Parasite transmission among relatives halts Red Queen dynamics

The theory that coevolving hosts and parasites create a fluctuating selective environment for one another (i.e., produce Red Queen dynamics) has deep roots in evolutionary biology; yet empirical evidence for Red Queen dynamics remains scarce. Fluctuating coevolutionary dynamics underpin the Red Queen hypothesis for the evolution of sex, as well as hypotheses explaining the persistence of genetic variation under sexual selection, local parasite adaptation, the evolution of mutation rate, and the evolution of nonrandom mating. Coevolutionary models that exhibit Red Queen dynamics typically assume that hosts and parasites encounter one another randomly. However, if related individuals aggregate into family groups or are clustered spatially, related hosts will be more likely to encounter parasites transmitted by genetically similar individuals. Using a model that incorporates familial parasite transmission, we show that a slight degree of familial parasite transmission is sufficient to halt coevolutionary fluctuations. Our results predict that evidence for Red Queen dynamics, and its evolutionary consequences, are most likely to be found in biological systems in which hosts and parasites mix mainly at random, and are less likely to be found in systems with familial aggregation. This presents a challenge to the Red Queen hypothesis and other hypotheses that depend on coevolutionary cycling.     

Parasite-mediated disruptive selection in a natural <Emphasis Type="Italic">Daphnia</Emphasis> population

Background  

A mismatch has emerged between models and data of host-parasite evolution. Theory readily predicts that parasites can promote host diversity through mechanisms such as disruptive selection. Yet, despite these predictions, empirical evidence for parasite-mediated increases in host diversity remains surprisingly scant.     

The evolution of intermediate castration virulence and ant coexistence in a spatially structured environment

Theory suggests that spatial structuring should select for intermediate levels of virulence in parasites, but empirical tests are rare and have never been conducted with castration (sterilizing) parasites. To test this theory in a natural landscape, we construct a spatially explicit model of the symbiosis between the ant-plant Cordia nodosa and its two, protecting ant symbionts, Allomerus and Azteca . Allomerus is also a castration parasite, preventing fruiting to increase colony fecundity. Limiting the dispersal of Allomerus and host plant selects for intermediate castration virulence. Increasing the frequency of the mutualist, Azteca , selects for higher castration virulence in Allomerus , because seeds from Azteca -inhabited plants are a public good that Allomerus exploits. These results are consistent with field observations and, to our knowledge, provide the first empirical evidence supporting the hypothesis that spatial structure can reduce castration virulence and the first such evidence in a natural landscape for either mortality or castration virulence.     

Parasites and supernormal manipulation.

Social parasites may exploit their hosts by mimicking other organisms that the hosts normally benefit from investing in or responding to in some other way. Some parasites exaggerate key characters of the organisms they mimic, possibly in order to increase the response from the hosts. The huge gape and extreme begging intensity of the parasitic common cuckoo chick (Cuculus canorus) may be an example. In this paper, the evolutionary stability of manipulating hosts through exaggerated signals is analysed using game theory. Our model indicates that a parasite's signal intensity must be below a certain threshold in order to ensure acceptance and that this threshold depends directly on the rate of parasitism. The only evolutionarily stable strategy (ESS) combination is when hosts accept all signallers and parasites signal at their optimal signal intensity, which must be below the threshold. Supernormal manipulation by parasites is only evolutionarily stable under sufficiently low rates of parasitism. If the conditions for the ESS combination are not satisfied, rejector hosts can invade using signal intensity as a cue for identifying parasites. These qualitative predictions are discussed with respect to empirical evidence from parasitic mimicry systems that have been suggested to involve supernormal signalling, including evicting avian brood parasites and insect-mimicking Ophrys orchids.     

Mechanisms of disease-induced extinction

Parasites are important determinants of ecological dynamics. Despite the widespread perception that parasites (in the broad sense, including microbial pathogens) threaten species with extinction, the simplest deterministic models of parasite dynamics (i.e. of specialist parasites with density‐dependent transmission) predict that parasites will always go extinct before their hosts. We review the primary theoretical mechanisms that allow disease‐induced extinction and compare them with the empirical literature on parasitic threats to populations to assess the importance of different mechanisms in threatening natural populations. Small pre‐epidemic population size and the presence of reservoirs are the most commonly cited factors for disease‐induced extinction in empirical studies.     

The role of parasites in regulating host abundance

It has been 11 years since Anderson and May demonstrated the theoretical ability of helminth parasites to regulate host population abundance. In this review we consider how their work has advanced our understanding of the role of parasites in host populations. In particular Marilyn Scott and Andy Dobson consider three questions. What is meant by regulation? Is there empirical evidence that parasites can regulate host population abundance? Is it possible to predict the sort of host parasite association where one is most likely to be able to detect parasites as a major regulatory force?     

Bloody‐minded parasites and sex: the effects of fluctuating virulence

Asexual lineages can grow at a faster rate than sexual lineages. Why then is sexual reproduction so widespread? Much empirical evidence supports the Red Queen hypothesis. Under this hypothesis, coevolving parasites favour sexual reproduction by adapting to infect common asexual clones and driving them down in frequency. One limitation, however, seems to challenge the generality of the Red Queen: in theoretical models, parasites must be very virulent to maintain sex. Moreover, experiments show virulence to be unstable, readily shifting in response to environmental conditions. Does variation in virulence further limit the ability of coevolving parasites to maintain sex? To address this question, we simulated temporal variation in virulence and evaluated the outcome of competition between sexual and asexual females. We found that variation in virulence did not limit the ability of coevolving parasites to maintain sex. In fact, relatively high variation in virulence promoted parasite‐mediated maintenance of sex. With sufficient variation, sexual females persisted even when mean virulence fell well below the threshold virulence required to maintain sex under constant conditions. We conclude that natural variation in virulence does not limit the relevance of the Red Queen hypothesis for natural populations; on the contrary, it could expand the range of conditions over which coevolving parasites can maintain sex.     

The regulation of gastrointestinal helminth populations

One quarter of the world's human population suffers infection with helminth parasites. The population dynamics of the ten or so species, which cause disease of clinical significance have been well characterized by epidemiological field survey. The parasites are in general highly aggregated between hosts, and their populations seem to be temporally stable and to recover rapidly from perturbation, including interventions designed to alleviate disease. This paper reviews current understanding of the population regulation of helminth species of medical significance. Both empirical (field and laboratory) and theoretical results are included, and we attempt to interpret the findings in the broader context of the population ecology of free-living species. We begin by considering the evidence for regulation from field data concerning the temporal stability of helminth populations within communities and from the results of perturbation experiments. The detection of regulatory processes is then discussed (with regard to statistical and logistical considerations), and the evidence from both the field and laboratory studies reviewed. Deterministic models are described to investigate the possible consequences of regulation imposed at different points in the parasite life-cycle. The causes and consequences of parasite aggregation are considered, and a stochastic model used to investigate the impact of different combination of regulatory processes and heterogeneity generating mechanisms.     

Diffuse coevolution: constraints on a generalist parasite favor use of a dead-end host

Many evolutionary models and empirical studies of parasite-host interactions consider single species of parasites exploiting single host species. However, many parasites are generalists in that they parasitize more than one host species (often many more) and establish associations with other hosts that cannot be described as true parasitism. We identify such an association, explain how constraints may maintain it, and indicate why such diffuse interactions are deserving of attention. We describe the use of two closely related Sympetrum dragonfly species by larvae of the water mite Arrenurus planus Marshall. Adults of one dragonfly species are resistant whereas adults of the other species are almost wholly susceptible to A. planus . However, A. planus attaches as often to the resistant host as it does to the susceptible host species when relative abundance and seasonal timing of adult emergence of both species is considered. We present evidence that mites track the susceptible host and are most active early in the season, when early-emerging unsuitable hosts are also present. Thus, use of resistant hosts appears an unavoidable outcome of constraints promoting discovery and use of susceptible hosts. Such findings have implications for studies of local adaptation and host switching.     

Social networks and the spread of Salmonella in a sleepy lizard population

Although theoretical models consider social networks as pathways for disease transmission, strong empirical support, particularly for indirectly transmitted parasites, is lacking for many wildlife populations. We found multiple genetic strains of the enteric bacterium Salmonella enterica within a population of Australian sleepy lizards (Tiliqua rugosa), and we found that pairs of lizards that shared bacterial genotypes were more strongly connected in the social network than were pairs of lizards that did not. In contrast, there was no significant association between spatial proximity of lizard pairs and shared bacterial genotypes. These results provide strong correlative evidence that these bacteria are transmitted from host to host around the social network, rather than that adjacent lizards are picking up the same bacterial genotype from some common source.     

Toxoplasma gondii,sex and premature rejection

Adaptive sex ratio theory explains why gametocyte sex ratios are female-biased in many populations of apicomplexan parasites such as Plasmodium and Toxoplasma. Recently, Ferguson has criticized this framework and proposed two alternative explanations--one for vector-borne parasites (e.g. Plasmodium) and one for Toxoplasma. Ferguson raises some interesting issues that certainly deserve more empirical attention. However, it should be pointed out that: (1) there are theoretical and empirical problems for his alternative hypotheses; and (2) existing empirical data support the application of sex ratio theory to these parasites, not its rejection.     

The virulence–transmission trade-off in vector-borne plant viruses: a review of (non-)existing studies

The adaptive hypothesis invoked to explain why parasites harm their hosts is known as the trade-off hypothesis, which states that increased parasite transmission comes at the cost of shorter infection duration. This correlation arises because both transmission and disease-induced mortality (i.e. virulence) are increasing functions of parasite within-host density. There is, however, a glaring lack of empirical data to support this hypothesis. Here, we review empirical investigations reporting to what extent within-host viral accumulation determines the transmission rate and the virulence of vector-borne plant viruses. Studies suggest that the correlation between within-plant viral accumulation and transmission rate of natural isolates is positive. Unfortunately, results on the correlation between viral accumulation and virulence are very scarce. We found only very few appropriate studies testing such a correlation, themselves limited by the fact that they use symptoms as a proxy for virulence and are based on very few viral genotypes. Overall, the available evidence does not allow us to confirm or refute the existence of a transmission–virulence trade-off for vector-borne plant viruses. We discuss the type of data that should be collected and how theoretical models can help us refine testable predictions of virulence evolution.     

Disease Ecology Meets Ecosystem Science

Growing evidence indicates that parasites—when considered—can play influential roles in ecosystem structure and function, highlighting the need to integrate disease ecology and ecosystem science. To strengthen links between these traditionally disparate fields, we identified mechanisms through which parasites can affect ecosystems and used empirical literature searches to explore how commonly such mechanisms have been documented, the ecosystem properties affected, and the types of ecosystems in which they occur. Our results indicate that ecosystem-disease research has remained consistently rare, comprising less than 2% of disease ecology publications. Existing studies from terrestrial, freshwater, and marine systems, however, demonstrate that parasites can strongly affect (1) biogeochemical cycles of water, carbon, nutrients, and trace elements, (2) fluxes of biomass and energy, and (3) temporal ecosystem dynamics including disturbance, succession, and stability. Mechanistically, most studies have demonstrated density-mediated indirect effects, rather than trait-mediated effects, or direct effects of parasites, although whether this is representative remains unclear. Looking forward, we highlight the importance of applying traits-based approaches to predict when parasites are most likely to exert ecosystem-level effects. Future research should include efforts to extend host–parasite studies across levels of ecological organization, large-scale manipulations to experimentally quantify ecosystem roles of parasites, and the integration of parasites and disease into models of ecosystem functioning.     

Parasites and sex: Catching the red queen

One version of the Red Queen hypothesis suggests that sexual reproduction may be an advantage in a coevolutionary arms race. Antagonistic biotic interactions, especially those between parasite and host, are thought to represent a sufficient evolutionary force to counterbalance the supposed inefficiency of sexual reproduction. Recent experimental studies demonstrate negative frequency-dependent selection, increased parasite load in parthenogenetic races relative to sympatric sexual conspecifics and correlations between recombination rate and frequency of parasitic chromosomes. These studies provide strong empirical evidence that there is an important role for parasites in maintaining sex.     

Pathways to mutualism breakdown

Mutualisms are ubiquitous in nature despite the widely held view that they are unstable interactions. Models predict that mutualists might often evolve into parasites, can abandon their partners to live autonomously and are also vulnerable to extinction. Yet a basic empirical question, whether mutualisms commonly break down, has been mostly overlooked. As we discuss here, recent progress in molecular systematics helps address this question. Newly constructed phylogenies reveal that parasites as well as autonomous (non-mutualist) taxa are nested within ancestrally mutualistic clades. Although models have focused on the propensity of mutualism to become parasitic, such shifts appear relatively rarely. By contrast, diverse systems exhibit reversions to autonomy, and this might be a common and unexplored endpoint to mutualism.     

THE EVOLUTIONARY IMPLICATIONS OF CONFLICT BETWEEN PARASITES WITH DIFFERENT TRANSMISSION MODES

Understanding the processes that shape the evolution of parasites is a key challenge for evolutionary biology. It is well understood that different parasites may often infect the same host and that this may have important implications to the evolutionary behavior. Here we examine the evolutionary implications of the conflict that arises when two parasite species, one vertically transmitted and the other horizontally transmitted, infect the same host. We show that the presence of a vertically transmitted parasite (VTP) often leads to the evolution of higher virulence in horizontally transmitted parasites (HTPs), particularly if the VTPs are feminizing. The high virulence in some HTPs may therefore result from coinfection with cryptic VTPs. The impact of an HTP on a VTP evolution depends crucially on the nature of the life‐history trade‐offs. Fast virulent HTPs select for intermediate feminization and virulence in VTPs. Coevolutionary models show similar insights, but emphasize the importance of host life span to the outcome, with higher virulence in both types of parasite in short‐lived hosts. Overall, our models emphasize the interplay of host and parasite characteristics in the evolutionary outcome and point the way for further empirical study.     

Helminths as vectors of pathogens in vertebrate hosts: a theoretical approach

Pathogens frequently use vectors to facilitate transmission between hosts and, for vertebrate hosts, the vectors are typically ectoparasitic arthropods. However, other parasites that are intimately associated with their hosts may also be ideal candidate vectors; namely the parasitic helminths. Here, we present empirical evidence that helminth vectoring of pathogens occurs in a range of vertebrate systems by a variety of helminth taxa. Using a novel theoretical framework we explore the dynamics of helminth vectoring and determine which host-helminth-pathogen characteristics may favour the evolution of helminth vectoring. We use two theoretical models: the first is a population dynamic model amalgamated from standard macro- and microparasite models, which serves as a framework for investigation of within-host interactions between co-infecting pathogens and helminths. The second is an evolutionary model, which we use to predict the ecological conditions under which we would expect helminth vectoring to evolve. We show that, like arthropod vectors, helminth vectors increase pathogen fitness. However, unlike arthropod vectors, helminth vectoring increases the pathogenic impact on the host and may allow the evolution of high pathogen virulence. We show that concomitant infection of a host with a helminth and pathogen are not necessarily independent of one another, due to helminth vectoring of microparasites, with profound consequences for pathogen persistence and the impact of disease on the host population.     

THE EFFECTS OF HOST GENOTYPE AND SPATIAL DISTRIBUTION ON TREMATODE PARASITISM IN A BIVALVE POPULATION

A basic assumption underlying models of host-parasite coevolution is the existence of additive genetic variation among hosts for resistance to parasites. However, estimates of additive genetic variation are lacking for natural populations of invertebrates. Testing this assumption is especially important in view of current models that suggest parasites may be responsible for the evolution of sex, such as the Red Queen hypothesis. This hypothesis suggests that the twofold reproductive disadvantage of sex relative to parthenogenesis can be overcome by the more rapid production of rare genotypes resistant to parasites. Here I present evidence of significant levels of additive genetic variance in parasite resistance for an invertebrate host-parasite system in nature. Using families of the bivalve mollusc, Transennella tantilla, cultured in the laboratory, then exposed to parasites in the field, I quantified heritable variation in parasite resistance under natural conditions. The spatial distribution of outplanted hosts was also varied to determine environmental contributions to levels of parasite infection and to estimate potential interactions of host genotype with environment. The results show moderate but significant levels of heritability for resistance to parasites (h² = 0.36). The spatial distribution of hosts also significantly influenced parasite prevalence such that increased host aggregation resulted in decreased levels of parasite infection. Family mean correlations across environments were positive, indicating no genotype-environment interaction. Therefore, these results provide support for important assumptions underlying coevolutionary models of host-parasite systems.     

Is there empirical evidence for the cost of begging?

Offspring should demand more food than the optimal amount for the parents to bring (parent–offspring conflict), and models on the evolution of parent–offspring communication suggest that an equilibrium is reached when the costs associated with begging make it unprofitable for the offspring to increase its level of begging. Empirical evidence for this cost, however, is mixed, and the conclusions of most of authors are that begging is inexpensive. In this study, the existing empirical evidence for this cost is reviewed. One cost proposed is the attraction of predators due to begging calls, but empirical support for this cost is low. However, studies performed cannot dismiss such a cost. Another possible cost is the metabolic expenditure, but empirical evidence for this cost is mixed, with some works contending that it is low, while others deem it important. Other possible metabolic costs have not been studied. A loss of inclusive fitness may be an important cost for the evolution of begging, and robust empirical evidence does exist for this cost. Costs associated with brood reduction also are reviewed. In conclusion, there is not enough empirical evidence to test the models on the evolution of begging. Most costs proposed have not yet been studied or the approach used has been insufficient to reject the null hypothesis (i.e., absence of cost).