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ABSTRACT: Summary1. Emerging infectious diseases may decimate populations or become endemic, but such worst-case scenarios do not occur as frequently as might be expected, even for virulent parasites.2. One explanation for this apparent paradox is that rapid evolution of host resistance may diminish or terminate epidemics. Theoretical and empirical studies have shown that evolution in host–parasite systems can dramatically alter the prevalence and intensity of infection.3. The potential for rapid evolution to protect host populations from negative effects of virulent parasites depends on the type of parasite-driven evolution that occurs. In some host–parasite systems, evolution of increased host resistance can terminate epidemics. However, evolution resulting from parasite-mediated disruptive selection might actually allow a disease to persist in the host population. Epidemics may also be sustained through coevolution of the parasite.4. The rate of evolution and subsequent disease dynamics will be affected by both the diversity of the host population and the community context in which the host–parasite interaction is embedded. Predators, competitors and food resources can all affect the rates of evolution of hosts and parasites and interact with evolution to determine the outcome of epidemics.5. Freshwater organisms have played an important role in the studies of eco-evolutionary dynamics. Rapid evolution in response to parasitism has been demonstrated in multiple freshwater host species, which appears to have protected some of these populations from the virulent effects of infectious diseases.6. Studies of emerging infectious diseases in freshwater ecosystems should consider the possibility of evolution of hosts and/or parasites on ecological timescales, since this phenomenon can profoundly affect disease dynamics.
Freshwater Biology 03/2011; 56(4):689 - 704. · 3.29 Impact Factor
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ABSTRACT: Trade-offs have been put forward as essential to the generation and maintenance of diversity. However, variation in trade-offs is often determined at the molecular level, outside the scope of conventional ecological inquiry. In this study, we propose that understanding the intracellular basis for trade-offs in microbial systems can aid in predicting and interpreting patterns of diversity. First, we show how laboratory experiments and mathematical models have unveiled the hidden intracellular mechanisms underlying trade-offs key to microbial diversity: (i) metabolic and regulatory trade-offs in bacteria and yeast; (ii) life-history trade-offs in bacterial viruses. Next, we examine recent studies of marine microbes that have taken steps toward reconciling the molecular and the ecological views of trade-offs, despite the challenges in doing so in natural settings. Finally, we suggest avenues for research where mathematical modelling, experiments and studies of natural microbial communities provide a unique opportunity to integrate studies of diversity across multiple scales.
Ecology Letters 09/2010; 13(9):1073-84. · 17.56 Impact Factor
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ABSTRACT: 1. The idea that parasites can affect host diversity is pervasive, and the possibility that parasites can increase host diversity is of particular interest. In this review, we focus on diversity in the resistance of hosts to their parasites, and on the different ways in which parasites can increase or decrease this resistance diversity. 2. Theoretically, parasites can exert many different types of selection on host populations, which each have consequences for host diversity. Specifically, theory predicts that parasites can exert negative frequency-dependent selection (NFDS) and disruptive selection on resistance, both of which increase host diversity, as well as directional selection and stabilizing selection on resistance, both of which decrease host diversity. 3. Despite these theoretical predictions, most biologists think of only NFDS or directional selection for increased resistance in response to parasitism. Here, we present empirical support for all of these types of selection occurring in natural populations. Interestingly, several recent studies demonstrate that there is spatiotemporal variation in the type of selection that occurs (and, therefore, in the effects of parasitism on host diversity). 4. A key question that remains, then, is: What determines the type of parasite-mediated selection that occurs? Theory demonstrates that the answer to this question lies, at least in part, with trade-offs associated with resistance. Specifically, the type of evolution that occurs depends critically on the strength and shape of these trade-offs. This, combined with empirical evidence for a strong effect of environment on the shape and strength of trade-offs, may explain the observed spatiotemporal variation in parasite-mediated selection. 5. We conclude that spatiotemporal variation in parasite-driven evolution is likely to be common, and that this variation may be driven by ecological factors. We suggest that the feedback between ecological and evolutionary dynamics in host-parasite interactions is likely to be a productive area of research. In particular, studies addressing the role of ecological factors (e.g. productivity and predation regimes) in driving the outcome of parasite-mediated selection on host populations are warranted. Such studies are necessary if we are to understand the mechanisms underlying the observed variation in the effects of parasites on host diversity.
Journal of Animal Ecology 06/2009; 78(6):1106-12. · 4.94 Impact Factor
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ABSTRACT: Given the difficulty of testing evolutionary and ecological theory in situ, in vitro model systems are attractive alternatives; however, can we appraise whether an experimental result is particular to the in vitro model, and, if so, characterize the systems likely to behave differently and understand why? Here we examine these issues using the relationship between phenotypic diversity and resource input in the T7-Escherichia coli co-evolving system as a case history. We establish a mathematical model of this interaction, framed as one instance of a super-class of host-parasite co-evolutionary models, and show that it captures experimental results. By tuning this model, we then ask how diversity as a function of resource input could behave for alternative co-evolving partners (for example, E. coli with lambda bacteriophages). In contrast to populations lacking bacteriophages, variation in diversity with differences in resources is always found for co-evolving populations, supporting the geographic mosaic theory of co-evolution. The form of this variation is not, however, universal. Details of infectivity are pivotal: in T7-E. coli with a modified gene-for-gene interaction, diversity is low at high resource input, whereas, for matching-allele interactions, maximal diversity is found at high resource input. A combination of in vitro systems and appropriately configured mathematical models is an effective means to isolate results particular to the in vitro system, to characterize systems likely to behave differently and to understand the biology underpinning those alternatives.
Nature 10/2008; 455(7210):220-3. · 36.28 Impact Factor
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ABSTRACT: Coevolutionary interactions are thought to play a crucial role in diversification of hosts and parasitoids. Furthermore, resource availability has been shown to be a fundamental driver of species diversity. Yet, we still do not have a clear understanding of how resource availability mediates the diversity generated by coevolution between hosts and parasitoids over time. We used experiments with bacteria and bacteriophage to test how resources affect variation in the competitive ability of resistant hosts and temporal patterns of diversity in the host and parasitoid as a result of antagonistic coevolution. Bacteria and bacteriophage coevolved for over 150 bacterial generations under high and low-resource conditions. We measured relative competitive ability of the resistant hosts and phenotypic diversity of hosts and parasitoids after the initial invasion of resistant mutants and again at the end of the experiment. Variation in relative competitive ability of the hosts was both time- and environment-dependent. The diversity of resistant hosts, and the abundance of host-range mutants attacking these phenotypes, differed among environments and changed over time, but the direction of these changes differed between the host and parasitoid. Our results demonstrate that patterns of fitness and diversity resulting from coevolutionary interactions can be highly dynamic.
Evolution 07/2008; 62(8):1830-9. · 5.15 Impact Factor
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ABSTRACT: Adaptive divergence among populations can result in local adaptation, whereby genotypes in native environments exhibit greater fitness than genotypes in novel environments. A body of theory has developed that predicts how different species traits, such as rates of gene flow and generation times, influence local adaptation in coevolutionary species interactions. We used a meta-analysis of local-adaptation studies across a broad range of host-parasite interactions to evaluate predictions about the effect of species traits on local adaptation. We also evaluated how experimental design influences the outcome of local adaptation experiments. In reciprocally designed experiments, the relative gene flow rate of hosts versus parasites was the strongest predictor of local adaptation, with significant parasite local adaptation only in the studies in which parasites had greater gene flow rates than their hosts. When nonreciprocal studies were included in analyses, species traits did not explain significant variation in local adaptation, although the overall level of local adaptation observed was lower in the nonreciprocal than in the reciprocal studies. This formal meta-analysis across a diversity of host-parasite systems lends insight into the role of both biology (species traits) and biologists (experimental design) in detecting local adaptation in coevolving species interactions.
The American Naturalist 04/2008; 171(3):275-90. · 4.72 Impact Factor
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ABSTRACT: Many natural populations are characterized by clinal patterns of adaptation, but it is unclear how gene flow and environmental gradients interact to drive such clines. We addressed this question by directly manipulating dispersal and productivity in an experimental landscape containing a microbial parasitoid, the bacteriophage T7, and its host, the bacterium Escherichia coli. We observed that the adaptation of parasitoids increased on hosts originating from lower-productivity communities in the absence of gene flow. However, adaptation decreased along the same productivity gradient with experimentally imposed gene flow of the host and parasitoid. This occurred despite relatively low rates of gene flow.
The American Naturalist 07/2007; 169(6):794-801. · 4.72 Impact Factor
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ABSTRACT: One of the central challenges of evolutionary biology is to understand how coevolution organizes biodiversity over complex geographic landscapes. Most species are collections of genetically differentiated populations, and these populations have the potential to become adapted to their local environments in different ways. The geographic mosaic theory of coevolution incorporates this idea by proposing that spatial variation in natural selection and gene flow across a landscape can shape local coevolutionary dynamics. These effects may be particularly strong when populations differ across productivity gradients, where gene flow will often be asymmetric among populations. Conclusive empirical tests of this theory have been particularly difficult to perform because they require knowledge of patterns of gene flow, historical population relationships and local selection pressures. We have tested these predictions empirically using a model community of bacteria and bacteriophage (viral parasitoids of bacteria). We show that gene flow across a spatially structured landscape alters coevolution of parasitoids and their hosts and that the resulting patterns of adaptation can fluctuate in both space and time.
Nature 11/2004; 431(7010):841-4. · 36.28 Impact Factor
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ABSTRACT: Although many biologists have embraced microbial model systems as tools to address genetic and physiological questions, the explicit use of microbial communities as model systems in ecology has traditionally been more restricted. Here, we highlight recent studies that use laboratory-based microbial model systems to address ecological questions. Such studies have significantly advanced our understanding of processes that have proven difficult to study in field systems, including the genetic and biochemical underpinnings of traits involved in ecological interactions, and the ecological differences driving evolutionary change. It is the simplicity of microbial model systems that makes them such powerful tools for the study of ecology. Such simplicity enables the high degrees of experimental control and replication that are necessary to address many questions that are inaccessible through field observation or experimentation.
Trends in Ecology & Evolution 05/2004; 19(4):189-97. · 15.75 Impact Factor
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ABSTRACT: Although many biologists have embraced microbial model systems as tools to address genetic and physiological questions, the explicit use of microbial communities as model systems in ecology has traditionally been more restricted. Here, we highlight recent studies that use laboratory-based microbial model systems to address ecological questions. Such studies have significantly advanced our understanding of processes that have proven difficult to study in field systems, including the genetic and biochemical underpinnings of traits involved in ecological interactions, and the ecological differences driving evolutionary change. It is the simplicity of microbial model systems that makes them such powerful tools for the study of ecology. Such simplicity enables the high degrees of experimental control and replication that are necessary to address many questions that are inaccessible through field observation or experimentation.
Trends in Ecology & Evolution.
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ABSTRACT: Insights gained from studying the interactions between viruses and bacteria have important implications for the ecology and evolution of virus–host interactions in many environments and for pathogen–host and predator–prey interactions in general. Here, we focus on the generation and maintenance of diversity, highlighting recent laboratory and field experiments with microorganisms.
Research in Microbiology.