No evidence for a cost of selection by carbaryl exposure in terms of vulnerability to fish predation in <Emphasis Type="Italic">Daphnia magna</Emphasis>

Natural populations are exposed to multiple stressors. These stressors may interact, leading to synergistic or antagonistic responses. In addition to these direct interaction effects, there may also be an interaction between stressors through a selection effect: as the population genetically responds to one stressor, it may become more vulnerable to another one, for instance because of an associated reduction in genetic variation. We here capitalized on a selection experiment involving the exposure of Daphnia populations to carbaryl pulses to test the hypothesis that selection imposed by this pesticide may increase vulnerability to fish predation in the resulting population. A direct predation experiment with individuals isolated from carbaryl-exposed and non-exposed populations revealed no effect of prior selection by carbaryl exposure on mortality due to stickleback predation.     

Evaluating the fitness consequences of plasticity in tolerance to pesticides

In a rapidly changing world, phenotypic plasticity may be a critical mechanism allowing populations to rapidly acclimate when faced with novel anthropogenic stressors. Theory predicts that if exposure to anthropogenic stress is heterogeneous, plasticity should be maintained as it allows organisms to avoid unnecessary expression of costly traits (i.e., phenotypic costs) when stressors are absent. Conversely, if exposure to stressors becomes constant, costs or limits of plasticity may lead to evolutionary trait canalization (i.e., genetic assimilation). While these concepts are well‐established in theory, few studies have examined whether these factors explain patterns of plasticity in natural populations facing anthropogenic stress. Using wild populations of wood frogs that vary in plasticity in tolerance to pesticides, the goal of this study was to evaluate the environmental conditions under which plasticity is expected to be advantageous or detrimental. We found that when pesticides were absent, more plastic populations exhibited lower pesticide tolerance and were more fit than less plastic populations, likely avoiding the cost of expressing high tolerance when it was not necessary. Contrary to our predictions, when pesticides were present, more plastic populations were as fit as less plastic populations, showing no signs of costs or limits of plasticity. Amidst unprecedented global change, understanding the factors shaping the evolution of plasticity will become increasingly important.     

Pesticide exposure strongly enhances parasite virulence in an invertebrate host model

Parasites are a common and constant threat to organisms at all levels of phyla. The virulence of a parasite, defined as the impact on survival and reproduction of its host, depends on the specific host–parasite combination and can also be influenced by environmental conditions. Environmental pollution might be an additional factor influencing host–parasite interactions. We here aimed to test whether the combined stress of pollutant exposure and parasite challenge results in stronger impacts on host organisms than expected from the single stressors applied alone. We used the water flea Daphnia magna and two of its endoparasites, the bacterium Pasteuria ramosa and the microsporidium Flabelliforma magnivora, as invertebrate host–parasite models. For each parasite, we tested in a full‐factorial design for interactions between parasitism and pollution using the neurotoxic pesticide carbaryl as a model substance. Sublethal concentrations of the pesticide synergistically enhanced the virulence of both parasites by increasing host mortality. Furthermore, host castration induced by P. ramosa was accelerated by carbaryl exposure. These effects likely reflect decreased host resistance due to direct or indirect immunosuppressive activity of carbaryl. The present study provides experimental evidence that the in vivo development of infectious diseases can be influenced by a pesticide at environmentally realistic concentrations. This implies that host–parasite interactions and subsequently co‐evolution might be influenced by environmental pollution at toxicant concentrations being sublethal to parasite‐free hosts. Standard toxicity testing as employed in the current way of conducting ecological risk assessments for anthropogenic substances does not consider natural antagonists such as infectious diseases, and thereby likely underestimates the impact these substances may pose to natural populations in the environment.     

Energy acquisition and allocation in an ectothermic predator exposed to a common environmental stressor

Stressors are commonly encountered by organisms and often prove to be energetically costly. Certain stressors can simultaneously affect multiple components of an animal's energy budget and can either exacerbate energetic costs to the individual or offset one another. Here we used a commonly encountered stressor, the pesticide carbaryl, to examine the complex effects that acute environmental disturbances can have on energy expenditure, allocation, and acquisition, important processes that influence growth and reproduction. After exposing lizards (Sceloporus occidentalis) to carbaryl, we measured their metabolism over a 48 h period and assessed their food consumption over 96 h. We found no difference in total energy expenditure among treatment groups, but lizards exposed to the highest dose of carbaryl allocated energy differently than other groups. Compared to controls, these lizards exhibited a 16-30% increase in standard metabolic rate (SMR), which was offset by a 45-58% decrease in additional energy expenditures. Lizards in the highest dose group also exhibited a 30-34% decrease in energy acquisition compared to controls. The net result was a 1.83 kJ decrease in energy assimilation, equivalent to 5 times their daily SMR requirements. Our results indicate that energetic consequences of stressors may result in complex energetic trade-offs, and emphasize the need to simultaneously examine the effect of stressors on multiple portions of an animal's energy budget.     

The costs of evolving resistance in heterogeneous parasite environments

The evolution of host resistance to parasites, shaped by associated fitness costs, is crucial for epidemiology and maintenance of genetic diversity. Selection imposed by multiple parasites could be a particularly strong constraint, as hosts either accumulate costs of multiple specific resistances or evolve a more costly general resistance mechanism. We used experimental evolution to test how parasite heterogeneity influences the evolution of host resistance. We show that bacterial host populations evolved specific resistance to local bacteriophage parasites, regardless of whether they were in single or multiple-phage environments, and that hosts evolving with multiple phages were no more resistant to novel phages than those evolving with single phages. However, hosts from multiple-phage environments paid a higher cost, in terms of population growth in the absence of phage, for their evolved specific resistances than those from single-phage environments. Given that in nature host populations face selection pressures from multiple parasite strains and species, our results suggest that costs may be even more critical in shaping the evolution of resistance than previously thought. Furthermore, our results highlight that a better understanding of resistance costs under combined control strategies could lead to a more 'evolution-resistant' treatment of disease.     

Inter‐ and intraspecific variation of spider mite susceptibility to fungal infections: Implications for the long‐term success of biological control

Spider mites are severe pests of several annual and perennial crops worldwide, often causing important economic damages. As rapid evolution of pesticide resistance in this group hampers the efficiency of chemical control, alternative control strategies, such as the use of entomopathogenic fungi, are being developed. However, while several studies have focused on the evaluation of the control potential of different fungal species and/or isolates as well as their compatibility with other control methods (e.g., predators or chemical pesticides), knowledge on the extent of inter‐ and intraspecific variation in spider mite susceptibility to fungal infection is as yet incipient. Here, we measured the mortality induced by two generalist fungi, Beauveria bassiana and Metarhizium brunneum, in 12 spider mite populations belonging to different Tetranychus species: T. evansi, T. ludeni, and T. urticae (green and red form), within a full factorial experiment. We found that spider mite species differed in their susceptibility to infection by both fungal species. Moreover, we also found important intraspecific variation for this trait. These results draw caution on the development of single strains as biocontrol agents. Indeed, the high level of intraspecific variation suggests that (a) the one‐size‐fits‐all strategy may fail to control spider mite populations and (b) hosts resistance to infection may evolve at a rapid pace. Finally, we propose future directions to better understand this system and improve the long‐term success of spider mite control strategies based on entomopathogenic fungi.     

Rapid Experimental Evolution of Pesticide Resistance in C. elegans Entails No Costs and Affects the Mating System

Pesticide resistance is a major concern in natural populations and a model trait to study adaptation. Despite the importance of this trait, the dynamics of its evolution and of its ecological consequences remain largely unstudied. To fill this gap, we performed experimental evolution with replicated populations of Caenorhabditis elegans exposed to the pesticide Levamisole during 20 generations. Exposure to Levamisole resulted in decreased survival, fecundity and male frequency, which declined from 30% to zero. This was not due to differential susceptibility of males. Rather, the drug affected mobility, resulting in fewer encounters, probably leading to reduced outcrossing rates. Adaptation, i.e., increased survival and fecundity, occurred within 10 and 20 generations, respectively. Male frequency also increased by generation 20. Adaptation costs were undetected in the ancestral environment and in presence of Ivermectin, another widely-used pesticide with an opposite physiological effect. Our results demonstrate that pesticide resistance can evolve at an extremely rapid pace. Furthermore, we unravel the effects of behaviour on life-history traits and test the environmental dependence of adaptation costs. This study establishes experimental evolution as a powerful tool to tackle pesticide resistance, and paves the way to further investigations manipulating environmental and/or genetic factors underlying adaptation to pesticides.     

Evolutionary and Ecological Effects of Multi-Generational Exposures to Anthropogenic Stressors

Biological and ecological responses to stress are dictated by duration and frequency, as well as instantaneous magnitude. Conditional compensatory responses at the physiological and behavioral levels, referred to as ‘acclimation’, may mitigate effects on individuals experiencing brief or infrequent periods of moderate stress. However, even modest stress over extended periods may reduce the fitness of some or all exposed individuals. In this way, specific stress that persists over multiple generations will increase probabilities for extinction of populations composed of sensitive individuals. For populations whose members demonstrate variance and heritability for stressor response, this selective loss of sensitive individuals may result in populations dominated by resistant individuals. The formation of these ‘adapted’ populations may be considered an ecological compensatory mechanism to multi-generational stress. Paradoxically, the biological costs to individuals of toxicity and physiological acclimation may result in obvious signs of stress in affected wildlife populations while the costs of genetic adaptation may be more covert. It is important to consider such costs because recent evidence suggests that anthropogenic stressors have acted as powerful selection agents that have modified the composition of wildlife populations subjected for successive generational exposures to specific stressors. This essay focuses on a case study where adaptation has been demonstrated in fish populations with a history of chronic exposure to persistent, bioaccumulative and toxic environmental contaminants. Because the magnitude, breadth and long-term outcomes of such changes are unknown, ecological risk assessments that are limited in focus to short-term exposures and consequences may seriously underestimate the ecological and evolutionary impacts of anthropogenic stressors.     

Experimental evolution of field populations of Daphnia magna in response to parasite treatment

Although there is little doubt that hosts evolve to reduce parasite damage, little is known about the evolutionary time scale on which host populations may adapt under natural conditions. Here we study the effects of selection by the microsporidian parasite Octosporea bayeri on populations of Daphnia magna. In a field study, we infected replicated populations of D. magna with the parasite, leaving control populations uninfected. After two summer seasons of experimental evolution (about 15 generations), the genetic composition of infected host populations differed significantly from the control populations. Experiments revealed that hosts from the populations that had evolved with the parasite had lower mortality on exposure to parasite spores and a higher competitive ability than hosts that had evolved without the parasite. In contrast, the susceptibility of the two treatment groups to another parasite, the bacterium Pasteuria ramosa, which was not present during experimental evolution of the populations, did not differ. Fitness assays in the absence of parasites revealed a higher fitness for the control populations, but only under low population density with high resource availability. Overall, our results show that, under natural conditions, Daphnia populations are able to adapt rapidly to the prevailing conditions and that this evolutionary change is specific to the environment.     

The evolution of resistance to a parasite is determined by resources

Given the ubiquity of parasites, it is critical to understand the evolution of defense against them. Using a selection experiment performed across a broad range of host resources, I examine how resistance and associated costs depend on resource availability. Higher resistance to a natural viral pathogen evolves in a host when there are more resources, and this directly suggests a resource-dependent cost of the evolution of resistance. Resistance is traded off with host growth rate, and the costs are stronger under poor resource environments, although adaptation to poor environments reduces these costs. The level of resistance and the costs that are paid for this resistance depend on both the selection environment and the environment in which hosts are assayed, implying that different resistance mechanisms may evolve in different environments. More broadly, the results emphasize that environmental heterogeneity in time and space may underpin variation in immune diversity.     

Environmental versus Anthropogenic Effects on Population Adaptive Divergence in the Freshwater Snail Lymnaea stagnalis

Repeated pesticide contaminations of lentic freshwater systems located within agricultural landscapes may affect population evolution in non-target organisms, especially in species with a fully aquatic life cycle and low dispersal ability. The issue of evolutionary impact of pollutants is therefore conceptually important for ecotoxicologists. The impact of historical exposure to pesticides on genetic divergence was investigated in the freshwater gastropod Lymnaea stagnalis, using a set of 14 populations from contrasted environments in terms of pesticide and other anthropogenic pressures. The hypothesis of population adaptive divergence was tested on 11 life-history traits, using Q _ST -F _ST comparisons. Despite strong neutral differentiation (mean F _ST = 0.291), five adult traits or parameters were found to be under divergent selection. Conversely, two early expressed traits showed a pattern consistent with uniform selection or trait canalization, and four adult traits appeared to evolve neutrally. Divergent selection patterns were mostly consistent with a habitat effect, opposing pond to ditch and channel populations. Comparatively, pesticide and other human pressures had little correspondence with evolutionary patterns, despite hatching rate impairment associated with global anthropogenic pressure. Globally, analyses revealed high genetic variation both at neutral markers and fitness-related traits in a species used as model in ecotoxicology, providing empirical support for the need to account for genetic and evolutionary components of population response in ecological risk assessment.     

Rapid growth reduces cold resistance: evidence from latitudinal variation in growth rate, cold resistance and stress proteins

Background

Physiological costs of rapid growth may contribute to the observation that organisms typically grow at submaximal rates. Although, it has been hypothesized that faster growing individuals would do worse in dealing with suboptimal temperatures, this type of cost has never been explored empirically. Furthermore, the mechanistic basis of the physiological costs of rapid growth is largely unexplored.

Methodology/Principal Finding

Larvae of the damselfly Ischnura elegans from two univoltine northern and two multivoltine southern populations were reared at three temperatures and after emergence given a cold shock. Cold resistance, measured by chill coma recovery times in the adult stage, was lower in the southern populations. The faster larval growth rates in the southern populations contributed to this latitudinal pattern in cold resistance. In accordance with their assumed role in cold resistance, Hsp70 levels were lower in the southern populations, and faster growing larvae had lower Hsp70 levels. Yet, individual variation in Hsp70 levels did not explain variation in cold resistance.

Conclusions/Significance

We provide evidence for a novel cost of rapid growth: reduced cold resistance. Our results indicate that the reduced cold resistance in southern populations of animals that change voltinism along the latitudinal gradient may not entirely be explained by thermal selection per se but also by the costs of time constraint-induced higher growth rates. This also illustrates that stressors imposed in the larval stage may carry over and shape fitness in the adult stage and highlights the importance of physiological costs in the evolution of life-histories at macro-scales.     

Ecological and genetic factors influencing evolution of pesticide resistance in tetranychid and phytoseiid mites

Among tetranychid spider mites and their phytoseiid predators, the evolution of pesticide resistance is a common event. In most cases, resistance is based on a single dominant or semidominant gene. However, polygenic, less-stable resistance often develops under laboratory selection. More rapid development of pesticide resistance in spider mites and predatory mites than among other arthropods might partly be due to their arrhenotokous reproduction. For both groups of mites, little study has been done on population genetic factors influencing pesticide resistance. A few studies have focussed on ecological factors. An important ecological factor influencing resistance evolution is the level of immigration of susceptible individuals into treated habitats. Spider mites and predatory mites both tend to reside in treated habitats at high levels and to immigrate at only modest levels from untreated habitats. This favors rapid resistance development. Another factor contributing to rapid resistance evolution in both mite groups is their rapid reproductive rate. A food-limitation factor may limit resistance evolution under field conditions more in predatory mites than spider mites. After treatment by a pesticide, spider mites have an unlimited food source, whereas predatory mites have a decimated food source (their prey), which leads to reduced reproduction, starvation, or migration. Because of the common occurrence of resistance among both mite groups, a strategy of resistance management is often feasible for them. Case histories of IPM where the population dynamics and genetics of pesticide resistance of tetranychid and phytoseiid mites have been considered are discussed. The overall conclusion is that greater understanding of the population genetics and ecology of these species will provide for improved systems of resistance management and IPM.     

Evolution of Drosophila resistance against different pathogens and infection routes entails no detectable maintenance costs

Pathogens exert a strong selective pressure on hosts, entailing host adaptation to infection. This adaptation often affects negatively other fitness‐related traits. Such trade‐offs may underlie the maintenance of genetic diversity for pathogen resistance. Trade‐offs can be tested with experimental evolution of host populations adapting to parasites, using two approaches: (1) measuring changes in immunocompetence in relaxed‐selection lines and (2) comparing life‐history traits of evolved and control lines in pathogen‐free environments. Here, we used both approaches to examine trade‐offs in Drosophila melanogaster populations evolving for over 30 generations under infection with Drosophila C Virus or the bacterium Pseudomonas entomophila, the latter through different routes. We find that resistance is maintained after up to 30 generations of relaxed selection. Moreover, no differences in several classical life‐history traits between control and evolved populations were found in pathogen‐free environments, even under stresses such as desiccation, nutrient limitation, and high densities. Hence, we did not detect any maintenance costs associated with resistance to pathogens. We hypothesize that extremely high selection pressures commonly used lead to the disproportionate expression of costs relative to their actual occurrence in natural systems. Still, the maintenance of genetic variation for pathogen resistance calls for an explanation.     

Assessment of fitness costs of resistance against the parasitoid Leptopilina victoriae in Drosophila bipectinata

How insects evolve resistance or counter-resistance against antagonists is a basic issue in the study of host-parasitoid coevolution. One of the factors that affect their coevolution is fitness costs of resistance and counter-resistance. Here, we assess fitness costs of resistance against the parasitoid Leptopilina victoriae in Drosophila bipectinata on the basis of selection experiments. We made a base population by mixing three geographic fly populations that differed in resistance. The established base population was divided into four populations, two for selection of resistance against a L. victoriae population and two for control. Resistance increased rapidly in response to selection and reached a very high level within four generations in the selected populations, while resistance of the control populations remained low during 20 generations. High resistance of the selected populations was maintained at least for 10 generations after selection was stopped. Both selected populations had lower female longevity than the control populations, and at least one of the selected populations had shorter thorax length, lower female desiccation tolerance and adult heat tolerance than both or either of the control populations. On the other hand, the selected populations had higher male starvation tolerance and longevity than the control populations. There were no significant differences in resistance against another population of L. victoriae and two other parasitoid species between the selected and control populations. These results suggest that the resistance against the L. victoriae population in D. bipectinata may incur some but not so high costs and act parasitoid-species- and/or parasitoid-population-specifically.     

Natives adapting to invasive species: ecology,genes, and the sustainability of conservation

Contemporary anthropogenic evolution is common. Biological invasions are an especially dynamic form of novel selection. This paper considers how native species evolve in response to biological invasions and the potential consequences of such evolution. Among numerous recent cases, the most widely reported instances are of phytophagous insects shifting onto introduced host plants. For example, our studies show that in North America and Australia, soapberry bugs evolved substantially after colonizing introduced hosts. Such cases permit close estimation of evolution’s direction and rate, and we have used cross-rearing studies of derived and ancestral-type populations to measure changes in reaction norms and performance tradeoffs. Different fitness traits have followed very different paths in evolving to their current phenotypic values. Our hybridization studies show that the genetic architecture of these adaptations involves a surprising degree of non-additive variation (epistasis, dominance). The importance of non-additive genetic variation in rapid evolution will be clarified as more studies take advantage of similar situations. As appreciation grows for the deep contemporary interplay of evolution and ecology, debate about qualitative terms describing evolution’s rate will become less relevant. From a conservation standpoint, contemporary evolution in native species presents challenges for ecologically appropriate and sustainable management. Evolving natives and invaders may reconfigure contemporary and future communities. Adaptive evolution may also enhance native communities’ capacity to control invasive populations.     

Local adaptation to biocontrol agents: A multi-objective data-driven optimization model for the evolution of resistance

Spatial and temporal variability in the application of biological control agents such as parasites or pathogenic bacteria can cause the evolution of resistance in pest organisms. Because biocontrol will be more effective if organisms are not resistant, it is desirable to examine the evolution of resistance under different application strategies.We present a computational method that integrates a genetic algorithm with experimental data for predicting when local populations are likely to evolve resistance to biocontrol pathogens. The model incorporates parameters that can be varied as part of pest control measures such as the distribution and severity of the biocontrol agent (e.g., pathogenic fungi). The model predicts the evolution of pathogen defense as well as indirect selection on several aspects of the organism's genetic system. Our results show that both variability of selection within populations as well as mean differences among populations are important in the evolution of defenses against biocontrol pathogens. The mean defense is changed through the pest organism's genotype and the variance is affected by components of the genetic system, namely, the resiliency, recombination rate and number of genes.The data-driven model incorporates experimental data on pathogen susceptibility and the cost of defense. The results suggest that spatial variability rather than uniform application of biological control will limit the evolution of resistance in pest organisms.     

Sexual selection expedites the evolution of pesticide resistance

The evolution of insecticide resistance by crop pests and disease vectors causes serious problems for agriculture and health. Sexual selection can accelerate or hinder adaptation to abiotic challenges in a variety of ways, but the effect of sexual selection on resistance evolution is little studied. Here, we examine this question using experimental evolution in the pest insect Tribolium castaneum. The experimental removal of sexual selection slowed the evolution of resistance in populations treated with pyrethroid pesticide, and also reduced the rate at which resistance was lost from pesticide‐free populations. These results suggest that selection arising from variance in mating and fertilization success can augment natural selection on pesticide resistance, meaning that sexual selection should be considered when designing strategies to limit the evolution of pesticide resistance.     

Brave New World: the epistatic foundations of natives adapting to invaders

Classical examples indicated rapid evolution to be both rare and largely anthropogenic. As the pace and scale of human disturbance increase, such evolution is becoming more the norm. Genetically based adaptation may underlie successful biological invasions, and may likewise characterize responses in natives to invasives. Recent published studies confirm that natives are adapting morphologically, behaviorally, physiologically and life historically to selection from invasive species. Some of the processes involved are evident in our studies of recent host shifts to invasive plants by native soapberry bugs in North America and Australia. On both continents populations have differentiated extensively in fitness traits. Genetic architecture of these adaptations involves a surprising degree of non-additive variation (epistasis, dominance), a result that in theory may reflect a history of colonization by a small number of individuals followed by population growth. Such “founder-flush” events may unleash extraordinary evolutionary potential, and their importance will be clarified as more studies take advantage of the accidental perturbation experiments that biotic invasions represent. From a conservation standpoint, rapid evolution in natives will present challenges for ecologically appropriate and sustainable management, but at the same time may enhance the capacity of the native community to act in the biological control of invasive species.