Host-parasite Interaction Networks Research Articles

A cyst-forming coccidian with large geographical range infecting forest and commensal rodents: Sarcocystis muricoelognathis sp. nov.

BackgroundThe geographic distribution and host-parasite interaction networks of Sarcocystis spp. in small mammals in eastern Asia remain incompletely known.MethodsExperimental infections, morphological and molecular characterizations were used for discrimination of a new Sarcocystis species isolated from colubrid snakes and small mammals collected in Thailand, Borneo and China.ResultsWe identified a new species, Sarcocystis muricoelognathis sp. nov., that features a relatively wide geographic distribution and infects both commensal and forest-inhabiting intermediate hosts. Sarcocystis sporocysts collected from rat snakes (Coelognathus radiatus, C. flavolineatus) in Thailand induced development of sarcocysts in experimental SD rats showing a type 10a cyst wall ultrastructure that was identical with those found in Rattus norvegicus from China and the forest rat Maxomys whiteheadi in Borneo. Its cystozoites had equal sizes in all intermediate hosts and locations, while sporocysts and cystozoites were distinct from other Sarcocystis species. Partial 28S rRNA sequences of S. muricoelognathis from M. whiteheadi were largely identical to those from R. norvegicus in China but distinct from newly sequenced Sarcocystiszuoi. The phylogeny of the nuclear 18S rRNA gene placed S. muricoelognathis within the so-called S. zuoi complex, including Sarcocystisattenuati, S. kani, S. scandentiborneensis and S. zuoi, while the latter clustered with the new species. However, the phylogeny of the ITS1-region confirmed the distinction between S. muricoelognathis and S. zuoi. Moreover, all three gene trees suggested that an isolate previously addressed as S. zuoi from Thailand (KU341120) is conspecific with S. muricoelognathis. Partial mitochondrial cox1 sequences of S. muricoelognathis were almost identical with those from other members of the group suggesting a shared, recent ancestry. Additionally, we isolated two partial 28S rRNA Sarcocystis sequences from Low’s squirrel Sundasciurus lowii that clustered with those of S. scandentiborneensis from treeshews.ConclusionsOur results provide strong evidence of broad geographic distributions of rodent-associated Sarcocystis and host shifts between commensal and forest small mammal species, even if the known host associations remain likely only snapshots of the true associations.Graphical

Bat-parasite interaction networks in urban green areas in northeastern Brazil.

Interaction networks can provide detailed information regarding ecological systems, helping us understand how communities are organized and species are connected. The goals of this study were to identify the pattern of interaction between bats and ectoparasites in urban green areas of Grande Aracaju, Sergipe, and calculate connectance, specialization, nesting, modularity and centrality metrics. Bats were captured using 10 mist nets inside and on the edges of the fragments, and the collected ectoparasites were stored in 70% alcohol. All analyses were performed using R software. The interaction network consisted of 10 species of bats and 13 ectoparasites. Connectivity was considered low (0.12). The specialization indices for ectoparasites ranged from 0.50 to 1.00, and the value obtained for the network was 0.96, which is high. The observed nesting metric was low (wNODF = 1.47), whereas the modularity was high (wQ = 0.74), indicating that the studied network had a modular topology. All centrality metrics had low values. The observed modularity may have been caused by the evolutionary history of the bats and ectoparasites involved and the high specificity index of the interactions. The low centrality values may be associated with low connectivity and a high degree of specialization. This study provides relevant information on bat–parasite interactions in an urban environment, highlighting the need for further studies to improve our understanding of host–parasite interaction networks.

Fish-parasite interaction networks reveal latitudinal and taxonomic trends in the structure of host-parasite associations.

In recent years, treating host–parasite associations as bipartite interaction networks has proven a powerful tool to identify structural patterns and their likely causes in communities of fish and their parasites. Network analysis allows for both community-level properties to be computed and investigated, and species-level roles to be determined. Here, using data from 31 host–parasite interaction networks from local fish communities around the world, we test for latitudinal trends at whole-network level, and taxonomic patterns at individual parasite species level. We found that while controlling for network size (number of species per network), network modularity, or the tendency for the network to be subdivided into groups of species that interact mostly with each other, decreased with increasing latitude. This suggests that tropical fish–parasite networks may be more stable than those from temperate regions in the event of community perturbations, such as species extinction. At the species level, after accounting for the effect of host specificity, we observed no difference in the centrality of parasite species within networks between parasites with different transmission modes. However, species in some taxa, namely branchiurans, acanthocephalans and larval trematodes, generally had higher centrality values than other parasite taxa. Because species with a central position often serve as module connectors, these 3 taxa may play a key role in whole-network cohesion. Our results highlight the usefulness of network analysis to reveal the aspects of fish–parasite community interactions that would otherwise remain hidden and advance our understanding of their evolution.

The role of ecological opportunity in shaping host-parasite networks.

Despite the great interest to quantify the structure of host-parasite interaction networks, the real influence of some factors such as taxonomy, host body size and ecological opportunity remains poorly understood. In this paper, we investigate the general patterns of organization and structure of interactions in two anuran-parasite networks in the Brazilian Pantanal (seasonally flooded environment) and Atlantic Forest (non-flooded forest). We present theoretical models to test whether the structures of these host-parasite interaction networks are influenced by neutrality, host taxonomy and host body size. Subsequently, we calculated metrics of connectance, nestedness and modularity to characterize the network structure. We demonstrated the structure networks were influenced mainly by body size and taxonomy of the host. Moreover, our results showed that the seasonally flooded environment present networks with higher connectance/nestedness and lower modularity compared to the other environment. The results also suggest that seasonal floods may promote ecological opportunities for new species associations.

Species-level drivers of mammalian ectoparasite faunas.

Traditionally, most studies have described the organization of host-parasite interaction networks by considering only few host groups at limited geographical extents. However, host-parasite relationships are merged within different taxonomic groups and factors shaping these interactions likely differ between host and parasite groups, making group-level differences important to better understand the ecological and evolutionary dynamics of these interactive communities. Here we used a dataset of 629 ectoparasite species and 251 species of terrestrial mammals, comprising 10 orders distributed across the Nearctic and Neotropical regions of Mexico to assess the species-level drivers of mammalian ectoparasite faunas. Specifically, we evaluated whether body weight, geographical range size and within-range mammal species richness (i.e. diversity field) predict mammal ectoparasite species richness (i.e. degree centrality) and their closeness centrality within the mammal-ectoparasite network. In addition, we also tested if the observed patterns differ among mammal orders and if taxonomic closely related host mammals could more likely share the same set of ectoparasites. We found that ectoparasite species richness of small mammals (mainly rodents) with large proportional range sizes was high compared to large-bodied mammals, whereas the diversity field of mammals had no predictive value (except for bats). We also observed that taxonomic proximity was a main determinant of the probability to share ectoparasite species. Specifically, the probability to share ectoparasites in congeneric species reached up to 90% and decreased exponentially as the taxonomic distance increased. Further, we also detected that some ectoparasites are generalists and capable to infect mammalian species across different orders and that rodents have a remarkable role in the network structure, being closely connected to many other taxa. Hence, because many rodent species have synanthropic habits they could act as undesired reservoirs of disease agents for humans and urban animals. Considering the reported worldwide phenomenon of the proliferation of rodents accompanying the demographic decrease or even local extinction of large-bodied mammal species, these organisms may already be an increasing health threat in many regions of the world.

Biological drivers of individual-based anuran-parasite networks under contrasting environmental conditions.

Understanding the mechanisms driving host-parasite interactions has important ecological and epidemiological implications. Traditionally, most studies dealing with host-parasite interaction networks have focused on species relationship patterns, and intra-population variation in such networks has been widely overlooked. In this study, we tested whether the composition of parasite communities of five anuran species (Leptodactylus chaquensis, Leptodactylus fuscus, Leptodactylus podicipinus, Pseudis paradoxa and Pithecopus azureus) vary across a pasture pond and a natural reserve site in south-eastern Pantanal, Brazil. We analysed the structure of individual-based networks of these five anuran species, assessed the species roles in the networks and the contribution of host species and body size to interaction strength in the networks, and tested if network ecological attributes varied between the two sites. We observed a total of 17 parasite morphospecies in 151 individual anurans and found that the abundance of parasite species tends to vary, with host species being the main filter driving parasite community structure. The composition of core parasite species remained similar between study sites, and network structure (i.e. parasite richness, interaction diversity, specialization, nestedness and modularity) did not change between pasture and natural reserve. Individual traits of hosts influenced network descriptors since larger hosts presented greater interaction strength independent of the study site. In short, we found that the occurrence of highly connected parasite taxa in both the pasture and the reserve sites may have promoted similarity in network structures, and host body size was the best predictor of associations with parasites in both study sites.

The risk of use small matrices to measure specialization in host-parasite interaction networks: a comment to Rivera-García et al. (2016).

In the last years, there were a growing number of studies using the metric H 2' to calculate complementary specialization in host-parasite interaction networks. However, only a few studies have explored the sensitivity of H 2' to network dimensions (i.e. species richness and number of interactions), which consequently could generate studies that are not comparable among them or lead to biased conclusions. In this study, we used the recent published study conducted by Rivera-García et al. in 2016 involving host-bat fly networks as an example to call attention to the risk of using H 2' to calculate specialization for small matrices. After conducting analyses based on both empirical and simulated data, we show that H 2' values are strongly affected by randomly allocation of species interactions to another cell in the matrix for small networks and that therefore the results and conclusions presented in Rivera-García et al. in 2016 are only an artefact of the dataset used. Therefore, we fully recommended taking into account the careful use of small networks to measuring specialization in host-parasite interactions.

The specificity of host-bat fly interaction networks across vegetation and seasonal variation

Vegetation type and seasonality promote changes in the species composition and abundance of parasite hosts. However, it is poorly known how these variables affect host-parasite interaction networks. This information is important to understand the dynamics of parasite-host relationships according to biotic and abiotic changes. We compared the specialization of host-bat fly interaction networks, as well as bat fly and host species composition between upland dry forest and riparian forest and between dry and rainy seasons in a tropical dry forest in Jalisco, Mexico. Bat flies were surveyed by direct collection from bats. Our results showed that host-bat fly interaction networks were more specialized in upland dry forest compared to riparian forest. Bat fly species composition was different between the dry and rainy seasons, while host species composition was different between upland dry forest and riparian forest. The higher specialization in upland dry forest could be related to the differences in bat host species composition and their respective roosting habits. Variation in the composition of bat fly species between dry and rainy seasons coincides with the seasonal shifts in their species richness. Our study confirms the high specialization of host-bat fly interactions and shows the importance of biotic and abiotic factors to understand the dynamics of parasite-host interactions.

Systems analysis of host-parasite interactions.

Parasitic diseases caused by protozoan pathogens lead to hundreds of thousands of deaths per year in addition to substantial suffering and socioeconomic decline for millions of people worldwide. The lack of effective vaccines coupled with the widespread emergence of drug‐resistant parasites necessitates that the research community take an active role in understanding host–parasite infection biology in order to develop improved therapeutics. Recent advances in next‐generation sequencing and the rapid development of publicly accessible genomic databases for many human pathogens have facilitated the application of systems biology to the study of host–parasite interactions. Over the past decade, these technologies have led to the discovery of many important biological processes governing parasitic disease. The integration and interpretation of high‐throughput ‐omic data will undoubtedly generate extraordinary insight into host–parasite interaction networks essential to navigate the intricacies of these complex systems. As systems analysis continues to build the foundation for our understanding of host–parasite biology, this will provide the framework necessary to drive drug discovery research forward and accelerate the development of new antiparasitic therapies. WIREs Syst Biol Med 2015, 7:381–400. doi: 10.1002/wsbm.1311For further resources related to this article, please visit the WIREs website.

Trophic Structure in a Seabird Host-Parasite Food Web: Insights from Stable Isotope Analyses

Ecological studies on food webs rarely include parasites, partly due to the complexity and dimensionality of host-parasite interaction networks. Multiple co-occurring parasites can show different feeding strategies and thus lead to complex and cryptic trophic relationships, which are often difficult to disentangle by traditional methods. We analyzed stable isotope ratios of C (13C/12C, δ13C) and N (15N/14N, δ15N) of host and ectoparasite tissues to investigate trophic structure in 4 co-occurring ectoparasites: three lice and one flea species, on two closely related and spatially segregated seabird hosts (Calonectris shearwaters). δ13C isotopic signatures confirmed feathers as the main food resource for the three lice species and blood for the flea species. All ectoparasite species showed a significant enrichment in δ15N relatively to the host tissue consumed (discrimination factors ranged from 2 to 5‰ depending on the species). Isotopic differences were consistent across multiple host-ectoparasite locations, despite of some geographic variability in baseline isotopic levels. Our findings illustrate the influence of both ectoparasite and host trophic ecology in the isotopic structuring of the Calonectris ectoparasite community. This study highlights the potential of stable isotope analyses in disentangling the nature and complexity of trophic relationships in symbiotic systems.

Are there general laws in parasite ecology?

As a scientific discipline matures, its theoretical underpinnings tend to consolidate around a few general laws that explain a wide range of phenomena, and from which can be derived further testable predictions. It is one of the goals of science to uncover the general principles that produce recurring patterns in nature. Although this has happened in many areas of physics and chemistry, ecology is yet to take this important step. Ecological systems are intrinsically complex, but this does not necessarily mean that everything about them is unpredictable or chaotic. Ecologists, whose grand aim is to understand the interactions that govern the distribution, abundance and diversity of living organisms at different scales, have uncovered several regular patterns, i.e. widely observable statistical tendencies, in the abundance or diversity of organisms in natural ecosystems. Some of these patterns, however, are contingent, i.e. they are only true under particular circumstances; nevertheless, the broad generality of many patterns hints at the existence of universal principles. What about parasite ecology: is it also characterized by recurring patterns and general principles? Evidence for repeatable empirical patterns in parasite ecology is reviewed here, in search of patterns that are consistently detectable across taxa or geographical areas. The coverage ranges from the population level all the way to large-scale patterns of parasite diversity and abundance (or biomass) and patterns in the structure of host-parasite interaction networks. Although general laws seem to apply to these extreme scales of studies, most patterns observed at the intermediate scale, i.e. the parasite community level, appear highly contingent and far from universal. The general laws uncovered to date are proving valuable, as they offer glimpses of the underlying processes shaping parasite ecology and diversity.

Species abundance and the distribution of specialization in host–parasite interaction networks

1 Recent studies have evaluated the distribution of specialization in species interaction networks. Species abundance patterns have been hypothesized to determine observed topological patterns. We evaluate this hypothesis in the context of host–parasite interaction networks. 2 We used two independent series of data sets, one consisting of data for seven sites describing interactions between freshwater fish and their metazoan parasites and another consisting of data for 25 localities describing interactions between fleas and their mammalian hosts. We evaluated the influence of species abundance patterns on the distribution of specialization in these host–parasite interaction networks with the aid of null models. 3 In parallel with recent studies of plant–animal mutualistic networks, our analyses suggest that host–parasite interactions in these systems are highly asymmetric: specialist parasites tend to interact with hosts with high parasite richness, whereas hosts with low parasite richness tend to interact mainly with generalist parasites. 4 The observed distribution of specialization was predicted by a null model that assumed that species-specific probabilities of being assigned a link during the randomization process were roughly proportional to their relative abundance. Thus, abundant hosts tend to harbour richer parasite faunas, with a high proportion of rare specialists.