skip to main content

Title: Contrasting drivers of diversity in hosts and parasites across the tropical Andes

Geographic turnover in community composition is created and maintained by eco-evolutionary forces that limit the ranges of species. One such force may be antagonistic interactions among hosts and parasites, but its general importance is unknown. Understanding the processes that underpin turnover requires distinguishing the contributions of key abiotic and biotic drivers over a range of spatial and temporal scales. Here, we address these challenges using flexible, nonlinear models to identify the factors that underlie richness (alpha diversity) and turnover (beta diversity) patterns of interacting host and parasite communities in a global biodiversity hot spot. We sampled 18 communities in the Peruvian Andes, encompassing ∼1,350 bird species and ∼400 hemosporidian parasite lineages, and spanning broad ranges of elevation, climate, primary productivity, and species richness. Turnover in both parasite and host communities was most strongly predicted by variation in precipitation, but secondary predictors differed between parasites and hosts, and between contemporary and phylogenetic timescales. Host communities shaped parasite diversity patterns, but there was little evidence for reciprocal effects. The results for parasite communities contradicted the prevailing view that biotic interactions filter communities at local scales while environmental filtering and dispersal barriers shape regional communities. Rather, subtle differences in precipitation had strong, fine-scale more » effects on parasite turnover while host–community effects only manifested at broad scales. We used these models to map bird and parasite turnover onto the ecological gradients of the Andean landscape, illustrating beta-diversity hot spots and their mechanistic underpinnings.

« less
Authors:
; ; ; ; ; ; ; ; ; ; ; ; ; ; ;
Publication Date:
NSF-PAR ID:
10217805
Journal Name:
Proceedings of the National Academy of Sciences
Volume:
118
Issue:
12
Page Range or eLocation-ID:
Article No. e2010714118
ISSN:
0027-8424
Publisher:
Proceedings of the National Academy of Sciences
Sponsoring Org:
National Science Foundation
More Like this
  1. Community composition is driven by a few key assembly processes: ecological selection, drift and dispersal. Nested parasite communities represent a powerful study system for understanding the relative importance of these processes and their relationship with biological scale. Quantifying β‐diversity across scales and over time additionally offers mechanistic insights into the ecological processes shaping the distributions of parasites and therefore infectious disease. To examine factors driving parasite community composition, we quantified the parasite communities of 959 amphibian hosts representing two species (the Pacific chorus frog, Pseudacris regilla and the California newt, Taricha torosa) sampled over 3 months from 10 ponds in California. Using additive partitioning, we estimated how much of regional parasite richness (γ‐diversity) was composed of within‐host parasite richness (α‐diversity) and turnover (β‐diversity) at three biological scales: across host individuals, across species and across habitat patches (ponds). We also examined how β‐diversity varied across time at each biological scale. Differences among ponds comprised the majority (40%) of regional parasite diversity, followed by differences among host species (23%) and among host individuals (12%). Host species supported parasite communities that were less similar than expected by null models, consistent with ecological selection, although these differences lessened through time, likely due to highmore »dispersal rates of infectious stages. Host individuals within the same population supported more similar parasite communities than expected, suggesting that host heterogeneity did not strongly impact parasite community composition and that dispersal was high at the individual host-level. Despite the small population sizes of within‐host parasite communities, drift appeared to play a minimal role in structuring community composition. Dispersal and ecological selection appear to jointly drive parasite community assembly, particularly at larger biological scales. The dispersal ability of aquatic parasites with complex life cycles differs strongly across scales, meaning that parasite communities may predictably converge at small scales where dispersal is high, but may be more stochastic and unpredictable at larger scales. Insights into assembly mechanisms within multi‐host, multi‐parasite systems provide opportunities for understanding how to mitigate the spread of infectious diseases within human and wildlife hosts.« less
  2. Understanding the role of biotic interactions in shaping natural communities is a long-standing challenge in ecology. It is particularly pertinent to parasite communities sharing the same host communities and individuals, as the interactions among parasites—both competition and facilitation—may have far-reaching implications for parasite transmission and evolution. Aggregated parasite burdens may suggest that infected host individuals are either more prone to infection, or that infection by a parasite species facilitates another, leading to a positive parasite–parasite interaction. However, parasite species may also compete for host resources, leading to the prediction that parasite–parasite associations would be generally negative, especially when parasite species infect the same host tissue, competing for both resources and space. We examine the presence and strength of parasite associations using hierarchical joint species distribution models fitted to data on resident parasite communities sampled on over 1300 small mammal individuals across 22 species and their resident parasite communities. On average, we detected more positive associations between infecting parasite species than negative, with the most negative associations occurring when two parasite species infected the same host tissue, suggesting that parasite species associations may be quantifiable from observational data. Overall, our findings suggest that parasite community prediction at the level of themore »individual host is possible, and that parasite species associations may be detectable in complex multi-species communities, generating many hypotheses concerning the effect of host community changes on parasite community composition, parasite competition within infected hosts, and the drivers of parasite community assembly and structure.« less
  3. null (Ed.)
    The likelihood an individual becomes infected depends on the community in which it is embedded. For environmentally transmitted parasites, host community composition can alter host density, the density of parasites that hosts encounter in the environment, and the dose to which hosts are subsequently exposed. While some multi-host theory incorporates some of these factors (e.g., competition among hosts), it does not currently consider the nonlinear relationships between parasite exposure dose and per-propagule infectivity (dose-infectivity relationships), between exposure dose and infected host mortality (dose-mortality relationships), and between exposure dose and parasite propagule excretion (dose-excretion relationships). This makes it difficult to predict the impact of host species on one another’s likelihood of infection. To understand the implications of these non-linear dose relationships for multi-host communities, we first performed a meta-analysis on published dose-infectivity experiments to quantify the proportion of accelerating, linear, or decelerating dose-infectivity relationships; we found that most experiments demonstrated decelerating dose-infectivity relationships. We then explored how dose-infectivity, dose-mortality, and dose-excretion relationships might alter the impact of heterospecific host density on infectious propagule density, infection prevalence, and density of a focal host using two-host, one-parasite models. We found that dose relationships either decreased the magnitude of the impact of heterospecific hostmore »density on propagule density and infection prevalence via negative feedback loops (decelerating dose-infectivity relationships, positive dose-mortality relationships, and negative dose-excretion relationships), or increased the magnitude of the impact of heterospecific host density on infection prevalence via positive feedback loops (accelerating dose-infectivity relationships and positive dose-excretion relationships). Further, positive dose-mortality relationships resulted in hosts that traditionally decrease disease (e.g. low-competence, strong competitors) increasing infection prevalence, and vice versa. Finally, we found that dose-relationships can create positive feedback loops that facilitate friendly competition (i.e., increased heterospecific density has a positive effect on focal host density because the reduction in disease outweighs the negative effects of interspecific competition). This suggests that without taking dose relationships into account, we may incorrectly predict the effect of heterospecific host interactions, and thus host community composition, on environmentally transmitted parasites.« less
  4. Abstract

    Biodiversity is changing at an accelerating rate at both local and regional scales. Beta diversity, which quantifies species turnover between these two scales, is emerging as a key driver of ecosystem function that can inform spatial conservation. Yet measuring biodiversity remains a major challenge, especially in aquatic ecosystems. Decoding environmental DNA (eDNA) left behind by organisms offers the possibility of detecting species sans direct observation, a Rosetta Stone for biodiversity. While eDNA has proven useful to illuminate diversity in aquatic ecosystems, its utility for measuring beta diversity over spatial scales small enough to be relevant to conservation purposes is poorly known. Here we tested how eDNA performs relative to underwater visual census (UVC) to evaluate beta diversity of marine communities. We paired UVC with 12S eDNA metabarcoding and used a spatially structured hierarchical sampling design to assess key spatial metrics of fish communities on temperate rocky reefs in southern California. eDNA provided a more-detailed picture of the main sources of spatial variation in both taxonomic richness and community turnover, which primarily arose due to strong species filtering within and among rocky reefs. As expected, eDNA detected more taxa at the regional scale (69 vs. 38) which accumulated quickly withmore »space and plateaued at only ~ 11 samples. Conversely, the discovery rate of new taxa was slower with no sign of saturation for UVC. Based on historical records in the region (2000–2018) we found that 6.9 times more UVC samples would be required to detect 50 taxa compared to eDNA. Our results show that eDNA metabarcoding can outperform diver counts to capture the spatial patterns in biodiversity at fine scales with less field effort and more power than traditional methods, supporting the notion that eDNA is a critical scientific tool for detecting biodiversity changes in aquatic ecosystems.

    « less
  5. Abstract Earth is rapidly losing free-living species. Is the same true for parasitic species? To reveal temporal trends in biodiversity, historical data are needed, but often such data do not exist for parasites. Here, parasite communities of the past were reconstructed by identifying parasites in fluid-preserved specimens held in natural history collections. Approximately 2500 macroparasites were counted from 109 English Sole ( Parophrys vetulus ) collected between 1930 and 2019 in the Salish Sea, Washington, USA. Alpha and beta diversity were measured to determine if and how diversity changed over time. Species richness of parasite infracommunities and community dispersion did not vary over time, but community composition of decadal component communities varied significantly over the study period. Community dissimilarity also varied: prior to the mid-20th century, parasites shifted in abundance in a seemingly stochastic manner and, after this time period, a canalization of community change was observed, where species' abundances began to shift in consistent directions. Further work is needed to elucidate potential drivers of these changes and to determine if these patterns are present in the parasite communities of other fishes of the Salish Sea.