The functional importance of parasites in animal communities: many roles at many levels?

Past research on parasites and community ecology has focussed on two distinct levels of the overall community. First, it has been shown that parasites can have a role in structuring host communities. They can have differential effects on the different hosts that they exploit, they can directly debilitate a host that itself is a key structuring force in the community, or they can indirectly alter the phenotype of their host and change the importance of the host for the community. Second, certain parasite species can be important in shaping parasite communities. Dominant parasite species can directly compete with other parasite species inside the host and reduce their abundance to some extent, and parasites that alter host phenotype can indirectly make the host more or less suitable for other parasite species. The possibility that a parasite species simultaneously affects the structure of all levels of the overall community, i.e. the parasite community and the community of free-living animals, is never considered. Given the many direct and indirect ways in which a parasite species can modulate the abundance of other species, it is conceivable that some parasite species have functionally important roles in a community, and that their removal would change the relative composition of the whole community. An example from a soft-sediment intertidal community is used to illustrate how the subtle, indirect effects of a parasite species on non-host species can be very important to the structure of the overall community. Future community studies addressing the many potential influences of parasites will no doubt identify other functionally important parasite species that serve to maintain biodiversity.     

Are there pros as well as cons to being parasitized?

The diversity of ways in which parasites reduce the fitness of their hosts has been documented during the past decades, and clearly indicates that parasites can often be considered as direct agents of selection. In natural systems, however, the outcome of a host-parasite interaction might be strongly determined by other ecological factors. Parasites can be detrimental to host fitness in one environment, whereas they can be beneficial to it in another. From an evolutionary perspective, this phenomenon is of considerable importance for understanding the dynamics of coevolution among geographically structured populations evolving under different ecological pressures. Here, Frédéric Thomas and colleagues review several ecological situations in which parasitized individuals enjoy a selective advantage over unparasitized conspecifics.     

The Repeat Region of the Circumsporozoite Protein is Critical for Sporozoite Formation and Maturation in Plasmodium

The circumsporozoite protein (CSP) is the major surface protein of the sporozoite stage of malaria parasites and has multiple functions as the parasite develops and then migrates from the mosquito midgut to the mammalian liver. The overall structure of CSP is conserved among Plasmodium species, consisting of a species-specific central tandem repeat region flanked by two conserved domains: the NH₂-terminus and the thrombospondin repeat (TSR) at the COOH-terminus. Although the central repeat region is an immunodominant B-cell epitope and the basis of the only candidate malaria vaccine in Phase III clinical trials, little is known about its functional role(s). We used the rodent malaria model Plasmodium berghei to investigate the role of the CSP tandem repeat region during sporozoite development. Here we describe two mutant parasite lines, one lacking the tandem repeat region (ΔRep) and the other lacking the NH₂-terminus as well as the repeat region (ΔNΔRep). We show that in both mutant lines oocyst formation is unaffected but sporozoite development is defective.     

Host ontogeny and the temporal decay of similarity in parasite communities of marine fish

Geographical distances between host populations are key determinants of how many parasite species they share. In principle, decay in similarity should also occur with increasing distance along any other dimension that characterizes some form of separation between communities. Here, we apply the biogeographical concept of distance decay in similarity to ontogenetic changes in the metazoan parasite communities of three species of marine fish from the Atlantic coast of South America. Using differences in body length between all possible pairs of size classes as measures of ontogenetic distances, we find that, using an index of similarity (Bray-Curtis) that takes into account the abundance of each parasite species, the similarity in parasite communities showed a very clear decay pattern; using an index (Jaccard) based on presence/absence of species only, we obtained slightly weaker but nevertheless similar patterns. As we predicted, the slope of the decay relationship was significantly steeper in the fish Cynoscion guatucupa, which goes through clear ontogenetic changes in diet and therefore in exposure to parasites, than in the other species, Engraulis anchoita and Micropogonias furnieri, which maintain a roughly similar diet throughout their lives. In addition, we found that for any given ontogenetic distance, i.e. for a given length difference between two size classes, the similarity in parasite communities was almost always higher if they were adult size classes, and almost always lower if they were juvenile size classes. This, combined with comparisons among individual fish within size classes, shows that parasite communities in juvenile fish are variable and subject to stochastic effects. We propose the distance decay approach as a rigorous and quantitative method to measure rates of community change as a function of host age, and for comparisons across host species to elucidate the role of host ecology in the development of parasite assemblages.     

Living on the edge

A report on the Second EMBL/EMBO Symposium on Functional Genomics: 'Exploring the Edges of Omics', European Molecular Biology Laboratory (EMBL), Heidelberg, Germany, 16-19 October 2004.     

Comparison of bisulfite sequencing PCR with pyrosequencing for measuring differences in DNA methylation

DNA methylation strongly affects chromatin structure and the regulation of gene expression. For many years, bisulfite sequencing PCR (BSP) has served as the “gold standard” for measuring DNA methylation. However, with the evolution of pyrosequencing as a tool to evaluate DNA methylation, the need arises to compare the relative efficiencies of the two techniques in measuring DNA methylation. We provide for the first time a direct assessment of BSP and pyrosequencing to detect and quantify hypomethylation, hypermethylation, and mixed methylation of the ABCB1 promoter in various drug-sensitive and drug-resistant MCF-7 breast cancer cell lines through head-to-head experimentation. Our findings indicate that although both methods can reliably detect increased, decreased, and mixed methylation of DNA, BSP appears to be more sensitive than pyrosequencing at detecting strong hypermethylation of DNA. However, we also observed greater variability in the methylation of CpG sites by BSP, possibly due to the additional bacterial cloning step required by BSP over pyrosequencing. BSP and pyrosequencing equally detected hypomethylation and mixed methylation of DNA. The ability of pyrosequencing to reliably detect differences in DNA methylation across cell populations without requiring the cloning of bisulfite-treated DNA into bacterial expression vectors was seen as a major advantage of this technique.     

Host–parasite interactions: a litmus test for ocean acidification?

The effects of ocean acidification (OA) on marine species and ecosystems have received significant scientific attention in the past 10 years. However, to date, the effects of OA on host-parasite interactions have been largely ignored. As parasites play a multidimensional role in the regulation of marine population, community, and ecosystem dynamics, this knowledge gap may result in an incomplete understanding of the consequences of OA. In addition, the impact of stressors associated with OA on host-parasite interactions may serve as an indicator of future changes to the biodiversity of marine systems. This opinion article discusses the potential effects of OA on host and parasite species and proposes the use of parasites as bioindicators of OA disturbance.     

Parasites in food webs: the ultimate missing links

Parasitism is the most common consumer strategy among organisms, yet only recently has there been a call for the inclusion of infectious disease agents in food webs. The value of this effort hinges on whether parasites affect food‐web properties. Increasing evidence suggests that parasites have the potential to uniquely alter food‐web topology in terms of chain length, connectance and robustness. In addition, parasites might affect food‐web stability, interaction strength and energy flow. Food‐web structure also affects infectious disease dynamics because parasites depend on the ecological networks in which they live. Empirically, incorporating parasites into food webs is straightforward. We may start with existing food webs and add parasites as nodes, or we may try to build food webs around systems for which we already have a good understanding of infectious processes. In the future, perhaps researchers will add parasites while they construct food webs. Less clear is how food‐web theory can accommodate parasites. This is a deep and central problem in theoretical biology and applied mathematics. For instance, is representing parasites with complex life cycles as a single node equivalent to representing other species with ontogenetic niche shifts as a single node? Can parasitism fit into fundamental frameworks such as the niche model? Can we integrate infectious disease models into the emerging field of dynamic food‐web modelling? Future progress will benefit from interdisciplinary collaborations between ecologists and infectious disease biologists.     

Abundance patterns and coexistence processes in communities of fleas parasitic on small mammals

The abundance of a given species in a community is likely to depend on both the total abundance and diversity of other species making up that community. A large number of co-occurring individuals or co-occurring species may decrease the abundance of any given species via diffuse competition; however, indirect interactions among many co-occurring species can have positive effects on a focal species. The existence of diffuse competition and facilitation remain difficult to demonstrate in natural communities. Here, we use data on communities of fleas ectoparasitic on small mammals from 27 distinct geographical regions to test whether the abundance of any given flea species in a community is affected by either the total abundance of all other co-occurring flea species, or the species richness and/or taxonomic diversity of the flea community. At all scales of analysis, i.e. whether we compared the same flea species on different host species, or different flea species, two consistent results emerged. First, the abundance of a given flea species correlates positively with the total abundance of all other co-occurring flea species in the community. Second, the abundance of any given flea species correlates negatively with either the species richness or taxonomic diversity of the flea community. The results do not support the existence of diffuse competition in these assemblages, because the more individuals of other flea species are present on a host population, the more individuals of the focal species are there as well. Instead, we propose explanations involving either apparent facilitation among flea species via suppression of host immune defenses, or niche filtering processes acting to restrict the taxonomic composition and abundance of flea assemblages.