Increased exposure to predators increases both exploration and activity level in Brachyrhaphis episcopi

Two temperament traits, tendency to explore and activity level, were measured in a tropical poeciliid fish, the Panamanian bishop Brachyrhaphis episcopi. Open-field arena tests were used to quantify how predation pressure shapes activity levels and exploratory behaviours. Fish behaviour differed between high and low-predation populations. Fish that experienced higher levels of predation were both more explorative and more active. There were also some individual differences within populations; fish varied in their levels of exploration and activity in a novel open arena, but these differences were not related to sex or size. Together with previous studies on this species, these results indicate that there is a behavioural syndrome associated with predation pressure. Fish from high-predation populations are bolder, more explorative and more active than those from low-predation populations.     

Correlation between boldness and body mass in natural populations of the poeciliid Brachyrhaphis episcopi

The boldness of individual Brachyrhaphis episcopi , collected from regions of high and low predation, was investigated using two independent assays: (1) the time to emerge from cover and (2) the propensity to leave shoal mates and investigate a novel object. A strong correlation between the two assays was revealed such that fish that emerged from shelter sooner were also more likely to approach a novel object. This is indicative of a boldness personality axis acting across both behavioural contexts. Fish from high-predation areas were bolder than those from low-predation areas and males were bolder than females. A significant correlation between body mass, standard length ( L _S) and boldness score was also found. In general, bold fish had a greater body mass at a given L _S than shy fish. These results suggest that personality traits are strongly influenced by population-specific ecological variables and may have fitness consequences in wild populations.     

Rapid evolution of escape ability in Trinidadian guppies (Poecilia reticulata)

Predators are widely assumed to create selection that shapes the evolution of prey escape abilities. However, this assumption is difficult to test directly due to the challenge of recording both predation and its evolutionary consequences in the wild. We examined these events by studying natural and experimental populations of Trinidadian guppies, Poecilia reticulata, which occur in distinct high-predation and low-predation environments within streams. Importantly, in the last two decades several populations of guppies have been experimentally introduced from one type of predatory environment into the other, allowing measurements of the consequences of change. We used this system to test two hypotheses: First, that changes in predatory environments create phenotypic selection favoring changes in escape ability of guppies, and second, that this selection can result in rapid evolution. For the first test we compared escape ability of wild caught guppies from high- versus low-predation environments by measuring survival rates during staged encounters with a major predator, the pike cichlid Crenicichla alta. We used guppies from three streams, comparing two within-stream pairs of natural populations and three within-stream pairs of an introduced population versus its natural source population. In every comparison, guppies from the high-predation population showed higher survival. These multiple, parallel divergences in guppy survival phenotype suggest that predatory environment does create selection of escape ability. We tested our second hypothesis by rearing guppies in common garden conditions in the laboratory, then repeating the earlier experiments using the F2 generation. As before, each comparison resulted in higher survival of guppies descended from the high-predation populations, demonstrating that population differences in escape ability have a genetic basis. These results also show that escape ability can evolve very rapidly in nature, that is, within 26-36 generations in the introduced populations. Interestingly, we found rapid evolutionary loss of escape ability in populations introduced into low-predation environments, suggesting that steep fitness trade-offs may influence the evolution of escape traits.     

Predation risk tradeoffs in prey: effects on energy and behaviour

The complexity of behavioural interactions in predator-prey systems has recently begun to capture trait-effects, or non-lethal effects, of predators on prey via induced behavioural changes. Non-lethal predation effects play crucial roles in shaping population and community dynamics, particularly by inducing changes to foraging, movement and reproductive behaviours of prey. Prey exhibit trade-offs in behaviours while minimizing predation risk. We use a novel evolutionary ecosystem simulation EcoSim to study such behavioural interactions and their effects on prey populations, thereby addressing the need for integrating multiple layers of complexity in behavioural ecology. EcoSim allows complex intra- and inter-specific interactions between behaviourally and genetically unique individuals called predators and prey, as well as complex predator-prey dynamics and coevolution in a tri-trophic and spatially heterogeneous world. We investigated the effects of predation risk on prey energy budgets and fitness. Results revealed that energy budgets, life history traits, allocation of energy to movements and fitness-related actions differed greatly between prey subjected to low-predation risk and high-predation risk. High-predation risk suppressed prey foraging activity, increased total movement and decreased reproduction relative to low-risk. We show that predation risk alone induces behavioural changes in prey which drastically affect population and community dynamics, and when interpreted within the evolutionary context of our simulation indicate that genetic changes accompanying coevolution have long-term effects on prey adaptability to the absence of predators.     

Life-history evolution in guppies. VII. The comparative ecology of high- and low-predation environments

Prior research has demonstrated a strong association between the species of predators that co-occur with guppies and the evolution of guppy life histories. The evolution of these differences in life histories has been attributed to the higher mortality rates experienced by guppies in high-predation environments. Here, we evaluate whether there might be indirect effects of predation on the evolution of life-history patterns and whether there are environmental differences that are correlated with predation. To do so, we quantified features of the physical and chemical environment and the population biology of guppies from seven high- and low-predation localities. We found that high-predation environments tend to be larger streams with higher light levels and higher primary productivity, which should enhance food availability for guppies. We also found that guppy populations from high-predation environments have many more small individuals and fewer large individuals than those from low-predation environments, which is caused by their higher birth rates and death rates. Because of these differences in size distribution, guppies from high-predation environments have only one-fourth of the biomass per unit area, which should also enhance food availability for guppies in these localities. Guppies from high-predation sites allocate more resources to reproduction, grow faster, and attain larger asymptotic sizes, all of which are consistent with higher levels of resource availability. We conclude that guppies from high-predation environments experience higher levels of resource availability in part because of correlated differences in the environment (light levels, primary productivity) and in part as an indirect consequence of predation (death rates and biomass density). These differences in resource availability can, in turn, augment the effect of predator-induced mortality as factors that shape the evolution of guppy life-history patterns. We found no differences in the invertebrate communities from high- and low-predation localities, so we conclude that there do not appear to be multitrophic, indirect effects associated with these differences in predation.     

Comparative studies of senescence in natural populations of guppies

Investigators have rarely sought evidence for senescence in natural populations because it is assumed that relatively few individuals will survive long enough in the wild to exhibit the intrinsic increase in mortality with age expected from senescent individuals. Nevertheless, senescence has been documented in some natural populations, mostly in birds and mammals. Here we report on a comparative study of senescence in two natural populations of guppies (Poecilia reticulata). We document senescence as an age-specific increase in mortality rate, with use of mark-recapture studies and implementation of program MARK for analysis of such observations. Extrinsic mortality was controlled for by choosing populations that experience low rates of predation because they coexist with only a single piscine predator (Rivulus hartii). These populations differ in their evolutionary history because one was native to such a site whereas the other was introduced to a site that previously contained no guppies. The source of the introduced guppies was a high-predation population downstream below a barrier waterfall. Theory predicts that the guppies derived from a high-predation locality should experience senescence at an earlier age than the native low-predation population; however, the historical differences among these populations are also confounded with everything else that differs among the two localities. We found that females from a natural low-predation population have delayed senescence compared with the recently established population and hence that the differences among localities in senescence conform to theoretical predictions. The males from natural low-predation environments also had lower overall mortality rates, but contrary to predictions, the pattern of senescence for males did not differ between populations. The difference between the sexes is potentially attributable to two factors that lower the statistical power for distinguishing differences in the age-specific acceleration of mortality in males. One factor is that males have higher mortality rates, so fewer survive to advanced ages. A second is that we had a greater ability to discriminate among older age classes in females. We also found that the introduced population sustained a higher rate of disease than the native low-predation population. Such disease may represent a confounding factor in our comparison, but it may also reflect one of the trade-offs inherent in the life-history differences of these populations.     

Competition as a selective mechanism for larger offspring size in guppies

Highly competitive environments are predicted to select for larger offspring. Guppies Poecilia reticulata from low-predation populations have evolved to make fewer, larger offspring than their counterparts from high-predation populations. As predation co-varies with the strength of competition in natural guppy populations, here I present two laboratory experiments that evaluate the role of competition in selecting for larger offspring size. In the first experiment, paired groups of large and small newborns from either a high- or a low-predation population were reared in mesocosms under a high- or a low-competition treatment. While large newborns retained their size advantage over small newborns in both treatments, newborn size increased growth only in the high-competition treatment. Moreover, the increase in growth with size was greater in guppies derived from the low-predation population. In the second experiment, pairs of large and small newborns were reared in a highly competitive environment until reproductive maturity. Small size at birth delayed maturation and the effect of birth size on male age of maturity was greater in the low-predation population. These results support the importance of competition as a selective mechanism in offspring size evolution.     

Back to school: can antipredator behaviour in guppies be enhanced through social learning?

The ability to recognize and respond to predators often has a learned component, but few studies have examined the role of social learning in the development of antipredator behaviour. We investigated whether wild-caught juvenile guppies, Poecilia reticulata, from a low-predation river in Trinidad increase their response towards a novel predator through association with conspecifics from a high-predation river. We assigned fish to one of three treatment groups: (1) repeated exposure to a model accompanied by high-predation conspecifics; (2) repeated exposure to a model with low-predation conspecifics; (3) a control group in which focal fish interacted with high-predation fish in the absence of the model. Guppies trained with high-predation, but not low-predation, ‘demonstrators’ significantly improved their antipredator behaviour (spent more time schooling and inspected the model from further away). The guppies assigned to the control group showed no significant improvement in antipredator behaviour after the training period, suggesting that association with experienced conspecifics in the absence of the model is not sufficient to enhance the antipredator behaviour of na?ve fish. We conclude that guppies can improve their antipredator behaviour through association with more experienced conspecifics in the presence of visual cues simulating high predation risk. Copyright 2003 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour.        

Behavioural differences between individuals and two populations of stickleback (Gasterosteus aculeatus)

Behavioural syndromes are correlations between behaviours in different functional contexts. Behavioural syndromes are attracting the attention of evolutionary biologists because they mean that different behaviours might not be free to evolve independently of one another. In a landmark study, Huntingford (1976) showed that individual stickleback which were bold toward predators were also aggressive toward conspecifics and active in an unfamiliar environment. Here, I revisited the activity-aggression-boldness syndrome in stickleback and tested the hypothesis that correlations between behaviours might act as evolutionary constraints. I measured a suite of behaviours on wild-caught individuals and their offspring from two different populations and calculated heritabilities and genetic correlations between the different behaviours. I found that these behaviours were phenotypically and genetically correlated in one population but not another. On average, boldness and aggression were negatively related to each other across the populations. These results suggest that behavioural syndromes don't always act as evolutionary constraints.     

The Relationship between Temperament and Autistic Traits in a Non-Clinical Students Sample

Since temperament affects the development of social behaviours and interpersonal relations, the possible links between autistic traits and temperament are of particular interest. The purpose of the study was to explore the relationships between autistic traits and temperamental characteristics in the framework of the Regulative Temperament Theory by Strelau, and the Emotionality, Activity and Sociability theory by Buss and Plomin, with particular emphasis on gender differences. The Autism Spectrum Quotient (AQ), Formal Characteristics of Behaviour – Temperament Inventory and Temperament Survey for Adults were administered. The participants were 593 university students, including 364 females and 229 males. Results showed positive correlations between autistic traits and Emotional Reactivity, Perseveration, Distress, Fear and Anger, and negative correlations with Activity, Briskness, Endurance and Sociability. The results of multiple regression analyses involving the Autism Spectrum Quotient score as a dependent measure were different for females and males. Results of exploratory PCA analysis showed that AQ score, Sociability and Activity loaded one factor (with AQ loading being opposite to two others). High AQ scorers demonstrated higher Emotional Reactivity, Perseveration, Distress and Anger, and lower Briskness, Endurance, Activity and Sociability as compared to norms for the general population. In this study we showed that temperament measures were able to identify items that correlated in parts with autistic traits, while other items were obverse. The relationships between temperament and autistic traits differ slightly between genders. We assume that with regard to the broader autism phenotype, temperaments might be helpful in characterizing healthy control samples.     

Mate choice, sexual coercion and gene flow in guppy populations

The role of behaviour in gene flow in Trinidadian guppies Poecilia reticulata was assessed using fish from an upstream and downstream pair of populations that differ in predation regime. High-predation (downstream) females preferred males from the corresponding low-predation population, but high-predation males achieved greater reproductive success under competition. This suggests that post-copulatory as well as pre-copulatory events are important in determining rates of gene flow.     

Both Geography and Ecology Contribute to Mating Isolation in Guppies

Local adaptation to different environments can promote mating isolation – either as an incidental by-product of trait divergence, or as a result of selection to avoid maladaptive mating. Numerous recent empirical examples point to the common influence of divergent natural selection on speciation based largely on evidence of strong pre-mating isolation between populations from different habitat types. Accumulating evidence for natural selection''s influence on speciation is therefore no longer a challenge. The difficulty, rather, is in determining the mechanisms involved in the progress of adaptive divergence to speciation once barriers to gene flow are already present. Here, we present results of both laboratory and field experiments with Trinidadian guppies (Poecilia reticulata) from different environments, who do not show complete reproductive isolation despite adaptive divergence. We investigate patterns of mating isolation between populations that do and do not exchange migrants and show evidence for both by-product and reinforcement mechanisms depending on female ecology. Specifically, low-predation females discriminate against all high-predation males thus implying a by-product mechanism, whereas high-predation females only discriminate against low-predation males from further upstream in the same river, implying selection to avoid maladaptive mating. Our study thus confirms that mechanisms of adaptive speciation are not necessarily mutually exclusive and uncovers the complex ecology-geography interactions that underlie the evolution of mating isolation in nature.     

Life-history evolution in guppies viii: the demographics of density regulation in guppies (poecilia reticulata)

In prior research, we found the way guppy life histories evolve in response to living in environments with a high or low risk of predation is consistent with life-history theory that assumes no density dependence. We later found that guppies from high-predation environments experience higher mortality rates than those from low-predation environments, but the increased risk was evenly distributed across all age/size classes. Life-history theory that assumes density-independent population growth predicts that life histories will not evolve under such circumstances, yet we have shown with field introduction experiments that they do evolve. However, theory that incorporates density regulation predicts this pattern of mortality can result in the patterns of life-history evolution we had observed. Here we report on density manipulation experiments performed in populations of guppies from low-predation environments to ask whether natural populations normally experience density regulation and, if so, to characterize the short-term demographic changes that underlie density regulation. Our experiments reveal that these populations are density regulated. Decreased density resulted in higher juvenile growth, decreased juvenile mortality rates, and increased reproductive investment by adult females. Increased density causes reduced offspring size, decreased fat storage by adult females, and increased adult mortality.     

Differential stress responses in fish from areas of high- and low-predation pressure

We subjected fish from regions of high and low levels of predation pressure in four independent streams to a mild stressor and recorded their opercular beat rates. Fish from low-predation areas showed higher maximum, minimum and mean opercular beat frequencies than fish from high-predation regions. The change in opercular beat frequency (scope) was also significantly greater in fish from low- than in fish from high-predation regions. Under normal activity levels, however, low predation fish showed a reduced opercular beat frequency, which may be indicative of reduced activity levels or metabolic rate. Opercular beat frequency was negatively correlated with standard length as one would expect based on higher metabolic rates in smaller fish. We suggest that these contrasting stress responses are most likely the result of differential exposure to predators in fish from high- and low-predation areas. We argue that reduced stress responses in high-predation areas evolved to prevent excessive energy expenditure by modulating the fright response.     

Embryonic exposure to predator odour modulates visual lateralization in cuttlefish

Predation pressure acts on the behaviour and morphology of prey species. In fish, the degree of lateralization varies between high- and low-predation populations. While lateralization appears to be widespread in invertebrates, we do not know whether heredity and early experience interact during development as in vertebrates. Here we show, for the first time, that an exposure to predator odour prior to hatching modulates visual lateralization in newly hatched cuttlefish. Only cuttlefish that have been exposed to predator odour display a left-turning bias when tested with blank seawater in a T-shaped apparatus. Exposure to predator odour all the incubation long could appear as an acute predictor of a high-predation surrounding environment. In addition, cuttlefish of all groups display a left-turning preference when tested with predator odour in the apparatus. This suggests the ability of cuttlefish to innately recognize predator odour. To our knowledge, this is the first clear demonstration that lateralization is vulnerable to ecological challenges encountered during embryonic life, and that environmental stimulation of the embryo through the olfactory system could influence the development of subsequent visual lateralization.     

Evolution of juvenile growth rates in female guppies (Poecilia reticulata): predator regime or resource level?

Recent theoretical and empirical work argues that growth rate can evolve and be optimized, rather than always being maximized. Chronically low resource availability is predicted to favour the evolution of slow growth, whereas attaining a size-refuge from mortality risk is predicted to favour the evolution of rapid growth. Guppies (Poecilia reticulata) evolve differences in behaviour, morphology and life-history traits in response to predation, thus demonstrating that predators are potent agents of selection. Predators in low-predation environments prey preferentially on small guppies, but those in high-predation environments appear to be non-selective. Because guppies can outgrow their main predator in low- but not high-predation localities, we predict that predation will select for higher growth rates in the low-predation environments.However, low-predation localities also tend to have lower productivity than high-predation localities, yield-ing the prediction that guppies from these sites should have slower growth rates. Here we compare the growth rates of the second laboratory-born generation of guppies from paired high- and low-predation localities from four different drainages. In two out of four comparisons, guppies from high-predation sites grew significantly faster than their low-predation counterparts. We also compare laboratory born descendants from a field introduction experiment and show that guppies introduced to a low-predation environment evolved slower growth rates after 13 years, although this was evident only at the high food level. The weight of the evidence suggests that resource availability plays a more important role than predation in shaping the evolution of growth rates.     

The role of predation in variation in body shape in guppies Poecilia reticulata: a comparison of field and common garden phenotypes

The body shapes of both wild-caught and laboratory-reared male and female Trinidadian guppies Poecilia reticulata from two low-predation and two high-predation populations were studied, but predation regime did not seem to be the most important factor affecting body shape. Instead, complicated patterns of plasticity in body shape among populations and the sexes were found. In particular, populations differed in the depth of the caudal peduncle, which is the muscular region just anterior to the tail fin rays and from which most swimming power is generated. Strikingly, the direction of population differences in caudal peduncle depth observed in wild-caught individuals was reversed when P. reticulata were raised in a common laboratory environment.     

Effects of predation pressure on the cognitive ability of the poeciliid Brachyraphis episcopi

Variable levels of predation pressure are known to have significantimpacts on the evolutionary ecology of different populationsand can affect life-history traits, behavior, and morphology.To date, no studies have directly investigated the impact ofpredation pressure on cognitive ability. Here we use a systemof replicate rivers, each with sites of high- and low-predationpressure, to investigate how this ecological variable affectslearning ability in a tropical poeciliid, Brachyraphis episcopi.We used a spatial task to assess the cognitive ability of eightpopulations from four independent streams (four high- and fourlow-predation populations). The fish were required to locatea foraging patch in one of four compartments by utilizing spatialcues. Fish from areas of low-predation pressure had shorterforaging latencies, entered fewer compartments before discoveringthe reward patch and navigated more actively within the maze,than fish from high-predation sites. The difference in performanceis discussed with reference to forage patch predictability,inter- and intraspecific foraging competition, geographic variationin predation pressure, boldness–shyness traits, and brainlateralization.     

Are host-parasite interactions influenced by adaptation to predators? A test with guppies and Gyrodactylus in experimental stream channels

Natural populations often face multiple mortality sources. Adaptive responses to one mortality source might also be beneficial with respect to other sources of mortality, resulting in "reinforcing adaptations"; or they might be detrimental with respect to other sources of mortality, resulting in "conflicting adaptations". We explored these possibilities by testing experimentally if the responses of guppies (Poecilia reticulata) to the monogenean ectoparasitic worm Gyrodactylus differed between populations adapted to different predation regimes. In experimental stream channels designed to replicate the natural environment, we exposed eight guppy populations (high-predation and low-predation populations from each of four separate rivers) either to their local Gyrodactylus parasites (infection treatment) or to the absence of those parasites (control). We found that infection dynamics varied dramatically among populations in a repeatable fashion, but that this variation was not related to the predation regime of origin. Consistent with previous work, high-predation guppy females gained more mass, had lower reproductive investment, and had more but smaller embryos than did low-predation females. Relative to control (no parasite) channels, guppies from treatment (infected) channels gained less mass but produced similar numbers and sizes of embryos-and thus had a higher reproductive effort. However, no interaction was evident between infection treatment and predation regime. We conclude that parasitism by Gyrodactylus and predation are both likely selective forces for guppies, but that adaptation to predation does not have an obvious deterministic effect on host-parasite dynamics or on life-history traits of female guppies.     

Trade-off between steady and unsteady swimming underlies predator-driven divergence in Gambusia affinis

Differences in predation intensity experienced by organisms can lead to divergent natural selection, driving evolutionary change. Western mosquitofish (Gambusia affinis) exhibit larger caudal regions and higher burst-swimming capabilities when coexisting with higher densities of predatory fish. It is hypothesized that a trade-off between steady (constant-speed cruising; important for acquiring resources) and unsteady (rapid bursts and turns; important for escaping predators) locomotion, combined with divergent selection on locomotor performance (favouring steady swimming in high-competition scenarios of low-predation environments, but unsteady swimming in high-predation localities) has caused such phenotypic divergence. Here, I found that morphological differences had a strong genetic basis, and low-predation fish required less hydromechanical power during steady swimming, leading to increased endurance. I further found individual-level support for cause-and-effect relationships between morphology, swimming kinematics and endurance. Results indicate that mosquitofish populations inhabiting low-predation environments have evolved increased steady-swimming abilities via stiffer bodies, larger anterior body/head regions, smaller caudal regions and greater three-dimensional streamlining.