Parasite species richness in carnivores: effects of host body mass, latitude, geographical range and population density

Aim  Comparative studies have revealed strong links between ecological factors and the number of parasite species harboured by different hosts, but studies of different taxonomic host groups have produced inconsistent results. As a step towards understanding the general patterns of parasite species richness, we present results from a new comprehensive data base of over 7000 host–parasite combinations representing 146 species of carnivores (Mammalia: Carnivora) and 980 species of parasites.
Methods  We used both phylogenetic and non-phylogenetic comparative methods while controlling for unequal sampling effort within a multivariate framework to ascertain the main determinants of parasite species richness in carnivores.
Results  We found that body mass, population density, geographical range size and distance from the equator are correlated with overall parasite species richness in fissiped carnivores. When parasites are classified by transmission mode, body mass and home range area are the main determinants of the richness of parasites spread by close contact between hosts, and population density, geographical range size and distance from the equator account for the diversity of parasites that are not dependent on close contact. For generalist parasites, population density, geographical range size and latitude are the primary predictors of parasite species richness. We found no significant ecological correlates for the richness of specialist or vector-borne parasites.
Main conclusions  Although we found that parasite species richness increases instead of decreases with distance from the equator, other comparative patterns in carnivores support previous findings in primates, suggesting that similar ecological factors operate in both these independent evolutionary lineages.     

The historical biogeography of co-evolution: emerging infectious diseases are evolutionary accidents waiting to happen

Ecological fitting refers to interspecific associations characterized by ecologically specialized, yet phylogenetically conservative, resource utilization. During periods of biotic expansion, parasites and hosts may disperse from their areas of origin. In conjunction with ecological fitting, this sets the stage for host switching without evolving novel host utilization capabilities. This is the evolutionary basis of emerging infectious diseases (EIDs). Phylogenetic analysis for comparing trees (PACT) is a method developed to delineate both general and unique historically reticulated and non‐reticulated relationships among species and geographical areas, or among parasites and their hosts. PACT is based on ‘Assumption 0’, which states that all species and all hosts in each input phylogeny must be analysed without modification, and the final analysis must be logically consistent with all input data. Assumption 0 will be violated whenever a host or area has a reticulated history with respect to its parasites or species. PACT includes a Duplication Rule, by which hosts or areas are listed for each co‐evolutionary or biogeographical event affecting them, which satisfies Assumption 0 even if there are reticulations. PACT maximizes the search for general patterns by using Ockam's Razor – duplicate only enough to satisfy Assumption 0. PACT applied to the host and geographical distributions of members of two groups of parasitic helminths infecting anthropoid primates indicates a long and continuous association with those hosts. Nonetheless, c. 30% of the host associations are due to host switching. Only one of those involves non‐primate hosts, suggesting that most were constrained by resource requirements that are phylogenetically conservative among primates (ecological fitting). In addition, most of the host switches were associated with episodes of biotic expansion, also as predicted by the ecological fitting view of EIDs.     

Relatedness and spatial proximity as determinants of host–parasite interactions in the brood parasitic Barrow's goldeneye (Bucephala islandica)

Recent studies, which have found evidence for kin-biased egg donation, have sparked interest in re-assessing the parasitic nature of conspecific brood parasitism (CBP). Since host–parasite kinship is essential for mutual benefits to arise from CBP, we explored the role of relatedness in determining the behaviour of conspecific nest parasites and their hosts in nesting female Barrow's goldeneyes ( Bucephala islandica ), a duck in which CBP is common. The results revealed that the amount of parasitism increased with host–parasite relatedness, the effect of which was independent of geographical proximity of host and parasite nests. Proximity per se was also positively associated with the amount of parasitism. Furthermore, while hosts appeared to reduce their clutch size as a response to the presence of parasitic eggs, the magnitude of host clutch reduction also tended to increase with increasing relatedness to the parasite. Hence, our results indicate that both relatedness and spatial proximity are important determinants of CBP, and that host clutch reduction may be an adaptation to nest parasitism, modulated by host–parasite relatedness. Taken together, the results provide a demonstration that relatedness influences host and parasite behaviour in Barrow's goldeneyes, resulting in kin-biased egg donation.     

Getting there and around: Host range oscillations during colonization of the Canary Islands by the parasitic nematode Spauligodon

Episodes of expansion and isolation in geographic range over space and time, during which parasites have the opportunity to expand their host range, are linked to the development of host–parasite mosaic assemblages and parasite diversification. In this study, we investigated whether island colonization events lead to host range oscillations in a taxon of host‐specific parasitic nematodes of the genus Spauligodon in the Canary Islands. We further investigated whether range oscillations also resulted in shifts in host breadth (i.e., specialization), as expected for parasites on islands. Parasite phylogeny and divergence time estimates were inferred from molecular data with Bayesian methods. Host divergence times were set as calibration priors after a priori evaluation with a global‐fit method of which individual host–parasite associations likely represent cospeciation links. Parasite colonization history was reconstructed, followed by an estimation of oscillation events and specificity level. The results indicate the presence of four Spauligodon clades in the Canary Islands, which originated from at least three different colonization events. We found evidence of host range oscillations to truly novel hosts, which in one case led to higher diversification. Contemporary host–parasite associations show strong host specificity, suggesting that changes in host breadth were limited to the shift period. Lineages with more frequent and wider taxonomic host range oscillations prior to the initial colonization event showed wider range oscillations during colonization and diversification within the archipelago. Our results suggest that a lineage's evolutionary past may be the best indicator of a parasite's potential for future range expansions.     

Understanding Host-Switching by Ecological Fitting

Despite the fact that parasites are highly specialized with respect to their hosts, empirical evidence demonstrates that host switching rather than co-speciation is the dominant factor influencing the diversification of host-parasite associations. Ecological fitting in sloppy fitness space has been proposed as a mechanism allowing ecological specialists to host-switch readily. That proposal is tested herein using an individual-based model of host switching. The model considers a parasite species exposed to multiple host resources. Through time host range expansion can occur readily without the prior evolution of novel genetic capacities. It also produces non-linear variation in the size of the fitness space. The capacity for host colonization is strongly influenced by propagule pressure early in the process and by the size of the fitness space later. The simulations suggest that co-adaptation may be initiated by the temporary loss of less fit phenotypes. Further, parasites can persist for extended periods in sub-optimal hosts, and thus may colonize distantly related hosts by a "stepping-stone" process.     

Variation in intensity of a parasitic mite (Spinturnix myoti) in relation to the reproductive cycle and immunocompetence of its bat host (Myotis myotis)

Given the intimate association in host–parasite systems, parasites are expected to initiate their own reproduction when vulnerable hosts become abundant and/or when adult hosts are less resistant. In this study, we examined the variation in the intensities of a blood-sucking mite ( Spinturnix myoti , Acarina) with respect to the reproductive cycle and immunocompetence of its host, the greater mouse-eared bat Myotis myotis . Reproductive, pregnant females were less immunocompetent and harboured more parasites than nonreproductive females, whilst, during lactation, immunocompetence was positively associated with female body mass. There was a dramatic increase in the T-cell response of gravid females with the advancement of gestation, which coincided with a diminution of individual parasite loads and a progressive switch of parasites from adults to juveniles. The latter not only harboured greater numbers of mites than adult female bats, but they also exhibited gravid parasites in higher proportions, indicating that juvenile hosts are more attractive for parasite reproduction than adult females.     

Host immunization shapes interspecific associations in trematode parasites

1. Individuals of free-living organisms are commonly infected by multiple parasite species. Under such circumstances, positive or negative associations between the species are possible because of direct or indirect interactions, details in parasite transmission ecology and host-mediated factors. One possible mechanism underlying these processes is host immunity, but its role in shaping these associations has rarely been tackled experimentally.
2. In this study, we tested the effect of host immunization on associations between trematode parasites infecting eyes of fish. We first analysed the associations between three species ( Diplostomum spathaceum , Diplostomum gasterostei and Tylodelphys clavata ) in wild hosts, roach ( Rutilus rutilus ) and perch ( Perca fluviatilis ). Second, using rainbow trout ( Oncorhynchus mykiss ) as a model fish species, we experimentally investigated how sequential immunization of the host (i.e. one parasite species infects and immunizes the host first) could affect the associations between two of the species.
3. The results indicated that most of the associations were positive in wild hosts, which supports between-individual variation in host susceptibility, rather than competitive exclusion between the parasite species. However, positive associations were more common in roach than in perch, possibly reflecting differences in ecological conditions of exposure between the host species. The experimental data showed that positive associations between two of the species were eroded by host immunization against one of the parasite species.
4. We conclude that sequential immunization of hosts has a marked effect on interspecific parasite associations and basically can determine if positive associations are detected or not. This implies that correlative results suggesting non-interactive community structure in general may be obscured by the sequence of previous parasite exposure and corresponding dynamics of host immunization.     

Are there general rules governing parasite diversity? Small mammalian hosts and gamasid mite assemblages

Parasite biodiversity varies on several scales, and in particular among different host species. Previous attempts at finding relationships between host features and the diversity of the parasite assemblages they harbour have yielded inconsistent results, suggesting strongly that any patterns might be taxon-specific. Here, we examined the potential of three host characteristics (host body mass, basal metabolic rate, and area of the geographical range) as determinants of parasite diversity in one group of ectoparasites, gamasid mites (superfamily Dermanyssoidea), using data from 63 species of small mammalian hosts. Our analyses used three measures of parasite diversity (species richness, the Shannon diversity index, and average taxonomic distinctness), and controlled for sampling effort and phylogenetic influences. Although several significant relationships were observed, they depended entirely on which diversity measure was used, or on which host taxon was investigated (insectivores vs. rodents and lagomorphs). In addition, the present results on patterns of mite diversity were not consistent with those of an earlier study involving roughly the same host taxa and the same biogeographical area, but a different group of ectoparasites, i.e. fleas. Thus, there appears to be no universal determinant of parasite diversity, and associations between host features and parasite diversity probably evolve independently in different host–parasite systems.     

Multi level ecological fitting: indirect life cycles are not a barrier to host switching and invasion

Many invasive species are able to escape from coevolved enemies and thus enjoy a competitive advantage over native species. However, during the invasion phase, non‐native species must overcome many ecological and/or physiological hurdles before they become established and spread in their new habitats. This may explain why most introduced species either fail to establish or remain as rare interstitials in their new ranges. Studies focusing on invasive species have been based on plants or animals where establishment requires the possession of preadapted traits from their native ranges that enables them to establish and spread in their new habitats. The possession of preadapted traits that facilitate the exploitation of novel resources or to colonize novel habitats is known as ‘ecological fitting’. Some species have evolved traits and life histories that reflect highly intimate associations with very specific types of habitats or niches. For these species, their phenological windows are narrow, and thus the ability to colonize non‐native habitats requires that a number of conditions need to be met in accordance with their more specialized life histories. Some of the strongest examples of more complex ecological fitting involve invasive parasites that require different animal hosts to complete their life cycles. For instance, the giant liver fluke, Fascioloides magna, is a major parasite of several species of ungulates in North America. The species exhibits a life cycle whereby newly hatched larvae must find suitable intermediate hosts (freshwater snails) and mature larvae, definitive hosts (ungulates). Intermediate and definitive host ranges of F. magna in its native range are low in number, yet this parasite has been successfully introduced into Europe where it has become a parasite of native European snails and deer. We discuss how the ability of these parasites to overcome multiple ecophysiological barriers represents an excellent example of ‘multiple‐level ecological fitting’.     

Animal migrations and parasitism: reciprocal effects within a unified framework

Migrations, i.e. the recurring, roundtrip movement of animals between distant and distinct habitats, occur among diverse metazoan taxa. Although traditionally linked to avoidance of food shortages, predators or harsh abiotic conditions, there is increasing evidence that parasites may have played a role in the evolution of migration. On the one hand, selective pressures from parasites can favour migratory strategies that allow either avoidance of infections or recovery from them. On the other hand, infected animals incur physiological costs that may limit their migratory abilities, affecting their speed, the timing of their departure or arrival, and/or their condition upon reaching their destination. During migration, reduced immunocompetence as well as exposure to different external conditions and parasite infective stages can influence infection dynamics. Here, we first explore whether parasites represent extra costs for their hosts during migration. We then review how infection dynamics and infection risk are affected by host migration, thereby considering parasites as both causes and consequences of migration. We also evaluate the comparative evidence testing the hypothesis that migratory species harbour a richer parasite fauna than their closest free-living relatives, finding general support for the hypothesis. Then we consider the implications of host migratory behaviour for parasite ecology and evolution, which have received much less attention. Parasites of migratory hosts may achieve much greater spatial dispersal than those of non-migratory hosts, expanding their geographical range, and providing more opportunities for host-switching. Exploiting migratory hosts also exerts pressures on the parasite to adapt its phenology and life-cycle duration, including the timing of major developmental, reproduction and transmission events. Natural selection may even favour parasites that manipulate their host's migratory strategy in ways that can enhance parasite transmission. Finally, we propose a simple integrated framework based on eco-evolutionary feedbacks to consider the reciprocal selection pressures acting on migratory hosts and their parasites. Host migratory strategies and parasite traits evolve in tandem, each acting on the other along two-way causal paths and feedback loops. Their likely adjustments to predicted climate change will be understood best from this coevolutionary perspective.     

Patterns of kleptoparasitism and inquilinism in social and non-social Dunatothrips on Australian Acacia

Abstract.  1. Australian Acacia thrips and their parasitic exploiters provide a novel system for analysing fundamental questions about host–parasite evolution and ecology.
2. In this study, colony collections were used to examine interactions between members of the genus Dunatothrips and the diverse assemblage of parasitic thrips that invade domiciles constructed by the host on various species of Acacia .
3.  Dunatothrips parasites adopt a range of strategies for exploiting their hosts, including lethal fighting, host eviction, and cohabitation.
4. Social Dunatothrips ( D. aneurae and D. skene ) were more frequently parasitised than non-social D. gloius , which could be related to differences in social organisation or the fact that D. gloius has shifted onto a novel host that is distantly related to other Dunatothrips ' hosts.
5. Parasitism rates of D. aneurae and D. skene domiciles were high (46% and 51% respectively), and were positively density dependent.     

Bird hosts, blood parasites and their vectors--associations uncovered by molecular analyses of blackfly blood meals

The level of host specificity of blood-sucking invertebrates may have both ecological and evolutionary implications for the parasites they are transmitting. We used blood meals from wild-caught blackflies for molecular identification of parasites and hosts to examine patterns of host specificity and how these may affect the transmission of avian blood parasites of the genus Leucocytozoon . We found that five different species of ornithophilic blackflies preferred different species of birds when taking their blood meals. Of the blackflies that contained avian blood meals, 62% were infected with Leucocytozoon parasites, consisting of 15 different parasite lineages. For the blackfly species, there was a significant association between the host width (measured as the genetic differentiation between the used hosts) and the genetic similarity of the parasites in their blood meals. The absence of similar parasite in blood meals from blackflies with different host preferences is interpreted as a result of the vector–host associations. The observed associations between blackfly species and host species are therefore likely to hinder parasites to be transmitted between different host-groups, resulting in ecologically driven associations between certain parasite lineages and hosts species.     

Parasite establishment and host extinction in model communities

Studies of host–parasite dynamics usually consider one, or at most two, host species, neglecting the possible effects of other species on the focal hosts and vice versa. To explore the interaction of community structure with host–parasite dynamics, we model the invasion of stable communities of varying size by a parasite. The communities are generated with random interaction coefficients and connectance 0.5. Each community is invaded by parasites with different values of virulence (disease-induced host mortality rate), specificity and transmission rate. The result of each invasion is determined by numerically simulating the dynamics of the community. We classify the outcomes by whether the parasite successfully establishes in the focal host population(s), and, if so, by the proportion of host and non-host species that go extinct as a result of the parasite's introduction. We discuss how the structure of the community and the interaction between hosts and other species affect several important processes of disease ecology: the density threshold for parasite invasion, extinction cascades caused by the parasite, and the frequency of extinctions of hosts and non-hosts. In our simulated communities, non-host species went extinct more frequently than hosts, suggesting the importance of the community context of disease. In some cases, the parasite's invasion induced regular population cycles in the previously stable community.     

Comparing host and parasite phylogenies: gyrodactylus flatworms jumping from goby to goby

The combination of exceptionally high species diversity, high host specificity, and a complex reproduction system raises many questions about the underlying mechanisms triggering speciation in the flatworm genus Gyrodactylus. The coevolutionary history with their goby hosts was investigated using both topology- and distance-based approaches; phylogenies were constructed of the V4 region of the 18S rRNA and the complete ITS rDNA region for the parasites, and 12S and 16S mtDNA fragments for the hosts. The overall fit between both trees was significant according to the topology-based programs (TreeMap 1.0, 2.0 beta and TreeFitter), but not according to the timed analysis in TreeMap 2.0 beta and the distance-based method (ParaFit). An absolute timing of speciation events in host and parasite ruled out the possibility of synchronous speciation for the gill parasites, favouring the distance-based result. Based on this information together with the biological background of host and parasite, the following TreeMap solution was selected. The group of gill parasites evolved from a host switch from G. arcuatus, parasitizing the three-spined stickleback onto the gobies, followed by several host-switching events among the respective goby hosts. The timing of these events is estimated to date back to the Late Pleistocene, suggesting a role for refugia-mediated mixing of parasite species. In contrast, it is suggested that co-speciation in the fin-parasites resulted in several host-associated species complexes. This illustrates that phylogenetically conserved host-switching mimics the phylogenetic signature of co-speciation, confounding topology-based programs.     

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.     

Metazoan parasite diversity of the endemic South African intertidal klipfish,Clinus superciliosus: Factors influencing parasite community composition

The current trend in marine parasitology research, particularly in South Africa, is to focus on a specific parasite taxon and not on the total parasite community of a specific fish host. However, these records do not always reveal the ecological role of parasites in ecosystems. Thus, the present study aimed to determine which factors influence the parasite community composition of the endemic southern African intertidal klipfish, Clinus superciliosus (n = 75). Metazoan parasites were sampled from four localities (two commercial harbours - west coast; and two relatively pristine localities - southeast coast) along the South African coast. A total of 75 klipfish were examined for parasites, where 30 distinct taxa, representing seven taxonomic groups were found: Acanthocephala (4 taxa), Cestoda (2 taxa), Crustacea (5 taxa), Digenea (11 taxa), Hirudinea (2 taxa), Monogenea (1 taxon) and Nematoda (5 taxa). Results indicated that the main driver of diversity was locality, with the highest diversity on the southeast coast, most likely due to higher water temperatures and upwelling compared to the west coast. The parasite community composition of the klipfish was significantly influenced by water temperature and parasite life cycle. These results emphasise the importance of parasitological surveys including all parasite taxa in hosts from multiple localities and seasons, to better comprehend their ecological role.     

Host dispersal as the driver of parasite genetic structure: a paradigm lost?

Understanding traits influencing the distribution of genetic diversity has major ecological and evolutionary implications for host–parasite interactions. The genetic structure of parasites is expected to conform to that of their hosts, because host dispersal is generally assumed to drive parasite dispersal. Here, we used a meta‐analysis to test this paradigm and determine whether traits related to host dispersal correctly predict the spatial co‐distribution of host and parasite genetic variation. We compiled data from empirical work on local adaptation and host–parasite population genetic structure from a wide range of taxonomic groups. We found that genetic differentiation was significantly lower in parasites than in hosts, suggesting that dispersal may often be higher for parasites. A significant correlation in the pairwise genetic differentiation of hosts and parasites was evident, but surprisingly weak. These results were largely explained by parasite reproductive mode, the proportion of free‐living stages in the parasite life cycle and the geographical extent of the study; variables related to host dispersal were poor predictors of genetic patterns. Our results do not dispel the paradigm that parasite population genetic structure depends on host dispersal. Rather, we highlight that alternative factors are also important in driving the co‐distribution of host and parasite genetic variation.     

Dispersal between host populations in field conditions: navigation rules in the parasitoid Venturia canescens

Abstract. 1. Dispersal is a life-history trait that can have great ecological and evolutionary consequences, however understanding of how insects disperse is limited.
2. Navigation rules of the solitary koinobiont parasitoid of the pyralid moth larvae Venturia canescens (Gravenhorst) were studied in conditions that it is likely to meet when dispersing between host populations and in the absence of cues related directly to the presence of hosts.
3. Mark–release–recapture experiments were conducted in a natural host-free habitat, and letting the animals disperse for different periods.
4. In the presence of vegetation, wasps seemed to disperse rapidly (1 h for an area of ≥ 1 ha) and capture rates were independent of both dispersal time and distance from the release point.
5. The navigation rules of V. canescens during dispersal between tree stands can be summarised as: move up- or down-wind, avoid or pass through open, sunny areas, and go for shady and dense vegetation.
6. The consequences of the navigation rules for host–parasitoid dynamics are discussed in relation to different spatial scales.     

Differential virulence in a multiple‐host parasite of bumble bees: resolving the paradox of parasite survival?

Parasite virulence determines both the impact that parasites have on their hosts and parasite fitness. While most studies of virulence have involved single-species host–parasite interactions, the majority of parasites are likely to use multiple concurrent host species. Our understanding of how this impacts on parasite epidemiology and virulence is limited. Using the bumble bee Bombus lucorum , which exists in sympatry with B. terrestris in multi-species assemblages, and their generalist micosporidian parasite Nosema bombi , we tested whether the apparent paradox of parasite maintenance due to parasite virulence in a single host, B. terrestris , could be resolved through understanding the parasite's virulence in this sympatric host species. Nosema bombi significantly impacted colony growth, individual longevity, and individual development in B. lucorum . However, these effects were different both qualitatively and quantitatively to the parasite's impact in B. terrestris . Infected colonies of B. lucorum successfully produced both male and female reproductives, and infected female reproductives were capable of successful mating. Variation in life-history across host species may explain differences in the virulence, or impact of the parasite in B. terrestris and B. lucorum , with species with shorter life-cycles being more likely to transfer the parasite from one annual generation to the next. These results suggest that to understand the virulence and epidemiology of multi-host parasites we need to examine their ecological interactions across their various host species.     

Ecological determinants of parasite acquisition by exotic fish species

Disease‐mediated threats posed by exotic species to native counterparts are not limited to introduced parasites alone, since exotic hosts frequently acquire native parasites with possible consequences for infection patterns in native hosts. Several biological and geographical factors are thought to explain both the richness of parasites in native hosts, and the invasion success of free‐living exotic species. However, the determinants of native parasite acquisition by exotic hosts remain unknown. Here, we investigated native parasite communities of exotic freshwater fish to determine which traits influence acquisition of native parasites by exotic hosts. Model selection suggested that five factors (total body length, time since introduction, phylogenetic relatedness to the native fish fauna, trophic level and native fish species richness) may be linked to native parasite acquisition by exotic fish, but 95% confidence intervals of coefficient estimates indicated these explained little of the variance in parasite richness. Based on R²‐values, weak positive relationships may exist only between the number of parasites acquired and either host size or time since introduction. Whilst our results suggest that factors influencing parasite richness in native host communities may be less important for exotic species, it seems that analyses of general ecological factors currently fail to adequately incorporate the physiological and immunological complexity of whether a given animal species will become a host for a new parasite.