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.     

Coinfecting parasites can modify fluctuating selection dynamics in host–parasite coevolution

Genetically specific interactions between hosts and parasites can lead to coevolutionary fluctuations in their genotype frequencies over time. Such fluctuating selection dynamics are, however, expected to occur only under specific circumstances (e.g., high fitness costs of infection to the hosts). The outcomes of host–parasite interactions are typically affected by environmental/ecological factors, which could modify coevolutionary dynamics. For instance, individual hosts are often infected with more than one parasite species and interactions between them can alter host and parasite performance. We examined the potential effects of coinfections by genetically specific (i.e., coevolving) and nonspecific (i.e., generalist) parasite species on fluctuating selection dynamics using numerical simulations. We modeled coevolution (a) when hosts are exposed to a single parasite species that must genetically match the host to infect, (b) when hosts are also exposed to a generalist parasite that increases fitness costs to the hosts, and (c) when coinfecting parasites compete for the shared host resources. Our results show that coinfections can enhance fluctuating selection dynamics when they increase fitness costs to the hosts. Under resource competition, coinfections can either enhance or suppress fluctuating selection dynamics, depending on the characteristics (i.e., fecundity, fitness costs induced to the hosts) of the interacting parasites.     

Evidence of parasite-mediated disruptive selection on genetic diversity in a wild fish population

Identifying the processes maintaining genetic variability in wild populations is a major concern in conservation and evolutionary biology. Parasite-mediated selection may strongly affect genetic variability in wild populations. The inbreeding depression theory predicts that directional selection imposed by parasites should act against the most inbred hosts, thus favouring genetic diversity in wild populations. We have tested this prediction by evaluating the strength and shape of the relationship between the load of a harmful fin-feeder ectoparasite ( Tracheliastes polycolpus ) and the genome-wide genetic diversity (i.e. heterozygosity measured at a set of 15 microsatellites) of its fish host, the rostrum dace ( Leuciscus leuciscus ). Contrary to expectation, we found a nonlinear relationship between host genetic diversity and ectoparasite load, with hosts that were either homozygous or heterozygous harbouring significantly fewer parasites than hosts with an intermediate level of heterozygosity. This relationship suggests that parasites could increase the variance of global heterozygosity in this host population through disruptive selection on genetic diversity. Moreover, when genetic diversity was measured at each locus separately, we found two very strong positive associations between host genetic diversity and the ectoparasite load. This latter result has three main implications: (i) genome-wide effect cannot alone explain the nonlinear relationship between global heterozygosity and ectoparasite load, (ii) negative non-additive allelic interactions (i.e. underdominance) may be a mechanism for resisting ectoparasite infection, and (iii) ectoparasites may favour homozygosity at some loci in this host population.     

Interaction of a host plant and its holoparasite: effects of previous selection by the parasite

If parasites decrease the fitness of their hosts one could expect selection for host traits (e.g. resistance and tolerance) that decrease the negative effects of parasitic infection. To study selection caused by parasitism, we used a novel study system: we grew host plants (Urtica dioica) that originated from previously parasitized and unparasitized natural populations (four of each) with or without a holoparasitic plant (Cuscuta europaea). Infectivity of the parasite (i.e. qualitative resistance of the host) did not differ between the two host types. Parasites grown with hosts from parasitized populations had lower performance than parasites grown with hosts from unparasitized populations, indicating host resistance in terms of parasite’s performance (i.e. quantitative resistance). However, our results suggest that the tolerance of parasitic infection was lower in hosts from parasitized populations compared with hosts from unparasitized populations as indicated by the lower above‐ground vegetative biomass of the infected host plants from previously parasitized populations.     

Determinants of host-specificity in parasites of freshwater fishes.

Factors responsible for interspecific variability in host-specificity were investigated within 15 genera (including 176 species) of metazoan parasites found in Canadian freshwater fish. For each species in a genus, the parasite's number of known hosts was determined from published host-parasite records. The effects of the total number and mean size of potential hosts (i.e. all fish species belonging to the family or families that include a parasite's known hosts) on number of hosts of congeneric species were evaluated using multiple regressions. Since parasite species that have been recorded often tend to have greater numbers of known hosts than do seldom-recorded parasites, it was necessary to control for the confounding effect of study intensity. In all parasite genera, whether from highly specific taxa such as monogeneans or from less host-specific ones, there was a positive relationship between the number of potential hosts and the number of known hosts. However, no consistent relationships were observed between the mean size of potential hosts and number of known hosts. These results suggest that the availability of suitable host species may have been a key factor limiting the colonization of new hosts by fish parasites.     

Gyro-scope: an individual-based computer model to forecast gyrodactylid infections on fish hosts

Individual-based computer models (IBM) feature prominently in current theoretical ecology but have only been applied in a small number of parasitological studies. Here we designed an IBM to simulate the infection dynamics of gyrodactylid parasites and immune defence of na?ve hosts (i.e. fish previously not exposed to these parasites). We compared the results of the model with empirical data from guppies (Poecilia reticulata) infected with Gyrodactylus parasites. The laboratory experiments on guppies showed that larger fish acquired a heavier parasite load at the peak of the infection. The survival probability declined with increased body size and no fish survived a parasite load of 80 or more worms in this experiment (i.e. lethal load). The model was a good predictor of the Gyrodactylus infection dynamics of guppies and the model output was congruent with previously published data on Gyrodactylus salaris infections of salmon (Salmo salar). Computer simulations indicated that the infections persisted longer on larger hosts and that the parasite load increased exponentially with the body size of the host. Simulations furthermore predicted that the parasite load of fish with a standard length in excess of 17mm (i.e. the size of adult guppies) reached a lethal load. This suggests that in the conditions of the experiment, the immune defence of na?ve guppies can offer moderate protection against gyrodactylid infections to juveniles, but not to na?ve adult guppies. The model is a useful tool to forecast the development of gyrodactylid infections on single hosts and make predictions about optimal life history strategies of parasites.     

Random parasite encounters coupled with condition-linked immunity of hosts generate parasite aggregation

Parasite aggregation is viewed as a natural law in parasite-host ecology but is a paradox insofar as parasites should follow the Poisson distribution if hosts are encountered randomly. Much research has focused on whether parasite aggregation in or on hosts is explained by aggregation of infective parasite stages in the environment, or by heterogeneity within host samples in terms of host responses to infection (e.g., through representation of different age classes of hosts). In this paper, we argue that the typically aggregated distributions of parasites may be explained simply. We propose that aggregated distributions can be derived from parasites encountering hosts randomly, but subsequently by parasites being 'lost' from hosts based on condition-linked escape or immunity of hosts. Host condition should be a normally distributed trait even among otherwise homogeneous sets of hosts. Our model shows that mean host condition and variation in host condition have different effects on the different metrics of parasite aggregation. Our model further predicts that as host condition increases, parasites become more aggregated but numbers of attending parasites are reduced overall and this is important for parasite population dynamics. The effects of deviation from random encounter are discussed with respect to the relationship between host condition and final parasite numbers.     

Manipulation of host behaviour by parasites: a weakening paradigm?

New scientific paradigms often generate an early wave of enthusiasm among researchers and a barrage of studies seeking to validate or refute the newly proposed idea. All else being equal, the strength and direction of the empirical evidence being published should not change over time, allowing one to assess the generality of the paradigm based on the gradual accumulation of evidence. Here, I examine the relationship between the magnitude of published quantitative estimates of parasite-induced changes in host behaviour and year of publication from the time the adaptive host manipulation hypothesis was first proposed. Two independent data sets were used, both originally gathered for other purposes. First, across 137 comparisons between the behaviour of infected and uninfected hosts, the estimated relative influence of parasites correlated negatively with year of publication. This effect was contingent upon the transmission mode of the parasites studied. The negative relationship was very strong among studies of parasites which benefit from host manipulation (transmission to the next host occurs by predation on an infected intermediate host), i.e. among studies which were explicit tests of the adaptive manipulation hypothesis. There was no correlation with year of publication among studies on other types of parasites which do not seem to receive benefits from host manipulation. Second, among 14 estimates of the relative, parasite-mediated increase in transmission rate (i.e. increases in predation rates by definitive hosts on intermediate hosts), the estimated influence of parasites again correlated negatively with year of publication. These results have several possible explanations, but tend to suggest biases with regard to what results are published through time as accepted paradigms changed.     

南极鱼类后生动物寄生虫研究进展: 线虫、绦虫与桡足类

极端的环境造就了南极独特的生物群体, 其中鱼类是南大洋生态系统中最具多样性的脊椎动物, 也是许多寄生虫的中间或终末宿主。南极鱼类寄生虫种类丰富, 是南大洋海洋生物多样性的重要组成部分。探究南极鱼类及其寄生虫的营养关系可为阐释南极海洋生态系统功能及其变动提供重要的生态数据。虽然关于南极鱼类寄生虫的研究已有一百多年的历史, 但这些研究主要集中在寄生虫的种类鉴定、区系调查和组织病理等方面。由于南极鱼类寄生虫研究跨度时间长、地域范围广, 相关研究较为零散。文章综述了南极鱼类寄生线虫、绦虫以及桡足类的种类组成、宿主范围和地理分布等方面的研究, 并对今后开展南极鱼类寄生虫研究工作提出了展望。     

Host diversity drives parasite diversity: meta‐analytical insights into patterns and causal mechanisms

Statistical correlations of biodiversity patterns across multiple trophic levels have received considerable attention in various types of interacting assemblages, forging a universal understanding of patterns and processes in free‐living communities. Host–parasite interactions present an ideal model system for studying congruence of species richness among taxa as obligate parasites are strongly dependent upon the availability of their hosts for survival and reproduction while also having a tight coevolutionary relationship with their hosts. The present meta‐analysis examined 38 case studies on the relationship between species richness of hosts and parasites, and is the first attempt to provide insights into the patterns and causal mechanisms of parasite biodiversity at the community level using meta‐regression models. We tested the distinct role of resource (i.e. host) availability and evolutionary co‐variation on the association between biodiversity of hosts and parasites, while spatial scale of studies was expected to influence the extent of this association. Our results demonstrate that species richness of parasites is tightly correlated with that of their hosts with a strong average effect size (r= 0.55) through both host availability and evolutionary co‐variation. However, we found no effect of the spatial scale of studies, nor of any of the other predictor variables considered, on the correlation. Our findings highlight the tight ecological and evolutionary association between host and parasite species richness and reinforce the fact that host–parasite interactions provide an ideal system to explore congruence of biodiversity patterns across multiple trophic levels.     

The role of specialist parasites in structuring host communities

Natural enemies can be a powerful force when structuring natural communities, and in facilitating or preventing species coexistence depending on the nature of the trophic interaction. In particular, “keystone” predators can promote species coexistence, provided they preferentially attack the competitively dominant species. However, it is not clear whether parasites can play a similar structuring role; parasites typically form chronic associations with their victims, reducing their fitness (i.e., fecundity) rather than survival, and allowing infected hosts to remain viable competitors within the community. Therefore the density-dependent suppression of the host is likely to be more subtle than that due to predation. Using a series of simple population-dynamic models we show that specialist parasites can facilitate species coexistence, although possibly less so than predators. These results contrast with those typically found with models of generalist parasites, which can reduce the likelihood of species coexistence through apparent competition. In addition, we show that the likelihood of parasite-facilitated species coexistence depends greatly on the specific type of parasite. In particular, macroparasites (e.g., parasitic helminths) may be less likely to facilitate species coexistence than microparasites (e.g., viruses or bacteria) due to their typically highly aggregated distribution amongst their hosts. Furthermore, species coexistence is more likely if the parasite is relatively benign to its host. Parasitism by apparently “harmless” specialist parasites may provide an important but overlooked factor in the maintenance of species diversity, facilitating species invasions into new communities and the emergence of novel infectious diseases.     

Proximate factors affecting the larval life history of Acanthocephalus lucii (Acanthocephala)

The growth and eventual size of larval helminths in their intermediate hosts presumably has a variety of fitness consequences. Therefore, elucidating the proximate factors affecting parasite development within intermediate hosts should provide insight into the evolution of parasite life histories. An experimental infection that resulted in heavy intensities of an acanthocephalan (Acanthocephalus lucii) in its isopod intermediate host (Asellus aquaticus) permitted the examination of parasite developmental responses to variable levels of resource availability and intraspecific competition. Isopods were infected by exposure to egg-containing fish feces, and larval infrapopulations were monitored throughout the course of A. lucii development. The relative rate of parasite growth slowed over time, and indications of resource constraints on developing parasites, e.g., crowding effects, were only observed in late infections. Consequently, the factors likely representative of resource availability to larval parasites (host size and molting rate) primarily affected parasite size in late infections. Moreover, at this stage of infection, competitive interactions, gauged by variation in worm size, seemed to be alleviated by greater resources, i.e., larger hosts that molted more frequently. The relatively rapid, unconstrained growth of young parasites may be worse for host viability than the slower, resource-limited growth of larger parasites.     

Phylogenetic signals in host–parasite associations for Neotropical bats and Nearctic desert rodents

Hosts and their parasites have strong ecological and evolutionary relationships, with hosts representing habitats and resources for parasites. In the present study, we use approaches developed to evaluate the statistical dependence of species trait values on phylogenetic relationships to determine whether host–parasite relationships (i.e. parasite infections) are contingent on host phylogeny. If host–parasite relationships are contingent on the ability of hosts to provide habitat or resources to parasites, and if host phylogeny is an effective surrogate for among‐host variation in habitat and resource quality, host–parasite relationships should evince phylogenetic signals (i.e. be contingent on host phylogeny). Because the strength of ecological relationships between parasites and their hosts may affect the likelihood of phylogenetic signals occurring in host–parasite relationships, we hypothesized that (1) host specificity would be positively correlated with the strength of phylogenetic signals and (2) the strength of phylogenetic signals will be greater for parasites that rely more on their host throughout their life cycle. Analyses were conducted for ectoparasites from tropical bats and for ectoparasites, helminths, and coccidians from desert rodents. Phylogenetic signals were evaluated for parasite presence and for parasite prevalence. The frequency of phylogenetic signal occurrence was similar for parasite presence and prevalence, with a signal detected in 24–27% of cases at the species level and in 67% and 15% of cases at the genus level for parasites of bats and rodents, respectively. No differences in signal strength or the likelihood of detecting a signal existed between groups of parasites. Phylogenetic signal strength was correlated with host specificity, suggesting that mechanisms increasing host specificity also increase the likelihood of a phylogenetic signal in host use by parasites. Differences in the transmission mode did not affect signal strength or the likelihood of detecting a signal, indicating that variation in host switching opportunities associated with the transmission mode does not affect signal strength.     

Parasite diversity declines with host evolutionary distinctiveness: A global analysis of carnivores

Evolutionarily distinctive host lineages might harbor fewer parasite species because they have fewer opportunities for parasite sharing than hosts having extant close relatives, or because diverse parasite assemblages promote host diversification. We evaluate these hypotheses using data from 930 species of parasites reported to infect free‐living carnivores. We applied nonparametric richness estimators to estimate parasite diversity among well‐sampled carnivore species and assessed how well host evolutionary distinctiveness, relative to other biological and environmental factors, explained variation in estimated parasite diversity. Species richness estimates indicate that the current published literature captures less than 50% of the true parasite diversity for most carnivores. Parasite species richness declined with evolutionary distinctiveness of carnivore hosts (i.e., length of terminal ranches of the phylogeny) and increased with host species body mass and geographic range area. We found no support for the hypothesis that hosts from more diverse lineages support a higher number of generalist parasites, but we did find evidence that parasite assemblages might have driven host lineage diversification through mechanisms linked to sexual selection. Collectively, this work provides strong support for host evolutionary history being an essential predictor of parasite diversity, and offers a simple model for predicting parasite diversity in understudied carnivore species.     

Why join groups? Lessons from parasite‐manipulated Artemia

Grouping behaviours (e.g. schooling, shoaling and swarming) are commonly explicated through adaptive hypotheses such as protection against predation, access to mates or improved foraging. However, the hypothesis that aggregation can result from manipulation by parasites to increase their transmission has never been demonstrated. We investigated this hypothesis using natural populations of two crustacean hosts (Artemia franciscana and Artemia parthenogenetica) infected with one cestode and two microsporidian parasites. We found that swarming propensity increased in cestode‐infected hosts and that red colour intensity was higher in swarming compared with non‐swarming infected hosts. These effects likely result in increased cestode transmission to its final avian host. Furthermore, we found that microsporidian‐infected hosts had both increased swarming propensity and surfacing behaviour. Finally, we demonstrated using experimental infections that these concurrent manipulations result in increased spore transmission to new hosts. Hence, this study suggests that parasites can play a prominent role in host grouping behaviours.     

Correlated evolution of life history and host range in the nonphotosynthetic parasitic flowering plants Orobanche and Phelipanche (Orobanchaceae)

Most members of the nonphotosynthetic parasitic genera Orobanche and Phelipanche (Orobanchaceae) have narrow host ranges, and, as they grow on perennial hosts, are (at least potentially) perennial themselves. A few species, however, have wide host ranges and grow on annual hosts, and are thus (at least facultatively) annuals themselves. Among the latter are the weedy species, which include economically important pest taxa such as Orobanche crenata or Phelipanche aegyptiaca. Using a phylogenetically based maximum likelihood approach, which takes phylogenetic and branch length uncertainty into account, we can show that the life trait host range and life history evolve in a correlated fashion. This supports the hypothesis that parasite specialization is associated with predictable resources (i.e. long-lived hosts) and generalism with unpredictable ones (i.e. short-lived hosts), a pattern often found in animal parasites. The mechanisms and temporal sequence of the life trait changes and their interrelations remain speculative.     

Cuckoos versus hosts in insects and birds: adaptations,counter‐adaptations and outcomes

Avian parents and social insect colonies are victimized by interspecific brood parasites—cheats that procure costly care for their dependent offspring by leaving them in another species' nursery. Birds and insects defend themselves from attack by brood parasites; their defences in turn select counter‐strategies in the parasite, thus setting in motion antagonistic co‐evolution between the two parties. Despite their considerable taxonomic disparity, here we show striking parallels in the way that co‐evolution between brood parasites and their hosts proceeds in insects and birds. First, we identify five types of co‐evolutionary arms race from the empirical literature, which are common to both systems. These are: (a) directional co‐evolution of weaponry and armoury; (b) furtiveness in the parasite countered by strategies in the host to expose the parasite; (c) specialist parasites mimicking hosts who escape by diversifying their genetic signatures; (d) generalist parasites mimicking hosts who escape by favouring signatures that force specialization in the parasite; and (e) parasites using crypsis to evade recognition by hosts who then simplify their signatures to make the parasite more detectable. Arms races a and c are well characterized in the theoretical literature on co‐evolution, but the other types have received little or no formal theoretical attention. Empirical work suggests that hosts are doomed to lose arms races b and e to the parasite, in the sense that parasites typically evade host defences and successfully parasitize the nest. Nevertheless hosts may win when the co‐evolutionary trajectory follows arms race a, c or d. Next, we show that there are four common outcomes of the co‐evolutionary arms race for hosts. These are: (1) successful resistance; (2) the evolution of defence portfolios (or multiple lines of resistance); (3) acceptance of the parasite; and (4) tolerance of the parasite. The particular outcome is not determined by the type of preceding arms race but depends more on whether hosts or parasites control the co‐evolutionary trajectory: tolerance is an outcome that parasites inflict on hosts, whereas the other three outcomes are more dependent on properties intrinsic to the host species. Finally, our review highlights considerable interspecific variation in the complexity and depth of host defence portfolios. Whether this variation is adaptive or merely reflects evolutionary lag is unclear. We propose an adaptive explanation, which centres on the relative strength of two opposing processes: strategy‐facilitation, in which one line of host defence promotes the evolution of another form of resistance, and strategy‐blocking, in which one line of defence may relax selection on another so completely that it causes it to decay. We suggest that when strategy‐facilitation outweighs strategy‐blocking, hosts will possess complex defence portfolios and we identify selective conditions in which this is likely to be the case.     

Realized vs apparent reduction in enemies of the European starling

Release from parasites, pathogens or predators (i.e. enemies) is a widely cited ‘rule of thumb’ to explain the proliferation of nonindigenous species in their introduced regions (i.e. the ‘enemy release hypothesis’, or ERH). Indeed, profound effects of some parasites and predators on host populations are well documented. However, some support for the ERH comes from studies that find a reduction in the species richness of enemies in the introduced range, relative to the native range, of particular hosts. For example, data on helminth parasites of the European starling in both its native Eurasia and in North America support a reduction of parasites in the latter. However, North American ‘founder’ starlings were likely not chosen randomly from across Eurasia. This could result in an overestimation of enemy release since enemies affect their hosts on a population level. We control for the effects of subsampling colonists and find, contrary to previous reports, no evidence that introduced populations of starlings experienced a reduction in the species richness of helminth parasites after colonization of North America. These results highlight the importance of choosing appropriate contrast groups in biogeographical analyses of biological invasions to minimize the confounding effects of ‘propagule biases’.     

How parasite interaction strategies alter virulence evolution in multi‐parasite communities

The majority of organisms host multiple parasite species, each of which can interact with hosts and competitors through a diverse range of direct and indirect mechanisms. These within‐host interactions can directly alter the mortality rate of coinfected hosts and alter the evolution of virulence (parasite‐induced host mortality). Yet we still know little about how within‐host interactions affect the evolution of parasite virulence in multi‐parasite communities. Here, we modeled the virulence evolution of two coinfecting parasites in a host population in which parasites interacted through cross immunity, immune suppression, immunopathology, or spite. We show (1) that these within‐host interactions have different effects on virulence evolution when all parasites interact with each other in the same way versus when coinfecting parasites have unique interaction strategies, (2) that these interactions cause the evolution of lower virulence in some hosts, and higher virulence in other hosts, depending on the hosts infection status, and (3) that for cross immunity and spite, whether parasites increase or decrease the evolutionarily stable virulence in coinfected hosts depended on interaction strength. These results improve our understanding of virulence evolution in complex parasite communities, and show that virulence evolution must be understood at the community scale.     

A simple model of host-parasite evolutionary relationships. Parasitism: compromise or conflict?

The evolutionary biology of host-parasite relationships are considered here using a simple game-theory model in which hosts play against parasite and vice versa. In this model, the players can choose between two strategies (aggressive or not aggressive) and the utility of the game is envisaged in terms of fitness and selective costs. The game solutions suggest that the two types of confrontation are encountered in symbiotic relationships and thus constitute two Evolutionary Stable Strategies (ESS). These observations lead us to discuss: (i) the status of different kinds of symbiotic relationships (i.e. parasitoidism; parasitism, commensalism and mutualism) related to selective costs and (ii) the position of coevolution in this game theory context.