Native and invasive hosts play different roles in host–parasite networks

Parasites are often key players in biological invasions since they can mediate the impact of host invasions or can themselves become invasive species. However, the nature and extent of parasite-mediated invasions are often difficult to delineate. Here, we used individual-based, weighted bipartite networks to study the roles (degrees of interactions of individuals in a modular network according to their within- and among-module connections) played by native and invasive host individuals to their parasite communities. We studied two phylogenetically and ecologically close fish species, Mugil cephalus s.l. and Planiliza haematocheilus (Teleostei: Mugilidae). Planiliza haematocheilus is native to the Sea of Japan and invasive in the Sea of Azov whereas, M. cephalus s.l. is native to both seas. Based on the common evolutionary history that drives native host–parasite networks, we hypothesised that 1) native networks have higher modularity than invaded ones; and 2) invasive hosts in the invaded area play a peripheral role to structure parasite communities. We analysed the whole parasite community and subsets based on transmission strategy and host specificity of the parasite species to establish whether modularity and host roles are related to these features in the native and invaded areas. All networks were found to be modular. However, modularity tended to be higher in networks of the native area rather than those of the invaded area. Host individuals of both fish species played similar roles in the native area, whereas invasive hosts played a peripheral role in the networks of the invaded area. We propose that long-term monitoring of the roles of invasive hosts in parasite communities can be a useful proxy for estimating the maturity of the establishment of the invasive hosts in an ecosystem.     

Potential Parasite Transmission in Multi-Host Networks Based on Parasite Sharing

Epidemiological networks are commonly used to explore dynamics of parasite transmission among individuals in a population of a given host species. However, many parasites infect multiple host species, and thus multi-host networks may offer a better framework for investigating parasite dynamics. We investigated the factors that influence parasite sharing – and thus potential transmission pathways – among rodent hosts in Southeast Asia. We focused on differences between networks of a single host species and networks that involve multiple host species. In host-parasite networks, modularity (the extent to which the network is divided into subgroups of rodents that interact with similar parasites) was higher in the multi-species than in the single-species networks. This suggests that phylogeny affects patterns of parasite sharing, which was confirmed in analyses showing that it predicted affiliation of individuals to modules. We then constructed “potential transmission networks” based on the host-parasite networks, in which edges depict the similarity between a pair of individuals in the parasites they share. The centrality of individuals in these networks differed between multi- and single-species networks, with species identity and individual characteristics influencing their position in the networks. Simulations further revealed that parasite dynamics differed between multi- and single-species networks. We conclude that multi-host networks based on parasite sharing can provide new insights into the potential for transmission among hosts in an ecological community. In addition, the factors that determine the nature of parasite sharing (i.e. structure of the host-parasite network) may impact transmission patterns.     

Island and taxon effects in parasitism revisited: avian malaria in the Lesser Antilles

We identify and describe the distribution of 12 genetically distinct malaria parasite lineages over islands and hosts in four common passerine birds in the Lesser Antilles. Combined parasite prevalence demonstrates strong host effects, little or no island effect, and a significant host-times-island interaction, indicating independent outcomes of host-parasite infections among island populations of the same host species. Host- and/or island-specific parasite lineages do not explain these host-parasite associations; rather, individual lineages themselves demonstrate the same type of independent interactions. Unlike overall prevalence, individual parasite lineages show considerable geographic structure (i.e., island effects) as well as species effects indicating that parasite lineages are constrained in their ability to move between hosts and locations. Together, our results suggest an upper limit to the number of host individuals that malaria parasites, as a community, can infect. Within this limit, however, the relative frequency of the different lineages varies reflecting fine scale interactions between host and parasite populations. Patterns of host-parasite associations within this system suggest both historical co-evolution and ecologically dynamic and independent host-parasite interactions.     

Migratory behavior of birds affects their coevolutionary relationship with blood parasites

Host traits, such as migratory behavior, could facilitate the dispersal of disease-causing parasites, potentially leading to the transfer of infections both across geographic areas and between host species. There is, however, little quantitative information on whether variation in such host attributes does indeed affect the evolutionary outcome of host-parasite associations. Here, we employ Leucocytozoon blood parasites of birds, a group of parasites closely related to avian malaria, to study host-parasite coevolution in relation to host behavior using a phylogenetic comparative approach. We reconstruct the molecular phylogenies of both the hosts and parasites and use cophylogenetic tools to assess whether each host-parasite association contributes significantly to the overall congruence between the two phylogenies. We find evidence for a significant fit between host and parasite phylogenies in this system, but show that this is due only to associations between nonmigrant parasites and their hosts. We also show that migrant bird species harbor a greater genetic diversity of parasites compared with nonmigrant species. Taken together, these results suggest that the migratory habits of birds could influence their coevolutionary relationship with their parasites, and that consideration of host traits is important in predicting the outcome of coevolutionary interactions.     

Antagonistic coevolution between a bacterium and a bacteriophage

Antagonistic coevolution between hosts and parasites is believed to play a pivotal role in host and parasite population dynamics, the evolutionary maintenance of sex and the evolution of parasite virulence. Furthermore, antagonistic coevolution is believed to be responsible for rapid differentiation of both hosts and parasites between geographically structured populations. Yet empirical evidence for host-parasite antagonistic coevolution, and its impact on between-population genetic divergence, is limited. Here we demonstrate a long-term arms race between the infectivity of a viral parasite (bacteriophage; phage) and the resistance of its bacterial host. Coevolution was largely driven by directional selection, with hosts becoming resistant to a wider range of parasite genotypes and parasites infective to a wider range of host genotypes. Coevolution followed divergent trajectories between replicate communities despite establishment with isogenic bacteria and phage, and resulted in bacteria adapted to their own, compared with other, phage populations.     

Evolutionary relationships, cospeciation, and host switching in avian malaria parasites

We used phylogenetic analyses of cytochrome b sequences of malaria parasites and their avian hosts to assess the coevolutionary relationships between host and parasite lineages. Many lineages of avian malaria parasites have broad host distributions, which tend to obscure cospeciation events. The hosts of a single parasite or of closely related parasites were nonetheless most frequently recovered from members of the same host taxonomic family, more so than expected by chance. However, global assessments of the relationship between parasite and host phylogenetic trees, using Component and ParaFit, failed to detect significant cospeciation. The event-based approach employed by TreeFitter revealed significant cospeciation and duplication with certain cost assignments for these events, but host switching was consistently more prominent in matching the parasite tree to the host tree. The absence of a global cospeciation signal despite conservative host distribution most likely reflects relatively frequent acquisition of new hosts by individual parasite lineages. Understanding these processes will require a more refined species concept for malaria parasites and more extensive sampling of parasite distributions across hosts. If parasites can disperse between allopatric host populations through alternative hosts, cospeciation may not have a strong influence on the architecture of host-parasite relationships. Rather, parasite speciation may happen more often in conjunction with the acquisition of new hosts followed by divergent selection between host lineages in sympatry. Detailed studies of the phylogeographic distributions of hosts and parasites are needed to characterize these events.     

指环虫属的早期辐射及其与宿主鲤科鱼类的协同进化关系

本研究利用28SrDNAC1-D2区序列分析采自鲤科鱼类中6亚科宿主和寄生在花鲈、梅花鲈上的共17种指环虫的系统发育关系。同时,通过比较宿主鲤科鱼类与指环虫的系统发育树,检验指环虫与其宿主是否存在协同进化关系。结果表明:17种指环虫形成5个进化支(Clade),其中寄生在团头鲂(亚科)和鲢、鳙(鲢亚科)上的6种指环虫聚为一支(Clade1),而它们的宿主鱼类在系统发育分析中也表现为近缘关系;寄生在鲮鱼(野鲮亚科)上的D.quanfami(Clade5)位于系统树最基部,鲫鱼和鲤鱼(鲤亚科)的寄生指环虫处在系统树的次基部位置,而鲤亚科与野鲮亚科组成的姐妹群在宿主系统树上同样处在基部位置,寄生虫和宿主在进化上较为原始的地位得到了很好地相互印证。因而,本研究首次利用分子系统学手段分析指环虫属远缘物种间的系统关系,揭示了指环虫属与宿主鱼类之间存在协同进化关系。另外,本研究首次发现,野鲮亚科鱼类也可能是指环虫类的早期宿主,这与先前认为鲤亚科鱼类为指环虫类的祖先宿主的推测有所不同。     

Specificity of host-parasite relations between arthropods and terrestrial vertebrates

Specificity of partners in host-parasite system is one of its main characteristics. Unfortunately this term has different senses in scientific literature. In everyday practice one judges an extent of host specificity of a parasite mainly by indices of its occurrence and abundance on different host species. An occurrence of parasites in nature reflects general result of complex eco-physiological interrelationships between partners in hostparasite system. Specificity of parasites in a choice of hosts may depend on a belonging of the latter to certain taxa (phylogenetic specificity), or on biotic and abiotic factors (ecological specificity). In arthropods, the phylogentic specificity and coevolution are characteristic to a greater extent for permanent hosts (lice, Mallophaga, cheyletoid and feather mites). A coevolutionaryphylogenesis is disturbed by transfers of parasites onto new hosts, by different rates of speciation in filial lines or by an extinction of several parasite taxa. In temporary parasites different forms of ecological specificity are prevalent. A host specificity is expressed to the lesser extent in mosquitoes, horseflies and in other blood-sucking Diptera. In temporary parasites with a long-term feeding (ticks) coevolutionary sequences are relatively rare, because this parasites had to adapt not only to a life on host, but also to a lesser stable environment. In some nest-burrow bloodsuckers (fleas, gamasid mites and argasid ticks) the ecological specificity is shown no by their relations with certain host species, but by an associations with habitats occupied by hosts (burrow, nests, caves). In relation with a high dynamics of host-parasite system, a specificity of its partners is comparative and it is kept up only under specific ecological conditions.     

Climate,host phylogeny and the connectivity of host communities govern regional parasite assembly

Aim

Identifying barriers that govern parasite community assembly and parasite invasion risk is critical to understand how shifting host ranges impact disease emergence. We studied regional variation in the phylogenetic compositions of bird species and their blood parasites (Plasmodium and Haemoproteus spp.) to identify barriers that shape parasite community assembly.

Location

Australasia and Oceania.

Methods

We used a data set of parasite infections from >10,000 host individuals sampled across 29 bioregions. Hierarchical models and matrix regressions were used to assess the relative influences of interspecies (host community connectivity and local phylogenetic distinctiveness), climate and geographic barriers on parasite local distinctiveness and composition.

Results

Parasites were more locally distinct (co‐occurred with distantly related parasites) when infecting locally distinct hosts, but less distinct (co‐occurred with closely related parasites) in areas with increased host diversity and community connectivity (a proxy for parasite dispersal potential). Turnover and the phylogenetic symmetry of parasite communities were jointly driven by host turnover, climate similarity and geographic distance.

Main conclusions

Interspecies barriers linked to host phylogeny and dispersal shape parasite assembly, perhaps by limiting parasite establishment or local diversification. Infecting hosts that co‐occur with few related species decreases a parasite's likelihood of encountering related competitors, perhaps increasing invasion potential but decreasing diversification opportunity. While climate partially constrains parasite distributions, future host range expansions that spread distinct parasites and diminish barriers to host shifting will likely be key drivers of parasite invasions.     

Novel application of species richness estimators to predict the host range of parasites

Host range is a critical life history trait of parasites, influencing prevalence, virulence and ultimately determining their distributional extent. Current approaches to measure host range are sensitive to sampling effort, the number of known hosts increasing with more records. Here, we develop a novel application of results-based stopping rules to determine how many hosts should be sampled to yield stable estimates of the number of primary hosts within regions, then use species richness estimation to predict host ranges of parasites across their distributional ranges. We selected three mistletoe species (hemiparasitic plants in the Loranthaceae) to evaluate our approach: a strict host specialist (Amyema lucasii, dependent on a single host species), an intermediate species (Amyema quandang, dependent on hosts in one genus) and a generalist (Lysiana exocarpi, dependent on many genera across multiple families), comparing results from geographically-stratified surveys against known host lists derived from herbarium specimens. The results-based stopping rule (stop sampling bioregion once observed host richness exceeds 80% of the host richness predicted using the Abundance-based Coverage Estimator) worked well for most bioregions studied, being satisfied after three to six sampling plots (each representing 25 host trees) but was unreliable in those bioregions with high host richness or high proportions of rare hosts. Although generating stable predictions of host range with minimal variation among six estimators trialled, distribution-wide estimates fell well short of the number of hosts known from herbarium records. This mismatch, coupled with the discovery of nine previously unrecorded mistletoe-host combinations, further demonstrates the limited ecological relevance of simple host-parasite lists. By collecting estimates of host range of constrained completeness, our approach maximises sampling efficiency while generating comparable estimates of the number of primary hosts, with broad applicability to many host-parasite systems.     

Metazoan parasite species richness and genetic variation among freshwater fish species: cause or consequence?

The factors responsible for the maintenance of genetic variation among natural populations remain a mystery. Recent models of host-parasite co-evolution assume that parasites exert frequency-dependent selection on their hosts by favouring rare alleles that may confer resistance against infection. We tested this prediction in a comparative analysis that sought relationships between levels of genetic variation and the number of metazoan parasite species exploiting each host species. We used data on 40 species of North American freshwater fishes. After controlling for sampling effort and phylogenetic influences, we found no relationship between genetic polymorphism and parasite species richness among fish species. However, we found a marginal negative correlation between parasite species richness and heterozygosity. This result goes against the prediction that increased selective pressure by parasites should be associated with higher levels of genetic variation. Instead, it suggests that parasites may be colonising host species showing low levels of genetic variation with greater success than genetically more variable host species.     

Patterns of interactions of a large fish-parasite network in a tropical floodplain

1.?Describing and explaining the structure of species interaction networks is of paramount importance for community ecology. Yet much has to be learned about the mechanisms responsible for major patterns, such as nestedness and modularity in different kinds of systems, of which large and diverse networks are a still underrepresented and scarcely studied fraction. 2.?We assembled information on fishes and their parasites living in a large floodplain of key ecological importance for freshwater ecosystems in the Paraná River basin in South America. The resulting fish-parasite network containing 72 and 324 species of fishes and parasites, respectively, was analysed to investigate the patterns of nestedness and modularity as related to fish and parasite features. 3.?Nestedness was found in the entire network and among endoparasites, multiple-host life cycle parasites and native hosts, but not in networks of ectoparasites, single-host life cycle parasites and non-native fishes. All networks were significantly modular. Taxonomy was the major host's attribute influencing both nestedness and modularity: more closely related host species tended to be associated with more nested parasite compositions and had greater chance of belonging to the same network module. Nevertheless, host abundance had a positive relationship with nestedness when only native host species pairs of the same network module were considered for analysis. 4.?These results highlight the importance of evolutionary history of hosts in linking patterns of nestedness and formation of modules in the network. They also show that functional attributes of parasites (i.e. parasitism mode and life cycle) and origin of host populations (i.e. natives versus non-natives) are crucial to define the relative contribution of these two network properties and their dependence on other ecological factors (e.g. host abundance), with potential implications for community dynamics and stability.     

Coevolution of resource trade-offs driving species interactions in a host–parasite network: an exploratory model

Patterns of specialization asymmetry, where specialist species interact mainly with generalists while generalists interact with both generalists and specialists, are often observed in mutualistic and antagonistic bipartite ecological networks. These have been explained in terms of the relative abundance of species, using a null model that assigns links in proportion to abundance, but doubts have been raised as to whether this offers a complete explanation. In particular, host–parasite networks offer a variety of examples in which the reverse patterns are observed. We propose that the link between specificity and species richness may also be driven by the coevolution of hosts and parasites, as hosts allocate resources to optimize defense against parasites, and parasites to optimize attack on hosts. In this hypothesis, species interactions are a result of resource allocations. This novel concept, linking together many different arguments for network structures, is introduced through the adaptive dynamics of a simple ecological toy system of two hosts and two parasites. We analyze the toy model and its functionality, demonstrating that coevolution leads to specialization asymmetry in networks with closely related parasites or fast host mutation rates, but not in networks with more distantly related species. Having constructed the toy model and tested its applicability, our model can now be expanded to the full problem of a larger system.     

The coevolutionary dynamics of obligate ant social parasite systems--between prudence and antagonism

In this synthesis we apply coevolutionary models to the interactions between socially parasitic ants and their hosts. Obligate social parasite systems are ideal models for coevolution, because the close phylogenetic relationship between these parasites and their hosts results in similar evolutionary potentials, thus making mutual adaptations in a stepwise fashion especially likely to occur. The evolutionary dynamics of host-parasite interactions are influenced by a number of parameters, for example the parasite's transmission mode and rate, the genetic structure of host and parasite populations, the antagonists' migration rates, and the degree of mutual specialisation. For the three types of obligate ant social parasites, queen-tolerant and queen-intolerant inquilines and slavemakers, several of these parameters, and thus the evolutionary trajectory, are likely to differ. Because of the fundamental differences in lifestyle between these social parasite systems, coevolution should further select for different traits in the parasites and their hosts. Queen-tolerant inquilines are true parasites that exert a low selection pressure on their host, because of their rarity and the fact that they do not conduct slave raids to replenish their labour force. Due to their high degree of specialisation and the potential for vertical transmission, coevolutionary theory would predict interactions between these workerless parasites and their hosts to become even more benign over time. Queen-intolerant inquilines that kill the host queen during colony take-over are best described as parasitoids, and their reproductive success is limited by the existing worker force of the invaded host nest. These parasites should therefore evolve strategies to best exploit this fixed resource. Slavemaking ants, by contrast, act as parasites only during colony foundation, while their frequent slave raids follow a predator prey dynamic. They often exploit a number of host species at a given site, and theory predicts that their associations are best described in terms of a highly antagonistic coevolutionary arms race.     

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

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

Influence of host profitability and microenvironmental conditions on parasite specialization on a main and an alternative hosts

Parasite success depends on both host profitability and the microenvironment provided by the host, which together define host-parasite compatibility and can differ between hosts. We experimentally disentangled the effects of host profitability and microenvironmental conditions provided by nest material on the reproduction of a nest-based ectoparasite when exploiting its main and an alternative avian host species. Parasite reproductive performance was similar on both hosts when breeding in nests of their own species, suggesting no difference in host-parasite compatibility between hosts. The apparent parasite specialization could therefore result from differences in host-parasite encounter processes. However, when hosts were successful, the main host produced more young in infested nests, whereas the alternative host produced less; furthermore, host reproductive performance was higher in nests of the main host species, suggesting that this nest material alleviates parasitism cost. Therefore, our results suggest different evolutionary responses to parasites of the main and alternative hosts, with either higher tolerance or higher resistance, modulated by nest material.     

Host traits associated with species roles in parasite sharing networks

The community of host species that a parasite infects is often explained by functional traits and phylogeny, predicting that closely related hosts or those with particular traits share more parasites with other hosts. Previous research has examined parasite community similarity by regressing pairwise parasite community dissimilarity between two host species against host phylogenetic distance. However, pairwise approaches cannot target specific host species responsible for disproportionate levels of parasite sharing. To better identify why some host species contribute differentially to parasite diversity patterns, we represent parasite sharing using ecological networks consisting of host species connected by instances of shared parasitism. These networks can help identify host species and traits associated with high levels of parasite sharing that may subsequently identify important hosts for parasite maintenance and transmission within communities. We used global‐scale parasite sharing networks of ungulates, carnivores, and primates to determine if host importance – encapsulated by the network measures degree, closeness, betweenness, and eigenvector centrality – was predictable based on host traits. Our findings suggest that host centrality in parasite sharing networks is a function of host population density and range size, with range size reflecting both species geographic range and the home range of those species. In the full network, host taxonomic family became an important predictor of centrality, suggesting a role for evolutionary relationships between host and parasite species. More broadly, these findings show that trait data predict key properties of ecological networks, thus highlighting a role for species traits in understanding network assembly, stability, and structure.     

Coevolution in host-parasite systems: behavioural strategies of slave-making ants and their hosts

Recently, avian brood parasites and their hosts have emerged as model systems for the study of host-parasite coevolution. However, empirical studies of the highly analogous social parasites, which use the workers of another eusocial species to raise their own young, have never explicitly examined the dynamics of these systems from a coevolutionary perspective. Here, we demonstrate interpopulational variation in behavioural interactions between a socially parasitic slave-maker ant and its host that is consistent with the expectations of host-parasite coevolution. Parasite pressure, as inferred by the size, abundance and raiding frequency of Protomognathus americanus colonies, was highest in a New York population of the host Leptothorax longispinosus and lowest in a West Virginia population. As host-parasite coevolutionary theory would predict, we found that the slave-makers and the hosts from New York were more effective at raiding and defending against raiders, respectively, than were conspecifics from the West Virginia population. Some of these variations in efficacy were brought about by apparently simple shifts in behaviour. These results demonstrate that defence mechanisms against social parasites can evolve, and they give the first indications of the existence of a coevolutionary arms race between a social parasite and its host.     

Causal mechanisms underlying host specificity in bat ectoparasites

In parasites, host specificity may result either from restricted dispersal capacity or from fixed coevolutionary host-parasite adaptations. Knowledge of those proximal mechanisms leading to particular host specificity is fundamental to understand host-parasite interactions and potential coevolution of parasites and hosts. The relative importance of these two mechanisms was quantified through infection and cross-infection experiments using mites and bats as a model. Monospecific pools of parasitic mites (Spinturnix myoti and S. andegavinus) were subjected either to individual bats belonging to their traditional, native bat host species, or to another substitute host species within the same bat genus (Myotis). The two parasite species reacted differently to these treatments. S. myoti exhibited a clear preference for, and had a higher fitness on, its native host, Myotis myotis. In contrast, S. andegavinus showed no host choice, although its fitness was higher on its native host M. daubentoni. The causal mechanisms mediating host specificity can apparently differ within closely related host-parasite systems.