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.     

Experimental elimination of parasites in nature leads to the evolution of increased resistance in hosts

A reduction in the strength of selection is expected to cause the evolution of reduced trait expression. Elimination of a parasite should thus cause the evolution of reduced resistance to that parasite. To test this prediction in nature, we studied the fourth- and eighth-generation descendants of guppies (Poecilia reticulata) introduced into four natural streams following experimental elimination of a common and deleterious parasite (Gyrodactylus spp.). After two generations of laboratory rearing to control for plasticity and maternal effects, we infected individual fish to assess their resistance to the parasite. Contrary to theoretical expectations, the introduced guppy populations had rapidly and repeatably evolved increased resistance to the now-absent parasite. This evolution was not owing to a resistance-tolerance trade-off, nor to differences in productivity among the sites. Instead, a leading candidate hypothesis is that the rapid life-history evolution typical in such introductions pleiotropically increases parasite resistance. Our study adds a new dimension to the growing evidence for contemporary evolution in the wild, and also points to the need for a re-consideration of simple expectations from host–parasite theory. In particular, our results highlight the need for increased consideration of multiple sources of selection and pleiotropy when studying evolution in natural contexts.     

Can Mixed-Species Groups Reduce Individual Parasite Load? A Field Test with Two Closely Related Poeciliid Fishes (Poecilia reticulata and Poecilia picta)

Predation and parasitism are two of the most important sources of mortality in nature. By forming groups, individuals can gain protection against predators but may increase their risk of being infected with contagious parasites. Animals might resolve this conflict by forming mixed-species groups thereby reducing the costs associated with parasites through a relative decrease in available hosts. We tested this hypothesis in a system with two closely related poeciliid fishes (Poecilia reticulata and Poecilia picta) and their host-specific monogenean ectoparasites (Gyrodactylus spp.) in Trinidad. Fish from three different rivers were sampled from single and mixed-species groups, measured and scanned for Gyrodactylus. The presence and abundance of Gyrodactylus were lower when fish of both species were part of mixed-species groups relative to single-species groups. This is consistent with the hypothesis that mixed-species groups provide a level of protection against contagious parasites. We discuss the importance of potentially confounding factors such as salinity and individual fish size.     

Evolutionary and plastic rescue in multitrophic model communities

Under changing environmental conditions, intraspecific variation can potentially rescue populations from extinction. There are two principal sources of variation that may ultimately lead to population rescue: genetic diversity and phenotypic plasticity. We compared the potential for evolutionary rescue (through genetic diversity) and plastic rescue (through phenotypic plasticity) by analysing their differential ability to produce dynamical stability and persistence in model food webs. We also evaluated how rescue is affected by the trophic location of variation. We tested the following hypotheses: (i) plastic communities are more likely to exhibit stability and persistence than communities in which genetic diversity provides the same range of traits. (ii) Variation at the lowest trophic level promotes stability and persistence more than variation at higher levels. (iii) Communities with variation at two levels have greater probabilities of stability and persistence than communities with variation at only one level. We found that (i) plasticity promotes stability and persistence more than genetic diversity; (ii) variation at the second highest trophic level promotes stability and persistence more than variation at the autotroph level; and (iii) more than variation at two trophic levels. Our study shows that proper evaluation of the rescue potential of intraspecific variation critically depends on its origin and trophic location.     

Estimating a predator-prey dynamical model with the parameter cascades method

Summary .   Ordinary differential equations (ODEs) are widely used in ecology to describe the dynamical behavior of systems of interacting populations. However, systems of ODEs rarely provide quantitative solutions that are close to real field observations or experimental data because natural systems are subject to environmental and demographic noise and ecologists are often uncertain about the correct parameterization. In this article we introduce "parameter cascades" as an improved method to estimate ODE parameters such that the corresponding ODE solutions fit the real data well. This method is based on the modified penalized smoothing with the penalty defined by ODEs and a generalization of profiled estimation, which leads to fast estimation and good precision for ODE parameters from noisy data. This method is applied to a set of ODEs originally developed to describe an experimental predator–prey system that undergoes oscillatory dynamics. The new parameterization considerably improves the fit of the ODE model to the experimental data sets. At the same time, our method reveals that important structural assumptions that underlie the original ODE model are essentially correct. The mathematical formulations of the two nonlinear interaction terms (functional responses) that link the ODEs in the predator–prey model are validated by estimating the functional responses nonparametrically from the real data. We suggest two major applications of "parameter cascades" to ecological modeling: It can be used to estimate parameters when original data are noisy, missing, or when no reliable priori estimates are available; it can help to validate the structural soundness of the mathematical modeling approach.     

Stabilizing mechanisms in a food web with an introduced omnivore

Intraguild predation (IGP) is an omnivorous food web configuration in which the top predator consumes both a competitor (consumer) and a second prey that it shares with the competitor. This omnivorous configuration occurs frequently in food webs, but theory suggests that it is unstable unless stabilizing mechanisms exist that can decrease the strength of the omnivore and consumer interaction. Although these mechanisms have been documented in native food webs, little is known about whether they operate in the context of an introduced species. Here, we study a marine mussel aquaculture system where the introduction of omnivorous mussels should generate an unstable food web that favors the extinction of the consumer, yet it persists. Using field and laboratory approaches, we searched for stabilizing mechanisms that could reduce interaction strengths in the food web. While field zooplankton counts suggested that mussels influence the composition and abundance of copepods, stable isotope results indicated that life‐history omnivory and cannibalism facilitated the availability of prey refugia, and reduced competition and the interaction strength between the mussel omnivore and zooplankton consumers. In laboratory experiments, however, we found no evidence of adaptive feeding which could weaken predator–consumer interactions. Our food web study suggests that the impact of an introduced omnivore may not only depend on its interaction with native species but also on the availability of stabilizing mechanisms that alter the strength of those interactions.     

Food web complexity and chaotic population dynamics

In mathematical models, very simple communities consisting of three or more species frequently display chaotic dynamics which implies that long‐term predictions of the population trajectories in time are impossible. Communities in the wild tend to be more complex, but evidence for chaotic dynamics from such communities is scarce. We used supercomputing power to test the hypothesis that chaotic dynamics become less frequent in model ecosystems when their complexity increases. We determined the dynamical stability of a universe of mathematical, nonlinear food web models with varying degrees of organizational complexity. We found that the frequency of unpredictable, chaotic dynamics increases with the number of trophic levels in a food web but decreases with the degree of complexity. Our results suggest that natural food webs possess architectural properties that may intrinsically lower the likelihood of chaotic community dynamics.     

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.     

Rapid contemporary evolution and clonal food web dynamics

Character evolution that affects ecological community interactions often occurs contemporaneously with temporal changes in population size, potentially altering the very nature of those dynamics. Such eco-evolutionary processes may be most readily explored in systems with short generations and simple genetics. Asexual and cyclically parthenogenetic organisms such as microalgae, cladocerans and rotifers, which frequently dominate freshwater plankton communities, meet these requirements. Multiple clonal lines can coexist within each species over extended periods, until either fixation occurs or a sexual phase reshuffles the genetic material. When clones differ in traits affecting interspecific interactions, within-species clonal dynamics can have major effects on the population dynamics. We first consider a simple predator–prey system with two prey genotypes, parametrized with data from a well-studied experimental system, and explore how the extent of differences in defence against predation within the prey population determine dynamic stability versus instability of the system. We then explore how increased potential for evolution affects the community dynamics in a more general community model with multiple predator and multiple prey genotypes. These examples illustrate how microevolutionary ‘details’ that enhance or limit the potential for heritable phenotypic change can have significant effects on contemporaneous community-level dynamics and the persistence and coexistence of species.