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.     

Recapture of male and female dragonflies in relation to parasitism by mites, time of season, wing length and wing cell symmetry

For aquatic mites parasitic on dragonflies, completion of their life cycle depends on their being returned to appropriate water bodies by their hosts, after completion of engorgement. We examined whether differences among hosts in timing of emergence or phenotypic attributes might affect their probability of return to an emergence pond, and hence success of mites. Parasitized males and females of the dragonfly Sympetrum obtrusum (Hagen) did not differ in overall recapture rates. Females that had wing cell symmetry and emerged early were more likely to be recaptured than females that emerged later or had wing cell asymmetry, but there were no consistent relations between these variables and parasitism by mites. No such relations between wing cell asymmetry, emergence date, and recapture likelihood were found for males. Using randomization tests, we found that mean intensities of Arrenurus planus (Marshall) mites at host emergence were the same for recaptured females and females not recaptured; however, males that were recaptured had lower mean intensities of mites at emergence than males not recaptured. Further, mature females carried more mites than mature males, and the latter had fewer mites than newlyemerged males not recaptured. Biases in detachment of engorging mites do not explain the differences in parasitism between mature males and females, nor the differences in mite numbers between mature males and newly emerged males that were not recaptured. Rather, heavily parasitized males appear to disperse or die and are not recaptured, which should have implications for dispersal of mites and fitness of male hosts.     

On understanding seasonal increases in damselfly defence and resistance against ectoparasitic mites

Abstract.  1. Defence against parasites and pathogens can be essential, yet not all hosts respond similarly to parasitic challenge. Environmental conditions are thought to explain variation in host responses to parasites.
2.  Lestes forcipatus damselflies emerging later in the season have shown higher resistance to the mite, Arrenurus planus , than hosts emerging earlier. This study was undertaken to determine whether variation in environmental temperatures characteristic of early vs. late emergence times, degree or costs of mite parasitism, and/or size of newly emerged adults could explain seasonal variation in defence and resistance to ectoparasitic mites.
3. In this study damselflies from early vs. late emergence groups differed in size at emergence and mite intensity. In general, early hosts were larger and had more mites than later hosts. However only experimental temperatures experienced by damselflies at emergence influenced defence and resistance against mites and not host size or degree of parasitism.
4. More specifically, hosts from early and late emergence groups did not differ in defence and resistance when held at the same temperatures in incubators. Housing at a high temperature, indicative of later in the season, was associated with higher defence and resistance for damselflies from both early and late emergence groups.
5. These results indicate that daily temperatures in relation to emergence timing can account for seasonal increases in resistance for this temperate insect. Seasonal increases in resistance may be expected for other temperate insect–parasite associations and should have important implications for the phenology of parasites and for seasonal variation in parasite-mediated selection.     

Explaining Susceptibility and Resistance to a Multi-Host Parasite

Closely related host species are known to show variation in the level of resistance towards the same or similar parasite species, but this phenomenon is understudied. Such studies are important for understanding the ecological factors that might promote susceptibility or resistance to parasites: in particular, whether one host species is a larger target of selection for the parasite by virtue of being more abundant locally or more regionally widespread than another host species. In this study, we examined the expression of resistance by two closely related species of damselflies (Nehalennia irene and Nehalennia gracilis) against an Arrenurus water mite species. We show that the host species at each of two isolated sphagnum bogs have statistically indistinguishable levels of prevalence and intensity of infection by mite larvae. Despite having similar measures of parasitism, the regionally less represented species (N. gracilis) showed total resistance, whereas the regionally well-represented species (N. irene) was completely susceptible. Moreover, the form of resistance expressed by N. gracilis was unique, in that the oral glands of the mite were melanised. Also, this mite species was not found outside of isolated bog habitats. These results suggest that there might have been strong historical selection from this mite on the bog specialist, N. gracilis, and that this selection may have resulted in resistance evolving to fixation in a series of isolated populations.     

Water mite parasitism in damselflies during emergence: two hosts, one pattern

The infections of emerging damselfly cohorts by ectoparasitic water mites Arrenurus cuspidator were followed closely over two years in two populations. In one pond Coenagrion puella was the single host species, whereas in the second pond C. hastulatum co-occurred. The prevalences found were close to 100%. The mean daily abundance of mites ranged from I to 45 mites per host with a peak after roughly one third of the emergence period.
The water mites displayed a clumped distribution on their hosts measured by the variance/mean ratio. No differences in parasite abundance due to host sex, head width, or host species could be detected. The abundance of mites was synchronised with host's emergence patterns. This was stronger in the system with two host species. Shaw and Dobson recently showed a generalised relationship of variance/mean of parasite abundance combining data from 269 host parasite systems. The data presented here and some other water mite associations show a significant deviation from this general rule.     

The influence of parasitic water mites on the instantaneous death rate of their hosts

Summary The effect of 2 species of water mites on the instantaneous death rate of their hosts was measured on the basis of laboratory experiments. In both parasite-host association — the parasitic water mite Hydryphantes tenuabilis on the aquatic insect host Hydrometra australis and the parasitic water mite Arrenurus pseudotenuicollis on the mosquito Anopheles crucians — the effect of mite load on the instantaneous death rate of the host appeared to be linear. Also, the impact of a single parasite on the host's death rate was apparently related to the ratio of parasite to host body weight. The results of this study are in general agreement with recent theoretical investigations of the regulation of host populations by parasites.     

Parasite-host associations and life cycles of spring-living water mites (Hydrachnidia, Acari) from Luxembourg

Larval water mites are parasites of various insect species. The main aim of the present study was to analyse the host range of spring dwelling water mites. The investigation focuses on seven spring sites in Luxembourg. Some 24 water mite species were recorded either from the benthos or as parasites attached to flying insects captured in emergence traps. For 20 mite species 35 host species from four Nematocera (Diptera) families were recorded. About 80% of the host species and over 90% of the host individuals were Chironomidae, the others were Limoniidae, Dixidae and Simuliidae. For all water mite species recorded we present the observed host spectrum and/or potential hosts as well as the intensity of parasitism and the phenology of the mites. For 10 mite species the hosts were previously unknown. For another ten species the known host spectrum can be confirmed and extended. The host spectrum ranged from one host species (e.g. for Sperchon insignis) to at least 10 host species (for Sperchon thienemanni, Ljania bipapillata), but the effective host range could not be definitively estimated due to the lack of corresponding data. The hypothesised host preference of the water mites, of which most are strictly confined to spring habitats, for similarly spring-preferring hosts could not be proven. The mean intensity of parasitism was highest for Thyas palustris (10.8 larvae/host) and lowest for Sperchon insignis and Hygrobates norvegicus (1.2 larvae per host for each). The hydryphantid mite Thyas palustris occurred at maximal intensity (41 larvae per host) and the two abdominal parasites Ljania bipapillata and Arrenurus fontinalis showed higher mean intensities than the thoracic parasites did. Larval water mites parasitising chironomids did not exhibit a preference for host sex. The phenology of the larval mite species was varied, some species were only present in samples early in the year and others exclusively in the summer. Another species showed two peaks of occurrence, springtime/early summer and late summer/autumn. In conclusion, the water mite larvae in the studied springs showed differences in host spectra and phenology but there are no clear evidences in both for host partitioning. Maybe, the relative low species diversity of water mites in individual springs and the low inter-specific competition for suitable hosts in combination with the high host abundances and species richness makes springs such favourable habitats for the mites.     

Better Hosts Dive: Detachment of Ectoparasitic Water Mites (Hydrachnellae: Arrenuridae) from Damselflies (Odonata: Coenagrionidae)

Water mite larvae parasitizing damselflies must detach while the host is in a suitable reproduction habitat for both parasites and itself. They should do so during the host's oviposition. In this paper I present experimental data for the detachment rate of water mite larvae (Arrenurus cuspidator) from different host species, Coenagrion hastulatum and C. puella, in relation to the host's oviposition behavior. C. hastulatum oviposits submerged, whereas C. puella oviposits at the water surface and aggregates with conspecifics. It was found that mite larvae detach at a significantly higher ratio from hosts with submerged oviposition. Experimental tests showed that this is not a species-specific effect. It is caused mainly by the oviposition behavior. The results are discussed in the light of different oviposition systems in damselflies.     

Inferring associations among parasitic gamasid mites from census data

Within a community, the abundance of any given species depends in large part on a network of direct and indirect, positive and negative interactions with other species, including shared enemies. In communities where experimental manipulations are often impossible (e.g., parasite communities), census data can be used to evaluate the strength or frequency of positive and negative associations among species. In ectoparasite communities, competitive associations can arise because of limited space or food, but facilitative associations can also exist if one species suppresses host immune defenses. In addition, positive associations among parasites could arise merely due to shared preferences for the same host, without any interaction going on. We used census data from 28 regional surveys of gamasid mites parasitic on small mammals throughout the Palaearctic, to assess how the abundance of individual mite species is influenced by the abundance and diversity of other mite species on the same host. After controlling for several confounding variables, the abundance of individual mite species was generally positively correlated with the combined abundances of all other mite species in the community. This trend was confirmed by meta-analysis of the results obtained for separate mite species. In contrast, there were generally no consistent relationships between the abundance of individual mite species and either the species richness or taxonomic diversity of the community in which they occur. These patterns were independent of mite feeding mode. Our results indicate either that synergistic facilitative interactions among mites increase the host’s susceptibility to further attacks (e.g., via immunosuppression) and lead to different species all having increased abundance on the same host, or that certain characteristics make some host species preferred habitats for many parasite species. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Co-evolution between ectoparasites and their insect hosts: a simulation study of a damselfly–water mite interaction

1. A simulation model investigating the co‐evolution of water mites infesting their aquatic insect hosts during emergence is presented. The model is based on field and experimental studies of the ectoparasitic water mite Arrenurus cuspidator and the damselfly Coenagrion puella. 2. Three scenarios were studied: (1) Only the host was allowed to evolve timing of emergence, while the timing of the parasites' infestation opportunity was held constant. (2) Both host and parasite were allowed to evolve. (3) Only the parasite's timing was allowed to evolve, while the host was constrained completely. 3. In the first two scenarios, parasite abundances decreased in the course of evolution and reached values well below those found in the field, whereas in the third scenario, parasite abundances were maintained at a level close to that found in the field. In the second scenario (co‐evolution), the host seemed to be the leader in the evolutionary race. 4. It is concluded that water mite parasitism is capable of shaping emergence patterns in aquatic insects and, despite the same life‐cycle length for host and parasite, the parasite evolves fast enough to shape its hatching pattern to match the emergence pattern of its host.     

Red queen meets Santa Rosalia: arms races and the evolution of host specialization in organisms with parasitic lifestyles

I argue that nonequilibrium allele frequency dynamics due to coevolution can drive the evolution of specialized host races in parasites capable of host choice-for example, herbivorous insects or parasitoids. The proposed mechanism does not require genetic trade-offs in performance on different host species. It is based on the premise that the ability of the parasite to overcome the resistance of different host species is to a large degree genetically independent-that is, controlled by different loci. The intuitive rationale is that the genetic lineage of a parasite that evolves host preference becomes more consistently exposed to selection for performance on its preferred host. Such a choosy lineage can thus coevolve faster in response to evolving host defenses than a generalist lineage distributed among several host species. Given genetic variation in host preference, an initially generalist parasite population evolves toward specialized host races, each choosing one host species. This idea is supported by a series of multilocus models of coevolution between a parasite and two host species, in which the parasite virulence on each host is affected by a different set of loci and an additional locus or two loci control host choice.     

Stability in abundance and niche breadth of gamasid mites across environmental conditions, parasite identity and host pools

There is substantial variability among populations of the same species in basic features such as abundance or niche breadth, and it is unclear to what extent these are true species traits as opposed to the product of local environmental factors. In parasites, abundance and niche breadth, i.e. host specificity, show repeatability among different populations of the same species, but may also be influenced by external forces, depending on the parasite taxa studied. We tested whether the abundance and host specificity of gamasid mites parasitic on small mammals from 26 different geographic regions of the Palaearctic, are species-specific or instead determined by host identity and/or parameters of the biotic and abiotic environment. Values of abundance and host specificity (measured as the number of host species used) were significantly more similar among populations of the same mite species than among different mite species; despite also showing consistency within particular host species or regions independently of mite species identity, both abundance and the number of host species used appear to be true mite species traits. In contrast, the taxonomic distinctness of host species used by a mite showed little repeatability among populations of the same mite species, and appears mostly determined by the local pool of available host species. Within given mite species, all three variables (abundance, number of host species used, and their taxonomic distinctness) covaried to some extent with one or more environmental factors (e.g., nature of the local host assemblage, temperature, precipitation) across geographical regions, but there was no universal pattern among results from different mite species. These results are similar to those obtained earlier on other taxa, e.g. fleas, and suggest that there are general laws acting on spatial patterns of parasite abundance and host specificity.     

Differential host defense against multiple parasites in ants

Host–parasite interactions are ideal systems for the study of coevolutionary processes. Although infections with multiple parasite species are presumably common in nature, most studies focus on the interactions of a single host and a single parasite. To the best of our knowledge, we present here the first study on the dependency of parasite virulence and host resistance in a multiple parasite system. We evaluated whether the strength of host defense depends on the potential fitness cost of parasites in a system of two Southeast Asian army ant hosts and five parasitic staphylinid beetle species. The potential fitness costs of the parasites were evaluated by their predation behavior on host larvae in isolation experiments. The host defense was assessed by the ants’ aggressiveness towards parasitic beetle species in behavioral studies. We found clear differences among the beetle species in both host–parasite interactions. Particular beetle species attacked and killed the host larvae, while others did not. Importantly, the ants’ aggressiveness was significantly elevated against predatory beetle species, while non-predatory beetle species received almost no aggression. As a consequence of this defensive behavior, less costly parasites are more likely to achieve high levels of integration in the ant society. We conclude that the selection pressure on the host to evolve counter-defenses is higher for costly parasites and, thus, a hierarchical host defense strategy has evolved that depends on the parasites’ impact.     

Host phenology,geographic range size and regional occurrence explain interspecific variation in damselfly–water mite associations

In this study, we tested which host species’ characteristics explain the nature and level of parasitism for host damselfly (Coenagrionidae)–water mite (Arrenuridae) parasite associations. Prevalence and intensity of mite parasites, and mite species richness were examined in relation to geographic range size, regional occurrence, relative local abundance, phenology and body size of host damselfly species. A total of 7107 damselfly individuals were collected representing 16 species from 13 sites in southeastern Ontario and southwestern Quebec, Canada. Using comparative methods, differences in prevalence and intensity of parasitism could be predicted by a host species’ geographic range and phenology. Barcoding based on Cytochrome Oxidase I revealed 15 operational taxonomic units (OTUs) for mite species. The number of mite OTUs known to infest a given host species was explained by a host species’ regional occurrence. Our findings demonstrate the need to measure factors at several ecological scales in order to understand the breadth of evolutionary interactions with host–parasite associations and the selective ‘milieu’ for particular species of both hosts and parasites.     

Stimuli inducing detachment of larvalArrenurus danbyensis (Hydrachnidia: Arrenuridae) from adultCoquillettidia perturbans (Diptera: Culicidae)

In this study, potential cues for detachment of parasitic larvalArrenurus danbyensis Mullen mites fromCoquillettidia perturbans (Walker) mosquitoes were investigated. Contact with water did not induce a dramatic rate of dissociation. Crushing the host's abdomen was not as effective as crushing the head or thorax; although general body trauma has an effect, it is not sufficient to explain these results. Crushing the host's head following application of a ligature slowed the rate of mite detachment. We infer that haemolymph-borne cues, possibly hormones, are released by crushing the head or thorax of the host and induce rapid mite detachment. External application of Ringers solution or body fluids from mosquitoes significantly increased rate of mite detachment. It is possible that two separate mechanisms stimulate detachment of mites: external haemolymph reception signifying damage to the host and internal reception of haemolymph-borne cues associated with oviposition behavior.     

Parasitism increases offspring size in a damselfly: experimental evidence for parasite-mediated maternal effects

The effects of parasites on host fitness and the fitness effects of maternal effects are widely discussed. In this study, I conducted an experiment linking both aspects. I manipulated the ectoparasite load (Acari: Arrenurus cuspidator) of damselflies, Coenagrion puella, and found that larvae from mothers with high parasite loads were larger (assessed by head width) than larvae from mothers with low parasite loads. Furthermore, there was a negative correlation between the number of eggs laid and parasite load. Parasitized mothers thus seemed to have fewer, but probably better, offspring. The ecological significance of these parasite-mediated maternal effects remains to be tested. However, size-dependent cannibalism almost certainly has important consequences for population dynamics. Copyright 1999 The Association for the Study of Animal Behaviour.     

Racing against host's immunity defenses: a likely strategy for passive evasion of encapsulation in Asobara tabida parasitoids

The hymenopteran Asobara tabida Nees (Braconidae, Alysiinae) develops as a solitary endophagous parasite in larvae of several Drosophila species. Most A. tabida eggs possess a sticky chorion which attaches to the tissue of the host organs within a few hours following oviposition. A. tabida sticky eggs usually avoid encapsulation, though the probability of survival decreases in hosts carrying a larger number of circulating hemocytes. Here, we hypothesized that the elicitation of the encapsulation reaction may result from a race between two phenomena: the host's hemocytic reaction and the embedment of the parasitic egg within the host tissues. In order to test this hypothesis, we measured the speed of capsule formation in D. melanogaster larvae of different ages, knowing that the number of circulating hemocytes increases with the age of the larvae. Using a non-virulent A. tabida strain, the eggs of which do not attach to the host tissue, we found that the speed of capsule formation increased correlatively with the age of the D. melanogaster larva. Therefore, the hypothesis of a physiological race between host's immunity defenses and parasite's avoidance of host's defenses is strongly supported by our results. Also, A. tabida eggs which attach to the host's tissue before the attack by the hemocytes has taken place may be considered as a strategy of passive evasion from encapsulation.     

Coupling between tolerance and resistance for two related Eimeria parasite species

Resistance (host capacity to reduce parasite burden) and tolerance (host capacity to reduce impact on its health for a given parasite burden) manifest two different lines of defense. Tolerance can be independent from resistance, traded off against it, or the two can be positively correlated because of redundancy in underlying (immune) processes. We here tested whether this coupling between tolerance and resistance could differ upon infection with closely related parasite species. We tested this in experimental infections with two parasite species of the genus Eimeria. We measured proxies for resistance (the (inverse of) number of parasite transmission stages (oocysts) per gram of feces at the day of maximal shedding) and tolerance (the slope of maximum relative weight loss compared to day of infection on number of oocysts per gram of feces at the day of maximal shedding for each host strain) in four inbred mouse strains and four groups of F1 hybrids belonging to two mouse subspecies, Mus musculus domesticus and Mus musculus musculus. We found a negative correlation between resistance and tolerance against Eimeria falciformis, while the two are uncoupled against Eimeria ferrisi. We conclude that resistance and tolerance against the first parasite species might be traded off, but evolve more independently in different mouse genotypes against the latter. We argue that evolution of the host immune defenses can be studied largely irrespective of parasite isolates if resistance–tolerance coupling is absent or weak (E. ferrisi) but host–parasite coevolution is more likely observable and best studied in a system with negatively correlated tolerance and resistance (E. falciformis).     

Structure of populations and ecological nishes of ectoparasites in the parasite communities of small forest mammals

The paper reports the results of eight-year investigations on the ectoparasites of rodents and insectivores carried out in southern taiga of the Ilmen-Volkhov lowland (Novgorod Region) and Kurgolovsky reserve (Leningrad Region). Twelve species of small mammals were captured including three dominate species--bank vole Clethrionomys glareolus (2722 specimens), common shrew Sorex araneus (1658 specimens), and wood mouse Apodemus uralensis (367 specimens). Parasite community of the bank vole comprises 34 species of mites, ticks, and insects, the community of common shrew comprises 25 species, and the community of A. uralensis includes 28 species. Taxonomic diversity of the ectoparasite communities was shown to be based on the diversity of types of parasitism and ecological nishes of the host body. Permanent ectoparasites are found to be represented by 2 species of lie and 14 species of acariform mites. The group of temporary parasites includes 13 species of fleas, 10 species of gamasid mites. 3 ixodid species and 1 Trombiculidae. There is a common pool of temporary parasites of small mammals in the ecological system of taiga. Significance of different shrew and rodent species as hosts were found to be dependent on the population density in possible hosts and many other factors. Species diversity in the parasite communities of different small mammal species is dependent on the number of possible ecological nishes in the host body. Actual infill of these nishes by ectoparasites is usually lesser than potential one. Species composition of temporary parasites, their occurrence and abundance changes according to season. Interspecific competition in the temporary parasite species can decrease because of the seasonal disjunction of their population peaks. Diversification of the ecological niches of ectoparasites allow simultaneous feeding of more parasite individuals on one host, than in the case of parasitising of single species or several species with similar ecological nishes. The distribution of parasites on their hosts was also studied. The aggregative distribution has been found in ixodid larvae only, and the distribution of fleas was close to the Poisson distribution. Deviations from the aggregative distribution can be an effect of several independent factors, including limited ability of small mammals for providing numerous parasites with food. On the most part of hosts simultaneous parasitizing of no more than 1-3 individuals of each tick, mite, and flea species was registered. Excessive infestation by ectoparasites may probably be limited by effective reactions of self-purification in the mammal hosts.     

Can helminth community patterns be amplified when transferred by predation from intermediate to definitive hosts?

Helminth communities in definitive hosts are formed by the acquisition of packets of larvae arriving each time an intermediate host is consumed. It is thus possible that associations between parasite species or other aspects of community structure get transferred from intermediate to definitive hosts. Earlier computer simulations showed that associations between 2 parasite species, in particular positive associations, could be transferred up the food chain. Here, we alter some of the assumptions of previous models and generate new simulations of several ways in which source infracommunities in intermediate hosts can be transferred to target infracommunities in definitive hosts. In particular, we introduced nonrandom selection of intermediate hosts by predatory definitive hosts, to mimic the phenomenon of host manipulation by parasites; this consisted in biasing predation toward intermediate hosts harboring a certain parasite species. Overall, our results show that positive covariances between 2 parasite species can not only be transferred but can also be amplified during transmission to definitive hosts; significant covariance between parasite species can even appear in the definitive hosts when none existed in the intermediate hosts. Negative covariance was not as readily transferred to definitive hosts and amplified, in part because of properties of the presence-absence covariance index. Amplification of covariance results from intermediate host manipulation as well as from other processes taking place during transmission. These results suggest that the patterns of association between helminth species in definitive hosts cannot be taken to reflect the processes acting inside those hosts: they may simply be inherited, with amplification, from intermediate hosts.