Antagonistic interactions between hosts and parasites are a key structuring force in natural populations, driving coevolution. However, direct empirical evidence of long-term host-parasite coevolution, in particular 'Red Queen' dynamics--in which antagonistic biotic interactions such as host-parasite interactions can lead to reciprocal evolutionary dynamics--is rare, and current data, although consistent with theories of antagonistic coevolution, do not reveal the temporal dynamics of the process. Dormant stages of both the water flea Daphnia and its microparasites are conserved in lake sediments, providing an archive of past gene pools. Here we use this fact to reconstruct rapid coevolutionary dynamics in a natural setting and show that the parasite rapidly adapts to its host over a period of only a few years. A coevolutionary model based on negative frequency-dependent selection, and designed to mimic essential aspects of our host-parasite system, corroborated these experimental results. In line with the idea of continuing host-parasite coevolution, temporal variation in parasite infectivity changed little over time. In contrast, from the moment the parasite was first found in the sediments, we observed a steady increase in virulence over time, associated with higher fitness of the parasite.
The description of coevolutionary dynamics requires a characterization of the evolutionary dynamics of both the parasite and its host. However, a thorough description of the underlying genetics of the coevolutionary process is often extremely difficult to carry out. We propose that measures of adaptation (mean population fitness) across time or space may represent a feasible alternative approach for characterizing important features of the coevolutionary process. We discuss recent experimental work in the light of simple mathematical models of coevolution to demonstrate the potential power of this phenotypic experimental approach.
It has been suggested that the harm parasites cause to their hosts is an unavoidable consequence of parasite reproduction with costs not only for the host but also for the parasite. Castrating parasites are thought to minimize their costs by reducing host fecundity, which may minimize the chances of killing both host and parasite prematurely. We conducted a series of experiments to understand the evolution of virulence of a castrating bacterium in the planktonic crustacean Daphnia magna. By manipulating food levels during the infection of D. magna with the bacterium Pasteuria ramosa, we showed that both antagonists are resource-limited and that a negative correlation between host and parasite reproduction exists, indicating resource competition among the antagonists. Pasteuria ramosa also induces enhanced growth of its hosts (gigantism), which we found to be negatively correlated with host fecundity but positively correlated with parasite reproduction. Because infected hosts never recovered from infections, we concluded that gigantism is beneficial only for the parasite. Hosts, however, have evolved counteradaptations. We showed that infected hosts have enhanced reproduction before castration. This shift to earlier reproduction increases overall host fecundity and compromises parasite reproduction. Finally, we showed that this resource conflict is subject to genetic variation among host and parasite genotypes within a population and is therefore likely to be an important force in the coevolution of virulence in this system. A verbal model is presented and suggests that the adaptive value of gigantism is to store host resources, which are liberated after parasitic castration for later use by the growing parasite. This hypothesis assumes that infections are long lasting, that is, that they have a high life expectancy.
Plants, animals and humans, are colonized by microorganisms (microbiota) and transiently exposed to countless others. The microbiota affects the development and function of essentially all organ systems, and contributes to adaptation and evolution, while protecting against pathogenic microorganisms and toxins. Genetics and lifestyle factors, including diet, antibiotics and other drugs, and exposure to the natural environment, affect the composition of the microbiota, which influences host health through modulation of interrelated physiological systems. These include immune system development and regulation, metabolic and endocrine pathways, brain function and epigenetic modification of the genome. Importantly, parental microbiotas have transgenerational impacts on the health of progeny. Humans, animals and plants share similar relationships with microbes. Research paradigms from humans and other mammals, amphibians, insects, planktonic crustaceans and plants demonstrate the influence of environmental microbial ecosystems on the microbiota and health of organisms, and indicate links between environmental and internal microbial diversity and good health. Therefore, overlapping compositions, and interconnected roles of microbes in human, animal and plant health should be considered within the broader context of terrestrial and aquatic microbial ecosystems that are challenged by the human lifestyle and by agricultural and industrial activities. Here, we propose research priorities and organizational, educational and administrative measures that will help to identify safe microbe-associated health-promoting modalities and practices. In the spirit of an expanding version of "One health" that includes environmental health and its relation to human cultures and habits (EcoHealth), we urge that the lifestyle-microbiota-human health nexus be taken into account in societal decision making.
The gut microbiota impacts many aspects of its host’s biology, and is increasingly considered as a key factor mediating performance of host individuals in continuously changing environments. Here we use gut microbiota transplants to show that both host genotype and gut microbiota mediate tolerance to toxic cyanobacteria in the freshwater crustacean Daphnia magna. Interclonal variation in tolerance to cyanobacteria disappears when Daphnia are made germ-free and inoculated with an identical microbial inoculum. Instead, variation in tolerance among recipient Daphnia mirrors that of the microbiota donors. Metagenetic analyses point to host genotype and external microbial source as important determinants of gut microbiota assembly, and reveal strong differences in gut microbiota composition between tolerant and susceptible genotypes. Together, these results show that both environmentally and host genotype-induced variations in gut microbiota structure mediate Daphnia tolerance to toxic cyanobacteria, pointing to the gut microbiota as a driver of adaptation and acclimatization to cyanobacterial harmful algal blooms in zooplankton.
The increasing urbanization process is hypothesized to drastically alter (semi‐)natural environments with a concomitant major decline in species abundance and diversity. Yet, studies on this effect of urbanization, and the spatial scale at which it acts, are at present inconclusive due to the large heterogeneity in taxonomic groups and spatial scales at which this relationship has been investigated among studies. Comprehensive studies analysing this relationship across multiple animal groups and at multiple spatial scales are rare, hampering the assessment of how biodiversity generally responds to urbanization. We studied aquatic (cladocerans), limno‐terrestrial (bdelloid rotifers) and terrestrial (butterflies, ground beetles, ground‐ and web spiders, macro‐moths, orthopterans and snails) invertebrate groups using a hierarchical spatial design, wherein three local‐scale (200 m × 200 m) urbanization levels were repeatedly sampled across three landscape‐scale (3 km × 3 km) urbanization levels. We tested for local and landscape urbanization effects on abundance and species richness of each group, whereby total richness was partitioned into the average richness of local communities and the richness due to variation among local communities. Abundances of the terrestrial active dispersers declined in response to local urbanization, with reductions up to 85% for butterflies, while passive dispersers did not show any clear trend. Species richness also declined with increasing levels of urbanization, but responses were highly heterogeneous among the different groups with respect to the richness component and the spatial scale at which urbanization impacts richness. Depending on the group, species richness declined due to biotic homogenization and/or local species loss. This resulted in an overall decrease in total richness across groups in urban areas. These results provide strong support to the general negative impact of urbanization on abundance and species richness within habitat patches and highlight the importance of considering multiple spatial scales and taxa to assess the impacts of urbanization on biodiversity.
Habitat selection behavior is an important predator-avoidance strategy for many organisms. Its particular expression is often explained as the result of a tradeoff between avoiding antagonists and acquiring resources. However, there is need for a broader perspective on this behavior, as organisms are often simultaneously involved in complex antagonistic relationships with multiple types of enemies. We show experimentally that a tradeoff between predator and parasite avoidance may be important in the evolution of habitat selection behavior in the waterflea, Daphnia magna. In this species, negatively phototactic clones suffer less from visually hunting predators by residing in deeper and darker portions of the water column during the day. However, this behavior increases the risk of parasitic infections when the Daphnia are exposed to pond sediments containing parasite spores. Positively phototactic clones, which are at a higher risk of predation, are less exposed to parasite spores in the sediment and consequently suffer less from parasitic infection. We show that the increased risk of infection remains even if the animals change their phototactic behavior on exposure to chemical cues from fish. This tradeoff highlights a substantial cost of predator-induced changes in habitat selection behavior. Tradeoffs caused by multiple enemies may explain genetic polymorphism for habitat selection behavior in many natural populations.I n the face of antagonistic interactions, habitat selection strategies in time and space are essential for the survival of many organisms. Many studies on predation have documented the ecological costs of antipredatory habitat selection behavior, such as reduced food intake, reduced competitive strength, and increased susceptibility to predation by a different kind of predator (1, 2). It has been suggested that such costs favor the evolution of inducible defenses (2) such as diel vertical migration (DVM), which is generally considered to be a predatoravoidance strategy of zooplankton (3-5). In this strategy, the zooplankton reside at greater depths during the day, thus reducing their chance of being detected by visual predators (4, 5). It has been shown that DVM can be induced in several taxa by exposing them to predator kairomones (6-8), i.e., chemical cues that indicate the presence of the predator. Phenotypic variation in induced and constitutive (not dependent on environmental stimuli for activation; ref. 9) DVM has a strong genetic component (8,(10)(11)(12), and the trait shows rapid evolutionary response to changing predator regimes (13).Predators are not the only antagonists that the zooplankton face. Parasites (including pathogens) are common in zooplankton populations, and the fitness costs of infection are severe (14-19). Many parasites produce infective stages within the bottom sediments, where they form long-lasting spore banks (14-16). Because DVM is often so pronounced that the zooplankton reside in, at, or near the bottom sediments during the day (20, 21), we hypothesized that t...
The recent emergence of powerful genomic tools, such as high‐throughput genomics, transcriptomics and metabolomics, combined with the study of gnotobiotic animals, have revealed overwhelming impacts of gut microbiota on the host phenotype. In addition to provide their host with metabolic functions that are not encoded in its own genome, evidence is accumulating that gut symbionts affect host traits previously thought to be solely under host genetic control, such as development and behavior. Metagenomics and metatranscriptomics studies further revealed that gut microbial communities can rapidly respond to changes in host diet or environmental conditions through changes in their structural and functional profiles, thus representing an important source of metabolic flexibility and phenotypic plasticity for the host. Hence, gut microbes appear to be an important factor affecting host ecology and evolution which is, however, not accounted for in life‐history theory, or in classic population genetics, ecological and eco‐evolutionary models. In this forum, we shed new light on life history and eco‐evolutionary dynamics by viewing these processes through the lens of host– microbiota interactions. We follow a three‐level approach. First, current knowledge on the role of gut microbiota in host physiology and behavior points out that gut symbionts can be a crucial medium of life‐history strategies. Second, the particularity of the microbiota is based on its multilayered structure, composed of both a core microbiota, under host genetic and immune control, and a flexible pool of microbes modulated by the environment, which differ in constraints on their maintenance and in their contribution to host adaptation. Finally, gut symbionts can drive the ecological and evolutionary dynamics of their host through effects on individual, population, community and ecosystem levels. In conclusion, we highlight some future perspectives for integrative studies to test hypotheses on life history and eco‐evolutionary dynamics in light of the gut microbiota.
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