Parasite diversity and coinfection determine pathogen infection success and host fitness

Abstract

While the importance of changes in host biodiversity for disease risk continues to gain empirical support, the influence of natural variation in parasite diversity on epidemiological outcomes remains largely overlooked. Here, we combined field infection data from 2,191 amphibian hosts representing 158 parasite assemblages with mechanistic experiments to evaluate the influence of parasite richness on both parasite transmission and host fitness. Using a guild of larval trematode parasites (six species) and an amphibian host, our experiments contrasted the effects of parasite richness vs. composition, observed vs. randomized assemblages, and additive vs. replacement designs. Consistent with the dilution effect hypothesis extended to intrahost diversity, increases in parasite richness reduced overall infection success, including infections by the most virulent parasite. However, the effects of parasite richness on host growth and survival were context dependent; pathology increased when parasites were administered additively, even when the presence of the most pathogenic species was held constant, but decreased when added species replaced or reduced virulent species, emphasizing the importance of community composition and assembly. These results were similar or stronger when community structures were weighted by their observed frequencies in nature. The field data also revealed the highly nested structure of parasite assemblages, with virulent species generally occupying basal positions, suggesting that increases in parasite richness and antagonism in nature will decrease virulent infections. Our findings emphasize the importance of parasite biodiversity and coinfection in affecting epidemiological responses and highlight the value of integrating research on biodiversity and community ecology for understanding infectious diseases.microbiome | parasite competition | emerging infectious disease | ecosystem function | amphibian decline E cological research has focused increasingly on the importance of changes in biodiversity, thereby forming a fundamental link between community and ecosystem ecology (1-4). The loss or gain of species into a community, often in association with anthropogenic activities, can have remarkable effects on productivity, carbon storage, nutrient cycling, and species invasions (5-8). More recently, this line of inquiry has been extended to explore the role of biodiversity in affecting parasite transmission (i.e., the dilution effect; ref. 9). Building from historical research on agricultural plant communities (10), a series of recent studies has reported an inverse relationship between host diversity and the risk of disease in humans, plants, birds, amphibians, and corals (9). On the basis of experimental manipulations of host diversity, common mechanisms for this relationship involve changes in susceptible host density, such that higher diversity leads to a concomitant decline in susceptible hosts, or in encounter reduction, with added species interfering with parasite transmission (11,12).Des...

Host and parasite diversity jointly control disease risk in complex communities

“…Although an increasing number of studies have reported negative correlations between host diversity and disease risk (29,38,39), the hidden effects of concurrent changes in parasite communities have rarely been explored (19,31,40). Future studies examining the biodiversity-disease relationship should focus more heavily on the relative importance of multiple components of biodiversity (and how they covary) in driving observed patterns in disease risk (41)(42)(43), including the direct and indirect effects of hosts, nonhosts (e.g., predators and competitors), parasites, as well as other microorganisms.…”

“…Increases in diversity will tend to reduce disease when high-competence host species and highvirulence parasites dominate in low-richness assemblages, with progressive decreases in disease as less-competent hosts and lower-virulence parasites are added. Although our experiments used realistic patterns of host and parasite assembly (15,19), the predictability of patterns involving host-parasite coassembly will be a key factor in determining the outcome of the diversity-disease relationship in other systems. If host communities assemble randomly with respect to competence (e.g., owing to stochastic or legacy-driven effects), for instance, but parasites assemble in order of increasing virulence, variation in parasite diversity will more sharply regulate disease risk than will host diversity.…”

“…Future studies examining the biodiversity-disease relationship should focus more heavily on the relative importance of multiple components of biodiversity (and how they covary) in driving observed patterns in disease risk (41)(42)(43), including the direct and indirect effects of hosts, nonhosts (e.g., predators and competitors), parasites, as well as other microorganisms. An important frontier in continued efforts to understand disease within complex communities will therefore involve cross-system comparisons of host-parasite combinations to determine (i) the predictability of community assembly/disassembly (ii), the relationship between species assembly order and either host competence or parasite virulence, and (iii) the degree to which parasitic and free-living communities assemble additively or substitutively (14,15,19,(44)(45)(46).…”

“…However, because we expected host diversity, parasite diversity, and parasite load to correlate in the field owing to links between colonization and diversity, we used an experimental approach first in the laboratory and then in seminatural outdoor mesocosms to decouple the unique effects of each form of diversity on infection by Ribeiroia and the total parasite community. While building upon previous efforts examining the individual effects of host and parasite richness in isolation (15,19,(27)(28)(29)(30), this study combines cross-sectional coinfection data, field-based measurements of transmission, and new experiments to explicitly examine the effects of host species richness on infection by an entire parasite assemblage, thereby mechanistically evaluating the joint effects of host and parasite diversity on disease risk.…”

“…Rather than contradicting each other, these seemingly divergent perspectives on the diversity-disease relationship emphasize differences in both terminology and ecological process. Parasite diversity is not equivalent to disease risk; given that many parasitic species cause relatively little harm to the host under normal conditions, disease risk is better equated to the abundance or prevalence of the most virulent parasites, rather than the overall richness of parasites per se (5,19). Increases in parasite diversity may even function to reduce transmission if parasites are antagonistic with one another within hosts (19)(20)(21)(22).…”