Spatial heterogeneity and the stability of host-parasite coexistence

Spatially heterogeneous environments can theoretically promote more stable coexistence of hosts and parasites by reducing the risk of parasite attack either through providing permanent spatial refuges or through providing ephemeral refuges by reducing dispersal. In experimental populations of Pseudomonas aeruginosa and the bacteriophage PP7, spatial heterogeneity promoted stable coexistence of host and parasite, while coexistence was significantly less stable in the homogeneous environment. Phage populations were found to be persisting on subpopulations of sensitive bacteria. Transferring populations to fresh microcosms every 24 h prevented the development of permanent spatial refuges. However, the lower dispersal rates in the heterogeneous environment were found to reduce parasite transmission thereby creating ephemeral refuges from phage attack. These results suggest that spatial heterogeneity can stabilize an otherwise unstable host-parasite interaction even in the absence of permanent spatial refuges.     

Sex and space destabilize intransitive competition within and between species

Organisms ranging from bacteria and corals to plants and vertebrates can form intransitive competitive networks, in which coexistence can be maintained because no one species or genotype is superior to all others. However, in the simplest case with three competing types, the long-term outcome may not be so clear if two of the three represent the ends of a continuous heritable trait distribution within one species, as has been recently demonstrated empirically in a short-term experiment with plants. Using simulation models of this scenario, results with asexual reproduction confirm previous studies which showed that local interactions promote coexistence. However, with sexual reproduction, genetic variance is reduced because selection fluctuates between favouring the two extremes during population cycles, while sex continually produces intermediates. Sex thus slows the response to selection when it is the strongest and therefore slows the recovery from extreme abundances, creating larger abundance fluctuations. Local interactions do not stabilize dynamics with sex because the resultant spatial patches of one species are genetically heterogeneous, such that particular phenotypes do not benefit from spatial refuges. In sharp contrast to previous models suggesting that sex or local interactions stabilize population dynamics, here sex and local interactions destabilize dynamics and increase extinction risk.     

The Role of Spatial Refuges in Coupled Map Lattice Model for Host-Parasitoid Systems

A Coupled Map Lattice (CML) model, for host-parasitoid Nicholson–Bailey interactions, with an explicit spatial distribution of partial refuge areas, is presented by considering the parasitoid attack rate as a patch dependent parameter. The effect of habitat heterogeneity on the dynamics of both populations, that is, on their spatial distribution and temporal behavior is analyzed. Our results show that depending on many features such as position, size, and fragmentation of a refuge, as well as the dispersal parameters of hosts and parasitoids, together with the parasitoid attack rate, the inclusion of refuges may as well stabilize as destabilize the host-parasitoid dynamics. The results are analyzed for the local and the global scales. Spatial patterns resulting from such heterogeneous patchy environments are also obtained.     

Rodent malaria parasites Plasmodium chabaudi and P. vinckei do not increase their rates of gametocytogenesis in response to mosquito probing

Several vector-borne infectious agents facultatively alter their life history strategies in response to local vector densities. Some evidence suggests that malaria parasites invest more heavily in transmission stage production (gametocytogenesis) when vectors are present. Such a strategy could rapidly increase malaria transmission rates, particularly when adult mosquitoes begin to appear after dry seasons. However, in contrast to a recent experiment with a rodent malaria (Plasmodium chabaudi), we found no change in gametocytogenesis in either P. chabaudi or in another rodent malaria, P. vinckei, when their mouse hosts were exposed to mosquitoes. Positive results in the earlier study may have been because mosquito-feeding caused anaemia in hosts, a known promoter of gametocytogenesis. The substantial evidence that malaria and a variety of other parasites facultatively alter transmission strategies in response to a variety of environmental influences makes our results surprising.     

Host phenology regulates parasite–host demographic cycles and eco‐evolutionary feedbacks

Parasite–host interactions can drive periodic population dynamics when parasites overexploit host populations. The timing of host seasonal activity, or host phenology, determines the frequency and demographic impact of parasite–host interactions, which may govern whether parasites sufficiently overexploit hosts to drive population cycles. We describe a mathematical model of a monocyclic, obligate‐killer parasite system with seasonal host activity to investigate the consequences of host phenology on host–parasite dynamics. The results suggest that parasites can reach the densities necessary to destabilize host dynamics and drive cycling as they adapt, but only in some phenological scenarios such as environments with short seasons and synchronous host emergence. Furthermore, only parasite lineages that are sufficiently adapted to phenological scenarios with short seasons and synchronous host emergence can achieve the densities necessary to overexploit hosts and produce population cycles. Host‐parasite cycles also generate an eco‐evolutionary feedback that slows parasite adaptation to the phenological environment as rare advantageous phenotypes can be driven extinct due to a population bottleneck depending on when they are introduced in the cycle. The results demonstrate that seasonal environments can drive population cycling in a restricted set of phenological patterns and provide further evidence that the rate of adaptive evolution depends on underlying ecological dynamics.     

Spatial heterogeneity and functional response: an experiment in microcosms with varying obstacle densities

Spatial heterogeneity of the environment has long been recognized as a major factor in ecological dynamics. Its role in predator–prey systems has been of particular interest, where it can affect interactions in two qualitatively different ways: by providing (1) refuges for the prey or (2) obstacles that interfere with the movements of both prey and predators. There have been relatively fewer studies of obstacles than refuges, especially studies on their effect on functional responses. By analogy with reaction–diffusion models for chemical systems in heterogeneous environments, we predict that obstacles are likely to reduce the encounter rate between individuals, leading to a lower attack rate (predator–prey encounters) and a lower interference rate (predator–predator encounters). Here, we test these predictions under controlled conditions using collembolans (springtails) as prey and mites as predators in microcosms. The effect of obstacle density on the functional response was investigated at the scales of individual behavior and of the population. As expected, we found that increasing obstacle density reduces the attack rate and predator interference. Our results show that obstacles, like refuges, can reduce the predation rate because obstacles decrease the attack rate. However, while refuges can increase predator dependence, we suggest that obstacles can decrease it by reducing the rate of encounters between predators. Because of their opposite effect on predator dependence, obstacles and refuges could modify in different ways the stability of predator–prey communities.     

Travel costs, oviposition behaviour and the dynamics of insect–plant systems

Insect attack can have major consequences for plant population dynamics. We used individually based simulation models to ask how insect oviposition behaviour influences persistence and potential stability of an herbivore–plant system. We emphasised effects on system dynamics of herbivore travel costs and of two kinds of behaviour that might evolve to mitigate travel costs: insect clutch size behaviour (whether eggs are laid singly or in groups) and female aggregation behaviour (whether females prefer or avoid plants already bearing eggs). Travel costs that increase as plant populations drop lead to inverse density dependence of plant reproduction under herbivore attack. Female clutch size and aggregation behaviours also strongly affect system dynamics. When females lay eggs in large clutches or aggregate their clutches, herbivore damage varies strongly among plants, providing probabilistic refuges that permit plant reproduction and persistence. However, the population dynamics depend strongly on whether insect behaviour is fixed or responds adaptively to plant population size: when (and only when) females increase clutch size or aggregation as plants become rare, refuges from herbivory weaken at high plant density, creating inverse density dependence in plant reproduction. Both herbivore travel costs themselves, and also insect behaviour that might evolve in response to travel costs, can thus create plant density dependence—a basic requirement for regulation of plant populations by their insect herbivores.     

Adaptive host preference and the dynamics of host-parasitoid interactions

Models of two independent host populations and a common parasitoid are investigated. The hosts have density-dependent population growth and only interact indirectly by their effects on parasitoid behavior and population dynamics. The parasitoid is assumed to experience a trade-off in its ability to exploit the two hosts. Three alternative types of parasitoid are investigated: (i) fixed generalists whose consumption rates are those that maximize fitness; (ii) "ideal free" parasitoids, which modify their behavior to maximize their rate of finding unparasitized hosts within a generation; and (iii) "evolving" parasitoids, whose capture rates change between generations based on quantitative genetic determination of the relative attack rates on the two hosts. The primary questions addressed are: (1) Do the different types of adaptive processes stabilize or destabilize the population dynamics? (2) Do the adaptive processes tend to equalize or to magnify differences in host densities? The models show that adaptive behavior and evolution frequently destabilize population dynamics and frequently increase the average difference between host densities.     

Adaptive Host Preference and the Dynamics of Host–Parasitoid Interactions

Models of two independent host populations and a common parasitoid are investigated. The hosts have density-dependent population growth and only interact indirectly by their effects on parasitoid behavior and population dynamics. The parasitoid is assumed to experience a trade-off in its ability to exploit the two hosts. Three alternative types of parasitoid are investigated: (i) fixed generalists whose consumption rates are those that maximize fitness; (ii) “ideal free” parasitoids, which modify their behavior to maximize their rate of finding unparasitized hosts within a generation; and (iii) “evolving” parasitoids, whose capture rates change between generations based on quantitative genetic determination of the relative attack rates on the two hosts. The primary questions addressed are: (1) Do the different types of adaptive processes stabilize or destabilize the population dynamics? (2) Do the adaptive processes tend to equalize or to magnify differences in host densities? The models show that adaptive behavior and evolution frequently destabilize population dynamics and frequently increase the average difference between host densities.     

Ancient host-pathogen associations maintained by specificity of chemotaxis and antibiosis

Switching by parasites to novel hosts has profound effects on ecological and evolutionary disease dynamics. Switching requires that parasites are able to establish contact with novel hosts and to overcome host defenses. For most host–parasite associations, it is unclear as to what specific mechanisms prevent infection of novel hosts. Here, we show that parasitic fungal species in the genus Escovopsis, which attack and consume the fungi cultivated by fungus-growing ants, are attracted to their hosts via chemotaxis. This response is host-specific: Escovopsis spp. grow towards their natural host cultivars more rapidly than towards other closely related fungi. Moreover, the cultivated fungi secrete compounds that can suppress Escovopsis growth. These antibiotic defenses are likewise specific: in most interactions, cultivars can inhibit growth of Escovopsis spp. not known to infect them in nature but cannot inhibit isolates of their naturally infecting pathogens . Cases in which cultivars are susceptible to novel Escovopsis are limited to a narrow set of host–parasite strain combinations. Targeted chemotactic and antibiotic responses therefore explain why Escovopsis pathogens do not readily switch to novel hosts, consequently constraining long-term dynamics of host–parasite coevolution within this ancient association.     

Host-parasite dynamics and the evolution of host immunity and parasite fecundity strategies

We explore evolutionarily stable co-evolution of host-macroparasite interactions in a discrete-time two-species population dynamics model, in which the dynamics may be stable, cyclic or chaotic. The macroparasites are assumed to harm host individuals through decreased reproductive output. Hosts may develop costly immune responses to defend themselves against parasites. Parasites compete with conspecifics by adjusting their fecundities. Overall, the presence of both parasites and the immune response in hosts produces more stable dynamics and lower host population sizes than that observed in the absence of the parasites. In our evolutionary analyses, we show that maximum parasite fecundity is always an evolutionarily stable strategy (ESS), irrespective of the type of population interaction, and that maximum parasite fecundity generally induces a minimum parasite population size through over-exploitation of the host. Phenotypic polymorphisms with respect to immunity in the host species are common and expected in ESS host strategies: the benefits of immunication depend on the frequency of the immune hosts in the population. In particular, the steady-state proportions of immune hosts depend, in addition to all the parameters of the parasite dynamics only on the cost of immunity and on the virulence of parasites in susceptible hosts. The implicit ecological dynamics of the host-parasite interaction affect the proportion of immune host individuals in the population. Furthermore, when changes in certain population parameters cause the dynamics of the host-parasite interaction to move from stability to cyclicity and then to chaos, the proportion of immune hosts tends to decrease; however, we also detected counter-examples to this result. As a whole, incorporating immunological and genetic aspects, as well as life-history trade-offs, into host-macroparasite dynamics produces a rich extension to the patterns observed in the models of ecological interactions and epidemics, and deserves more attention than is currently the case.     

Within-host population dynamics and the evolution of microparasites in a heterogeneous host population

Abstract Why do parasites harm their hosts? The general understanding is that if the transmission rate and virulence of a parasite are linked, then the parasite must harm its host to maximize its transmission. The exact nature of such trade‐offs remains largely unclear, but for vertebrate hosts it probably involves interactions between a microparasite and the host immune system. Previous results have suggested that in a homogeneous host population in the absence of super‐ or coinfection, within‐host dynamics lead to selection of the parasite with an intermediate growth rate that is just being controlled by the immune system before it kills the host (Antia et al. 1994). In this paper, we examine how this result changes when heterogeneity is introduced to the host population. We incorporate the simplest form of heterogeneity–random heterogeneity in the parameters describing the size of the initial parasite inoculum, the immune response of the host, and the lethal density at which the parasite kills the host. We find that the general conclusion of the previous model holds: parasites evolve some intermediate growth rate. However, in contrast with the generally accepted view, we find that virulence (measured by the case mortality or the rate of parasite‐induced host mortality) increases with heterogeneity. Finally, we link the within‐host and between‐host dynamics of parasites. We show how the parameters for epidemiological spread of the disease can be estimated from the within‐host dynamics, and in doing so examine the way in which trade‐offs between these epidemiological parameters arise as a consequence of the interaction of the parasite and the immune response of the host.     

Ancient Host–Pathogen Associations Maintained by Specificity of Chemotaxis and Antibiosis

Switching by parasites to novel hosts has profound effects on ecological and evolutionary disease dynamics. Switching requires that parasites are able to establish contact with novel hosts and to overcome host defenses. For most host–parasite associations, it is unclear as to what specific mechanisms prevent infection of novel hosts. Here, we show that parasitic fungal species in the genus Escovopsis, which attack and consume the fungi cultivated by fungus-growing ants, are attracted to their hosts via chemotaxis. This response is host-specific: Escovopsis spp. grow towards their natural host cultivars more rapidly than towards other closely related fungi. Moreover, the cultivated fungi secrete compounds that can suppress Escovopsis growth. These antibiotic defenses are likewise specific: in most interactions, cultivars can inhibit growth of Escovopsis spp. not known to infect them in nature but cannot inhibit isolates of their naturally infecting pathogens . Cases in which cultivars are susceptible to novel Escovopsis are limited to a narrow set of host–parasite strain combinations. Targeted chemotactic and antibiotic responses therefore explain why Escovopsis pathogens do not readily switch to novel hosts, consequently constraining long-term dynamics of host–parasite coevolution within this ancient association.     

The ecology of virulence

Theoretical work has shown that parasites should evolve intermediate levels of virulence. Less attention has been given to the ecology of virulence. Here I explore population-dynamic models of infection in an annual host. The infection does not kill the host; but it can decrease the number of offspring produced by the host, and the magnitude of this effect depends on host population size. Hence, 'virulence' is density dependent, and is defined here as the difference in birth rates between uninfected and infected hosts, divided by the birth rate of uninfected hosts. The results suggest that infection can be highly virulent at the host's equilibrium density, even though the parasite has no effect on the host's intrinsic birth rate. The results also suggest that parasites may help to stabilize host population dynamics. In general, the impact of infection may be underestimated in natural populations.     

Modeling the ecology of symbiont-mediated protection against parasites

There is increasing evidence that many maternally transmitted symbionts protect their hosts against parasites, thus ensuring their own persistence. Despite the protection they provide, such symbionts are typically found in only a fraction of the host population. This suggests that symbiont-conferred resistance is costly or that the maternal inheritance of symbionts is not perfect. To investigate these hypotheses and other properties of this complex ecological system, we develop a mathematical model based on the example of bacterial endosymbionts that protect aphids against parasitoid wasps. Simulations show that in the absence of more complex effects, a very fine balance between the costs of harboring symbionts and the strength of protection they provide is required to maintain coexistence of protected and unprotected hosts. These constraints are significantly relaxed and coexistence becomes a common outcome if deployment of symbiont-provided defenses upon a parasite attack entails an additional (induced) cost. Transmission rates of symbionts also affect coexistence, which is more frequently observed under high (but not perfect) fidelity of vertical transfer and low rates of horizontal transfer. Finally, we show that the prevalence of defensive symbionts has a strong influence on the population dynamics of hosts and parasites: population sizes are stable if and only if protected hosts dominate.     

Host defence versus intraspecific competition in the regulation of infrapopulations of the flea Xenopsylla conformis on its rodent host Meriones crassus

Mechanisms that regulate parasite populations may influence the evolution of hosts and parasites, as well as the stability of host-parasite dynamics but are still poorly understood. A manipulation experiment on the grooming ability of rodent hosts (Meriones crassus) and flea (Xenopsylla conformis) densities on these hosts successfully disentangled two possible regulating mechanisms: (i) behavioural defence of the host and (ii) intraspecific competition among parasites, and revealed their importance in suppressing the feeding of fleas. Moreover, the results suggest that flea competition is direct and is not mediated by host grooming, immune response, or parasite-induced damage to the host. These mechanisms, together with interspecific competition and density-dependent parasite-induced host damage, may limit the parasite burden on an individual host and may prevent parasites from overexploiting their host population.     

Ecological immunology: costly parasite defences and trade-offs in evolutionary ecology

In the face of continuous threats from parasites, hosts have evolved an elaborate series of preventative and controlling measures - the immune system - in order to reduce the fitness costs of parasitism. However, these measures do have associated costs. Viewing an individual's immune response to parasites as being subject to optimization in the face of other demands offers potential insights into mechanisms of life history trade-offs, sexual selection, parasite-mediated selection and population dynamics. We discuss some recent results that have been obtained by practitioners of this approach in natural and semi-natural populations, and suggest some ways in which this field may progress in the near future.     

Evolution of pathogen virulence: the role of variation in host phenotype

Selection on pathogens tends to favour the evolution of growth and reproductive rates and a concomitant level of virulence (damage done to the host) that maximizes pathogen fitness. Yet, because hosts often pose varying selective environments to pathogens, one level of virulence may not be appropriate for all host types. Indeed, if a level of virulence confers high fitness to the pathogen in one host phenotype but low fitness in another host phenotype, alternative virulence strategies may be maintained in the pathogen population. Such strategies can occur either as polymorphism, where different strains of pathogen evolve specialized virulence strategies in different host phenotypes or as polyphenism, where pathogens facultatively express alternative virulence strategies depending on host phenotype. Polymorphism potentially leads to specialist pathogens capable of infecting a limited range of host phenotypes, whereas polyphenism potentially leads to generalist pathogens capable of infecting a wider range of hosts. Evaluating how variation among hosts affects virulence evolution can provide insight into pathogen diversity and is critical in determining how host pathogen interactions affect the phenotypic evolution of both hosts and pathogens.     

The coevolution of parasites with host-acquired immunity and the evolution of sex

Abstract. Here I present a deterministic model of the coevolution of parasites with the acquired immunity of their hosts, a system in which coevolutionary oscillations can be maintained. These dynamics can confer an advantage to sexual reproduction within the parasite population, but the effect is not strong enough to outweigh the twofold cost of sex. The advantage arises primarily because sexual reproduction impedes the response to fluctuating epistasis and not because it facilitates the response to directional selection—in fact, sexual reproduction often slows the response to directional selection. Where the cost of sexual reproduction is small, a polymorphism can be maintained between the sexuals and the asexuals. A polymorphism is maintained in which the advantage gained due to recombination is balanced by the cost of sex. At much higher costs of sex, a polymorphism between the asexual and sexual populations can still be maintained if the asexuals do not have a full complement of genotypes available to them, because the asexuals only outcompete those sexuals with which they share the same selected alleles. However, over time we might expect the asexuals to amass the full array of genotypes, thus permanently eliminating sexuals from the population. The sexuals may avoid this fate if the parasite population is finite. Although the model presented here describes the coevolution of parasites with the acquired immune responses of their hosts, it can be compared with other host-parasite models that have more traditionally been used to investigate Red Queen theories of the evolution of sex.     

Selective predation and productivity jointly drive complex behavior in host-parasite systems

Successful invasion of a parasite into a host population and resulting host-parasite dynamics can depend crucially on other members of a host's community such as predators. We do not fully understand how predation intensity and selectivity shape host-parasite dynamics because the interplay between predator density, predator foraging behavior, and ecosystem productivity remains incompletely explored. By modifying a standard susceptible-infected model, we show how productivity can modulate complex behavior induced by saturating and selective foraging behavior of predators in an otherwise stable host-parasite system. When predators strongly prefer parasitized hosts, the host-parasite system can oscillate, but predators can also create alternative stable states, Allee effects, and catastrophic extinction of parasites. In the latter three cases, parasites have difficulty invading and/or persisting in ecosystems. When predators are intermediately selective, these more complex behaviors become less important, but the host-parasite system can switch from stable to oscillating and then back to stable states along a gradient of predator control. Surprisingly, at higher productivity, predators that neutrally select or avoid parasitized hosts can catalyze extinction of both hosts and parasites. Thus, synergy between two enemies can end disastrously for the host. Such diverse outcomes underscore the crucial importance of the community and ecosystem context in which host-parasite interactions occur.