosystem and is greatly affected by human activities. To date, most studies focused on single-trait analyses, while considering multiple traits is expected to better predict how an individual interacts with its environment. Here, we used a mesocosm experiment with fish Oryzias latipes to test whether individual growth, boldness and functional traits (feeding rate and stoichiometric traits) formed one functional pace-of-life syndrome (POLS). We then tested the effects of among-individual mean and variance of fish functional POLSs within mesocosms on invertebrate community (e.g. zoobenthos and zooplankton abundances) and ecosystem processes (e.g. ecosystem metabolism, algae stock, nutrient concentrations). Stoichiometric traits correlated with somatic growth and behaviours, forming two independent functional POLS (i.e. two major covariance axes). Mean values of the first syndrome were sex- and environment-dependent and were associated with (i) long-term (10 generations; 4 years) selection for small or large body size resulting in contrasting life histories and (ii) short-term (6 weeks) effects of experimental treatments on resource availability (through manipulation of light intensity and interspecific competition). Specifically, females and individuals from populations selected for a small body size presented fast functional POLS with faster growth rate, higher carbon body content and lower boldness. Individuals exposed to low resources (low light and high competition) displayed a slow functional POLS. Higher mesocosm mean and variance values in the second functional POLS (i.e. high feeding rate, high carbon:nitrogen body ratio, low ammonium excretion rate) were associated to decreased prey abundances, but did not affect any of the ecosystem processes. We highlighted the presence of functional multi-trait covariation in medaka, which were affected by sex, long-term selection history and short-term environmental conditions, that ultimately had cascading ecological consequences. We stressed the need for applying this approach to better predict ecosystem response to anthropogenic global changes.
Project description:Genetic selection for body size during domestication of animal species can inadvertently affect a number of physiological and behavioural traits. The pace-of-life syndrome (POLS) hypothesis predicts that domestication in an artificial environment lacking predators and providing abundant resources prefers proactive individuals with strong feeding motivation, high levels of aggression and risk taking, with low hypothalamus-pituitary-adrenal (HPA) axis responsiveness. In the present experiment we weaned fingerling pike-perch from live feed and habituated them to formulated feed. We recorded the number of weeks needed for the fish to accept pellets, their body length at the age of 100 days, their boldness in a novel object test and their HPI axis responsiveness. Individuals accepting the artificial feed within the first week grew larger than fish habituating later; therefore early weaners would be kept and bred in routine aquaculture procedures. Contrary to predictions of POLS hypothesis, fish weaning earlier and thus growing faster were less bold and had higher HPI axis responsiveness than fish accepting the pellets later or never. As live feed is preferred to artificial pellets, less competitive individuals may switch to pellets earlier. Inadvertent selection for stress sensitive fish may have an effect on production in aquaculture as well as on natural population after intensive restocking.
Project description:The pace-of-life syndrome (POLS) hypothesis predicts variation in behaviour and physiology among individuals to be associated with variation in life history. Thus, individuals on the "fast" end of POLS continuum grow faster, exhibit higher metabolism, are more risk prone, but die earlier than ones on the "slow" end. Empirical support is nevertheless mixed and modelling studies suggested POLS to vary along selection gradients. Therefore, including ecological variation when testing POLS is vastly needed to determine whether POLS is a fixed construct or the result of specific selection processes. Here, we tested POLS predictions between and within two fish populations originating from different ecological conditions. We observed opposing life histories between populations, characterized by differential investments into growth, fecundity, and functional morphology under identical laboratory conditions. A slower life history was, on average, associated with boldness (latency to emergence from a refuge), high activity (short freezing time and long distance travelled), and increased standard metabolism. Correlation structures among POLS traits were not consistent between populations, with the expression of POLS observed in the slow-growing but not in the fast-growing population. Our results suggest that POLS traits can evolve independently from one another and that their coevolution depends upon specific ecological processes.
Project description:In passively operated fishing gear, boldness-related behaviors should fundamentally affect the vulnerability of individual fish and thus be under fisheries selection. To test this hypothesis, we used juvenile common-garden reared carp (Cyprinus carpio) within a narrow size range to investigate the mechanistic basis of behavioral selection caused by angling. We focused on one key personality trait (i.e., boldness), measured in groups within ponds, two morphological traits (body shape and head shape), and one life-history trait (juvenile growth capacity) and studied mean standardized selection gradients caused by angling. Carp behavior was highly repeatable within ponds. In the short term, over seven days of fishing, total length, not boldness, was the main predictor of angling vulnerability. However, after 20 days of fishing, boldness turned out to be the main trait under selection, followed by juvenile growth rate, while morphological traits were only weakly related to angling vulnerability. In addition, we found juvenile growth rate to be moderately correlated with boldness. Hence, direct selection on boldness will also induce indirect selection on juvenile growth and vice versa, but given that the two traits are not perfectly correlated, independent evolution of both traits is also possible. Our study is among the first to mechanistically reveal that energy-acquisition-related behaviors, and not growth rate per se, are key factors determining the probability of capture, and hence, behavioral traits appear to be the prime targets of angling selection. We predict an evolutionary response toward increased shyness in intensively angling-exploited fish stocks, possibly causing the emergence of a timidity syndrome.
Project description:Individuals in a fish population differ in key life-history traits such as growth rate and body size. This raises the question of whether such traits cluster along a fast-slow growth continuum according to a pace-of-life syndrome (POLS). Fish species like salmonids may develop a bimodal size distribution, providing an opportunity to study the relationships between individual growth and behavioural responsiveness. Here we test whether proactive characteristics (bold behaviour coupled with low post-stress cortisol production) are related to fast growth and developmental rate in Atlantic salmon, Salmo salar. Boldness was tested in a highly controlled two-tank hypoxia test were oxygen levels were gradually decreased in one of the tanks. All fish became inactive close to the bottom at 70% oxygen saturation. At 40% oxygen saturation level a fraction of the fish actively sought to avoid hypoxia. A proactive stress coping style was verified by lower cortisol response to a standardized stressor. Two distinct clusters of bimodal growth trajectories were identified, with fast growth and early smoltification in 80% of the total population. There was a higher frequency of proactive than reactive individuals in this fast-developing fraction of fish. The smolts were associated with higher post-stress plasma cortisol than parr, and the proactive smolts leaving hypoxia had significant lower post-stress cortisol than the stayers. The study demonstrated a link between a proactive coping and fast growth and developmental ratio and suggests that selection for domestic production traits promotes this trait cluster.
Project description:Vertebrates exhibit extensive variation in relative brain size. It has long been assumed that this variation is the product of ecologically driven natural selection. Yet, despite more than 100 years of research, the ecological conditions that select for changes in brain size are unclear. Recent laboratory selection experiments showed that selection for larger brains is associated with increased survival in risky environments. Such results lead to the prediction that increased predation should favour increased brain size. Work on natural populations, however, foreshadows the opposite trajectory of evolution; increased predation favours increased boldness, slower learning, and may thereby select for a smaller brain. We tested the influence of predator-induced mortality on brain size evolution by quantifying brain size variation in a Trinidadian killifish, Rivulus hartii, from communities that differ in predation intensity. We observed strong genetic differences in male (but not female) brain size between fish communities; second generation laboratory-reared males from sites with predators exhibited smaller brains than Rivulus from sites in which they are the only fish present. Such trends oppose the results of recent laboratory selection experiments and are not explained by trade-offs with other components of fitness. Our results suggest that increased male brain size is favoured in less risky environments because of the fitness benefits associated with faster rates of learning and problem-solving behaviour.
Project description:This study (1) investigated variation among populations and the effects of sex and body size on boldness, activity and shoal-association tendency among wild zebrafish, and (2) tested for existence of correlations between behaviours, controlling for sex and body size. Individuals across four natural populations were tested for general activity in a novel situation, number of predator inspections undertaken and tendency to associate with a conspecific shoal in the presence of predators. Results showed a significant effect of population on boldness with a population from high-predation habitat being bolder than populations from low-predation habitats. Males showed significantly higher tendencies than females to associate with a conspecific shoal in the presence of predators. Further, a negative relationship was found between activity and boldness only within two low-predation populations. Individual body size had a strong effect on the activity-boldness relationship within the low-predation population from flowing water habitat. Smaller fish were bolder and less active while larger fish were more cautious and active. Overall, the results indicated that while population-level behavioural responses might be shaped by predation pressure, state-dependent factors could determine behavioural correlations among individuals within populations.
Project description:Fish often undergo predation stress and food shortages in nature, and living in groups may provide the ecological benefits of decreased predator risk but the costs of increased food competition. The main aim of the present study was to test whether the behavioral response of qingbo (Spinibarbus sinensis) to predators and/or starvation differed between a singleton and a group. We measured the locomotor activity and distance to a predator and/or food item of prior predator-experienced, starved, double-treated and control qingbo; the qingbo were tested both as singletons and in a group (five individuals). Fish from all groups showed increased activity when tested collectively compared to individually. The predator-experienced fish showed decreased locomotor activity to predators as an antipredator strategy when tested as singletons; however, increased locomotor activity occurred when tested in a group, which might be partially due to the decreased predator risk when living in a group and thus higher levels of boldness. As expected, starvation elicited increased activity indicating increased foraging willingness when tested in a group; however, the difference between starved and normal-fed fish was no longer significant when they were tested as singletons, possibly due to the increased predation risk and decreased food competition when living individually and higher behavioral variation among individual fish than among those in a shoal. Compared with the control fish, the double-treated fish showed no difference in activity when tested both individually and collectively (except a slower speed when tested in a group). The reason for the results from the singletons might be an offset of the effect of predator exposure and starvation. The reason for this difference in the group might be due to the impaired body condition indicated by a slower swimming speed as a consequence of severe stress. The present study demonstrated that behavioral adjustment was closely related to the size of the group, which might be due to differences in the predation risk and food competition.
Project description:Background:Animal growth is often constrained by unfavourable conditions and divergences from optimal body size can be detrimental to an individual's fitness, particularly in species with determinate growth and a narrow time-frame for life-time reproduction. Growth restriction in early juvenile stages can later be compensated by means of plastic developmental responses, such as adaptive catch-up growth (the compensation of growth deficits through delayed development). Although sex differences regarding the mode and degree of growth compensation have been coherently predicted from sex-specific fitness payoffs, inconsistent results imply a need for further research. We used the African Nephila senegalensis, representing an extreme case of female-biased sexual size dimorphism (SSD), to study fitness implications of sex-specific growth compensation. We predicted effective catch-up growth in early food-restricted females to result in full compensation of growth deficits and a life-time fecundity (LTF) equivalent to unrestricted females. Based on a stronger trade-off between size-related benefits and costs of a delayed maturation, we expected less effective catch-up growth in males. Methods:We tracked the development of over one thousand spiders in different feeding treatments, e.g., comprising a fixed period of early low feeding conditions followed by unrestricted feeding conditions, permanent unrestricted feeding conditions, or permanent low feeding conditions as a control. In a second experimental section, we assessed female fitness by measuring LTF in a subset of females. In addition, we tested whether compensatory development affected the reproductive lifespan in both sexes and analysed genotype-by-treatment interactions as a potential cause of variation in life-history traits. Results:Both sexes delayed maturation to counteract early growth restriction, but only females achieved full compensation of adult body size. Female catch-up growth resulted in equivalent LTF compared to unrestricted females. We found significant interactions between experimental treatments and sex as well as between treatments and family lineage, suggesting that family-specific responses contribute to the unusually large variation of life-history traits in Nephila spiders. Our feeding treatments had no effect on the reproductive lifespan in either sex. Discussion:Our findings are in line with predictions of life-history theory and corroborate strong fecundity selection to result in full female growth compensation. Males showed incomplete growth compensation despite a delayed development, indicating relaxed selection on large size and a stronger trade-off between late maturation and size-related benefits. We suggest that moderate catch-up growth in males is still adaptive as a 'bet-hedging' strategy to disperse unavoidable costs between life-history traits affected by early growth restriction (the duration of development and adult size).
Project description:One explanation for animal personality is that different behavioural types derive from different life-history strategies. Highly productive individuals, with high growth rates and high fecundity, are assumed to live life at a fast pace showing high levels of boldness and risk taking, compared with less productive individuals. Here, we investigate among-individual differences in mean boldness (the inverse of the latency to recover from a startling stimulus) and in the consistency of boldness, in male hermit crabs in relation to two aspects of life-history investment. We assessed aerobic scope by measuring the concentration of the respiratory pigment haemocyanin, and we assessed fecundity by measuring spermatophore size. First, we found that individuals investing in large spermatophores also had high concentrations of haemocyanin. Using doubly hierarchical-generalized linear models to analyse longitudinal data on startle responses, we show that hermit crabs vary both in their mean response durations and in the consistency of their behaviour. Individual consistency was unrelated to haemocyanin concentration or spermatophore size, but mean startle response duration increased with spermatophore size. Thus, counter to expectations, it was the most risk-averse individuals, rather than the boldest and most risk prone, that were the most productive. We suggest that similar patterns should be present in other species, if the most productive individuals avoid risky behaviour.