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.     

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.     

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.     

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.     

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.     

Predator exposure alters stress physiology in guppies across timescales

In vertebrates, glucocorticoids mediate a wide-range of responses to stressors. For this reason, they are implicated in adaptation to changes in predation pressure. Trinidadian guppies (Poecilia reticulata) from high-predation environments have repeatedly and independently colonized and adapted to low-predation environments, resulting in parallel changes in life history, morphology, and behavior. We validated methods for non-invasive waterborne hormone sample collection in this species, and used this technique to examine genetic and environmental effects of predation on basal glucocorticoid (cortisol) levels. To examine genetic differences, we compared waterborne cortisol levels in high- and low-predation fish from two distinct population pairs. We found that fish from high-predation localities had lower cortisol levels than their low-predation counterparts. To isolate environmental influences, we compared waterborne cortisol levels in genetically similar fish reared with and without exposure to predator chemical cues. We found that fish reared with predator chemical cues had lower waterborne cortisol levels than those reared without. Comparisons of waterborne and whole-body cortisol levels demonstrated that populations differed in overall cortisol levels in the body, whereas rearing conditions altered the release of cortisol from the body into the water. Thus, evolutionary history with predators and lifetime exposure to predator cues were both associated with lower cortisol release, but depended on distinct physiological mechanisms.     

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.     

LIFE-HISTORY EVOLUTION IN GUPPIES (POECILIA RETICULATA) 6. DIFFERENTIAL MORTALITY AS A MECHANISM FOR NATURAL SELECTION

We have previously reported a correlation between the life-history patterns of guppies and the types of predators with which they coexist. Guppies from localities with an abundance of large predators (high predation localities) mature at an earlier age and devote more resources to reproduction than those found in localities with only a single, small species of predator (low predation localities). We also found that when guppies were introduced from a high to low predation locality, the guppy life history evolved to resemble what was normally found in this low predation locality. The presumed mechanism of natural selection is differences among localities in age/size-specific mortality (the age/size-specific mortality hypothesis); in high predation localities we assumed that guppies experienced high adult mortality rates while in the low predation localities we assumed that guppies experienced high juvenile mortality rates. These assumptions were based on stomach content analyses of wild-caught predators and on laboratory experiments. Here, we evaluate these assumptions by directly estimating the mortality rates of guppies in natural populations. We found that guppies from high predation localities experience significantly higher mortality rates than their counterparts from low predation localities, but that these higher mortality rates are uniformly distributed across all size classes, rather than being concentrated in the larger size classes. This result appears to contradict the predictions of the age/size-specific predation hypothesis. However, we argue, using additional data on growth rates and the probabilities of survival to maturity in each type of locality, that the age-specific mortality hypothesis remains plausible. This is because the probability of survival to first reproduction is very similar in each type of locality, but the guppies from high predation localities have a much lower probability of survival per unit time after maturity. We also argue for the plausibility of two other mechanisms of natural selection. These results thus reveal mortality patterns that provide a potential cause of natural selection, but expand, rather than narrow, the number of possible mechanisms responsible for life-history evolution in guppies.     

Predation intensity does not cause microevolutionary change in maximum speed or aerobic capacity in trinidadian guppies (Poecilia reticulata Peters)

We measured maximal oxygen consumption (VO(2max)) and burst speed in populations of Trinidadian guppies (Poecilia reticulata) from contrasting high- and low-predation habitats but reared in "common garden" conditions. We tested two hypothesis: first, that predation, which causes rapid life-history evolution in guppies, also impacts locomotor physiology, and second, that trade-offs would occur between burst and aerobic performance. VO(2max) was higher than predicted from allometry, and resting VO(2) was lower than predicted. There were small interdrainage differences in male VO(2max), but predation did not affect VO(2max) in either sex. Maximum burst speed was correlated with size; absolute burst speed was higher in females, but size-adjusted speed was greater in males. For both sexes, burst speed conformed to allometric predictions. There were differences in burst speed between drainages in females, but predation regime did not affect burst speed in either sex. We did not find a significant correlation between burst speed and VO(2max), suggesting no trade-off between these traits. These results indicate that predation-mediated evolution of guppy life history does not produce concomitant evolution in aerobic capacity and maximum burst speed. However, other aspects of swimming performance (response latencies or acceleration) might show adaptive divergence in contrasting predation regimes.     

Constraints on adaptive evolution: the functional trade-off between reproduction and fast-start swimming performance in the Trinidadian guppy (Poecilia reticulata)

The empirical study of natural selection reveals that adaptations often involve trade-offs between competing functions. Because natural selection acts on whole organisms rather than isolated traits, adaptive evolution may be constrained by the interaction between traits that are functionally integrated. Yet, few attempts have been made to characterize how and when such constraints are manifested or whether they limit the adaptive divergence of populations. Here we examine the consequences of adaptive life-history evolution on locomotor performance in the live-bearing guppy. In response to increased predation from piscivorous fish, Trinidadian guppies evolve an increased allocation of resources toward reproduction. These populations are also under strong selection for rapid fast-start swimming performance to evade predators. Because embryo development increases a female's wet mass as she approaches parturition, an increased investment in reproductive allocation should impede fast-start performance. We find evidence for adaptive but constrained evolution of fast-start swimming performance in laboratory trials conducted on second-generation lab-reared fish. Female guppies from high-predation localities attain a faster acceleration and velocity and travel a greater distance during fast-start swimming trials. However, velocity and distance traveled decline more rapidly over the course of pregnancy in these same females, thus reducing the magnitude of divergence in swimming performance between high- and low-predation populations. This functional trade-off between reproduction and swimming performance reveals how different aspects of the phenotype are integrated and highlights the complexity of adaptation at the whole-organism level.     

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.     

PHENOTYPIC DIVERSIFICATION ACROSS AN ENVIRONMENTAL GRADIENT: A ROLE FOR PREDATORS AND RESOURCE AVAILABILITY ON THE EVOLUTION OF LIFE HISTORIES

Changes in age/size‐specific mortality, due to such factors as predation, have potent evolutionary consequences. However, interactions with predators commonly impact prey growth rates and food availability and such indirect effects may also influence evolutionary change. We evaluated life‐history differences in Trinidadian killifish, Rivulus hartii, across a gradient in predation. Rivulus are located in (1) “high predation” sites with large piscivores, (2) “Rivulus/guppy” sites with guppies, and (3) “Rivulus‐only” sites with just Rivulus. Rivulus suffer higher mortality with large predators, and guppies may prey upon small/young Rivulus in Rivulus/guppy environments. In turn, population densities decline while growth rates increase in both localities compared to Rivulus‐only sites. To explore how the direct and indirect effects of predators and guppies influence trait diversification in Rivulus, we examined life‐history phenotypes across five rivers. High predation phenotypes exhibited a smaller size at reproduction, a greater number of eggs that were smaller, and increased reproductive allotment. Such changes are consistent with a direct response to predation. Rivulus from Rivulus/guppy sites were intermediate; they exhibited a smaller size at reproduction, increased fecundity, smaller eggs, and larger reproductive allotment than Rivulus‐only fish. These changes are consistent with models that incorporate the impacts of growth and resources.     

Adding parasites to the guppy-predation story: insights from field surveys

Studies of phenotypic variation in nature often consider only a single potential selective agent. In such cases, it remains an open question as to whether variation attributed to that single measured agent might be influenced by some other unmeasured agent. Previous research has shown that phenotypic variation in the Trinidadian guppy (Poecilia reticulata) is strongly influenced by predation regime, and we here ask whether parasitism might represent an additional important selective agent shaping this variation. We performed a field survey of 26 natural guppy populations of known predation regime in northern Trinidad. We quantified levels of parasitism of guppies by the monogenean ecotoparasite, Gyrodactylus, and examined whether this parasite was associated with guppy body size or male colour. Spatial variation in Gyrodactylus parasitism was consistent between years, and parasite prevalence was generally, but not always, higher at high-predation sites than at low-predation sites. Consistent with previous work, predation regime was related to guppy size and some aspects of male colour, whereas parasitism showed few and only minor associations with the same traits. Moreover, a consideration of parasitism did not alter any interpretations regarding associations between guppy traits and predation regimes. These results suggest that parasitism, at least as quantified in the present study, does not play a major role in shaping variation in guppy body size or colour. Nevertheless, considerable variation in these traits, even within a predation regime, suggests the likely importance of other selective agents beyond just predation regime.     

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.     

This is not déjà vu all over again: male guppy colour in a new experimental introduction

We use an experimental introduction in nature to examine factors that influence parallel evolution. In 1996, 200 high-predation guppies (Poecilia reticulata) from the Yarra River were introduced into the Damier River, which previously lacked guppies. Eight years later, we quantified the colour of wild-caught guppies ('phenotypic' divergence) and lab-reared guppies ('genetic' divergence) from low- and high-predation environments in both rivers. Phenotypic and genetic divergence between predation environments within the Yarra was evident for black and for orange. Phenotypic divergence within the Damier was parallel to the Yarra for black but not for orange. Genetic divergence was absent between predation environments within the Damier, but was evident when comparing both Damier populations to their Yarra ancestors. The evolution of male colour thus depends on factors other than the simple contrast between 'high' and 'low' predation. We suggest that the parallel evolution of male signalling traits may sometimes first require the parallel evolution of female preferences.     

INFLUENCE OF THE INDIRECT EFFECTS OF GUPPIES ON LIFE‐HISTORY EVOLUTION IN RIVULUS HARTII

Early theories of life‐history evolution predict that increased predation on young/small individuals selects for delayed maturation and decreased reproductive effort, but such theory only considers changes in mortality. Predators reduce prey abundance and increase food to survivors. Theory that incorporates such indirect effects yields different predictions. Trinidadian killifish, Rivulus hartii, inhabit communities with and without guppies. Guppies prey on young Rivulus and Rivulus densities decline and growth rates increase when guppies are present. Prior work showed that Rivulus phenotypes from communities with guppies matured earlier and had higher fecundity, consistent with theories that incorporate indirect effects. Here we examined the genetic basis of these differences by rearing 2nd generation, laboratory‐born Rivulus from sites with and without guppies under two food levels that match natural differences in growth. Many locality × food interactions were significant, often reversing the relationship between communities. Such interactions imply that there are fitness trade‐offs associated with adaptation to high or low resource environments. On high food, Rivulus from localities with guppies matured earlier, produced many small eggs, and exhibited increased reproductive investment; these differences reversed on low food. Our results suggest that indirect effects mold Rivulus evolution and thereby highlight connections between community processes and evolutionary change.     

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.     

Disturbance cues as a source of risk assessment information under natural conditions

1. Disturbance cues are released by stressed or disturbed prey prior to a predator attack and convey useful risk assessment information regarding local threats. While studies have shown that disturbance cues may be important early on within the predation sequence (prior to an attack), their role in predator–prey interactions remains relatively overlooked by ecologists. Critically, experimental studies examining disturbance cues, especially among prey fishes, have been conducted primarily under laboratory or semi-natural conditions.
2. Here, we tested the prediction that disturbance cues function as sources of risk assessment information in situ. We exposed Trinidadian guppies, in two natural populations differing in predation risk, to a model predator paired with stream water or the disturbance cue collected from guppies from either a high- or low-predation risk population.
3. We found that the predator inspection response of guppies to disturbance cues depends on the level of risk of both the focal and the cue source population. Guppies from both populations exhibited increased latencies to inspect, lower inspection rates and reduced inspecting group sizes towards the model paired with conspecific disturbance cues versus a stream water control. Interestingly, guppies of both populations showed evidence of higher perceived predation risk towards the disturbance cues collected from high-predation risk donors compared to low-predation risk donors.
4. Our results support the hypothesis that disturbance cues function as a source of information used by prey fish in the assessment of predation risk and provide the first evidence of disturbance cue function under fully natural conditions.

     

Experimentally induced life-history evolution in a killifish in response to the introduction of guppies

Life-history theory predicts that increased predation on juvenile age/size-classes favors delayed maturation and decreased reproductive investment. Although this theory has received correlative support, experimental tests in nature are rare. In 1976 and 1981, guppies (Poecilia reticulata) were transplanted into localities that previously only contained a killifish, Rivulus hartii. This situation presents an opportunity to experimentally test this life-history prediction because guppies prey upon young Rivulus. We evaluated the response to selection in Rivulus by measuring phenotypic and genotypic divergence between introduction and upstream "control" localities that lack guppies. Contrary to expectations, Rivulus from the introduction sites evolved earlier maturation and increased reproductive investment within 25 years. Such evolutionary changes parallel previous investigations on natural communities of Rivulus, but do not comply with predictions of age/size-specific theory. Guppies also caused reduced densities and increased growth rates of Rivulus, which are hypothesized indirect effects of predation. Additional life-history theories show that changes in density and growth can interact with predator-induced mortality to alter the predicted trajectory of evolution. We discuss how these latter frameworks improve the fit between theory and evolution in Rivulus.     

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.