Host–parasite interactions are embedded within complex communities composed of multiple host species and a cryptic assemblage of other parasites. To date, however, surprisingly few studies have explored the joint effects of host and parasite richness on disease risk, despite growing interest in the diversity–disease relationship. Here, we combined field surveys and mechanistic experiments to test how transmission of the virulent trematode
Ribeiroia ondatrae was affected by the diversity of both amphibian hosts and coinfecting parasites. Within natural wetlands, host and parasite species richness correlated positively, consistent with theoretical predictions. Among sites that supported
Ribeiroia, however, host and parasite richness interacted to negatively affect
Ribeiroia transmission between its snail and amphibian hosts, particularly in species-poor assemblages. In laboratory and outdoor experiments designed to decouple the relative contributions of host and parasite diversity, increases in host richness decreased
Ribeiroia infection by 11–65%. Host richness also tended to decrease total infections by other parasite species (four of six instances), such that more diverse host assemblages exhibited ∼40% fewer infections overall. Importantly, parasite richness further reduced both per capita and total
Ribeiroia infection by 15–20%, possibly owing to intrahost competition among coinfecting species. These findings provide evidence that parasitic and free-living diversity jointly regulate disease risk, help to resolve apparent contradictions in the diversity–disease relationship, and emphasize the challenges of integrating research on coinfection and host heterogeneity to develop a community ecology-based approach to infectious diseases.One of the most fundamental challenges facing contemporary disease ecology involves understanding host–parasite interactions within complex communities (
1,
2). Whereas epidemiological research has historically focused on interactions between individual host and parasite species, growing evidence indicates that incorporating more realistic levels of diversity is essential for managing infectious diseases. Because most emerging parasites use or depend on multiple host species (
3,
4), understanding transmission dynamics often demands detailed information on the host community (e.g., refs.
5 and
6). Concurrently, interactions among parasites are increasingly recognized in affecting disease outcomes (
7,
8). Virtually all hosts in nature support a diverse assemblage of pathogenic and nonpathogenic microorganisms (
9), which can interact both directly (e.g., competition for space or resources) or indirectly through host immunity (
10,
11). Thus far, however, there have been few empirical efforts to unite these disparate lines of research and understand disease dynamics within multihost, multiparasite communities, in part owing to the challenges involved in understanding complex interactions operating across different scales (e.g., within and between hosts) (
12,
13).A central question, therefore, concerns how host and parasite assemblages interact to determine transmission and disease severity within ecological communities. Thus far, two divergent perspectives have emerged regarding the relationship between biodiversity and parasitism. On one hand, recent interest has focused on the dilution effect hypothesis, which posits that increases in host diversity will reduce transmission or disease risk when accompanied by declines in the overall competence of the community (e.g., refs.
14 and
15). On the other hand, increases in host diversity are also hypothesized to promote parasite diversity by enhancing colonization opportunities and supporting a wider suite of parasite life cycles (host diversity begets parasite diversity hypothesis; ref.
16), such that host diversity and parasite diversity correlate positively (
17,
18). 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–
22).Static patterns of parasite richness or species composition may also offer relatively little insight into transmission, or the capacity of a parasite to move locally between hosts (
15,
23). Thus, even if more species-rich communities support higher parasite diversity owing to greater colonization opportunities, this provides limited information about how diversity per se affects parasite transmission within the community. Indeed, if parasite diversity alters transmission of the most virulent infections, it could function to amplify or mask any host-driven dilution effects, emphasizing the importance of field and experimental studies that explicitly measure transmission dynamics. These observations raise an intriguing question: If parasite diversity increases with host diversity and higher parasite richness can function to reduce disease risk, what are the individual and combined contributions of free-living and parasitic diversity to the diversity–disease relationship? Given the ubiquity of coinfection in natural host communities and the predominant tendency of diversity–disease research to focus on field-based correlations, studies that can disentangle the magnitude and relative contributions of differing components of community diversity—both free-living and parasitic—are increasingly essential.Here, we integrated field surveys and experimental manipulations of a multihost, multiparasite system to concurrently test the effects of host and parasite richness on transmission of a virulent parasite. By linking previously collected field data on host richness from 345 wetlands in California with new information on the full macroparasite communities of 1,686 hosts, we tested the influence of amphibian host and parasite richness on realized transmission of the pathogenic trematode
Ribeiroia ondatrae, which causes mortality and malformations in amphibians (
24–
26). 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–
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.
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