skip to main content


Title: Taxonomic resolution affects host−parasite association model performance
Abstract Identifying the factors that structure host–parasite interactions is fundamental to understand the drivers of species distributions and to predict novel cross-species transmission events. More phylogenetically related host species tend to have more similar parasite associations, but parasite specificity may vary as a function of transmission mode, parasite taxonomy or life history. Accordingly, analyses that attempt to infer host−parasite associations using combined data on different parasite groups may perform quite differently relative to analyses on each parasite subset. In essence, are more data always better when predicting host−parasite associations, or does parasite taxonomic resolution matter? Here, we explore how taxonomic resolution affects predictive models of host−parasite associations using the London Natural History Museum's database of host–helminth interactions. Using boosted regression trees, we demonstrate that taxon-specific models (i.e. of Acanthocephalans, Nematodes and Platyhelminthes) consistently outperform full models in predicting mammal-helminth associations. At finer spatial resolutions, full and taxon-specific model performance does not vary, suggesting tradeoffs between phylogenetic and spatial scales of analysis. Although all models identify similar host and parasite covariates as important to such patterns, our results emphasize the importance of phylogenetic scale in the study of host–parasite interactions and suggest that using taxonomic subsets of data may improve predictions of parasite distributions and cross-species transmission. Predictive models of host–pathogen interactions should thus attempt to encompass the spatial resolution and phylogenetic scale desired for inference and prediction and potentially use model averaging or ensemble models to combine predictions from separately trained models.  more » « less
Award ID(s):
2021909
NSF-PAR ID:
10312495
Author(s) / Creator(s):
;
Date Published:
Journal Name:
Parasitology
Volume:
148
Issue:
5
ISSN:
0031-1820
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract

    Species invasion and redistribution, driven by climate change and other anthropogenic influences, alter global biodiversity patterns and disrupt ecosystems. As host species move, they can bring their associated parasites with them, potentially infecting resident species, or leave their parasites behind, enhancing their competitive ability in their new ranges. General rules to predict why invading hosts will retain some parasites but not others are relatively unexplored, and the potential predictors are numerous, ranging from parasite life history to host community composition.

    In this study, we focus on the parasite retention process during host invasion. We used the Global Mammal Parasite Database to identify terrestrial mammal hosts sampled for parasites in both native and non‐native ranges. We then selected predictors likely to play a role in parasite retention, such as parasite type, parasite specialism, species composition of the invaded community, and the invading host's phylogenetic or trait‐based similarity to the new community.

    We modelled parasite retention using boosted regression trees, with a suite of 25 predictors describing parasite and host community traits. We further tested the generality of our predictions by cross‐validating models on data for other hosts and invasion locations.

    Our results show that parasite retention is nonrandom and predictable across hosts and invasions. It is broadly shaped by parasite type and parasite specialism, with more specialist parasites that infect many closely related hosts more likely to be retained. This trend is pronounced across parasite types; helminths, however, show a more uniform likelihood of retention regardless of specificity.

    Overall, we see that most parasites are not retained (11% retained), meaning many invasive species may benefit from enemy release. However, species redistribution does have the potential to spread parasites, and this also has great relevance to understanding conservation implications of species invasions. We see that specialist parasites are most likely to coinvade with their hosts, which suggests that species closely related to the invasive hosts are most likely to be affected by parasite spillover.

     
    more » « less
  2. Abstract

    Geographic variation in environmental conditions as well as host traits that promote parasite transmission may impact infection rates and community assembly of vector‐transmitted parasites.

    Identifying the ecological, environmental and historical determinants of parasite distributions and diversity is therefore necessary to understand disease outbreaks under changing environments. Here, we identified the predictors and contributions of infection probability and phylogenetic diversity ofLeucocytozoon(an avian blood parasite) at site and species levels across the New World.

    To explore spatial patterns in infection probability and lineage diversity forLeucocytozoonparasites, we surveyed 69 bird communities from Alaska to Patagonia. Using phylogenetic Bayesian hierarchical models and high‐resolution satellite remote‐sensing data, we determined the relative influence of climate, landscape, geography and host phylogeny on regional parasite community assembly.

    Infection rates and parasite diversity exhibited considerable variation across regions in the Americas. In opposition to the latitudinal gradient hypothesis, both the diversity and prevalence ofLeucocytozoonparasites decreased towards the equator. Host relatedness and traits known to promote vector exposure neither predicted infection probability nor parasite diversity. Instead, the probability of a bird being infected withLeucocytozoonincreased with increasing vegetation cover (NDVI) and moisture levels (NDWI), whereas the diversity of parasite lineages decreased with increasing NDVI. Infection rates and parasite diversity also tended to be higher in cooler regions and higher latitudes.

    Whereas temperature partially constrainsLeucocytozoondiversity and infection rates, landscape features, such as vegetation cover and water body availability, play a significant role in modulating the probability of a bird being infected. This suggests that, forLeucocytozoon, the barriers to host shifting and parasite host range expansion are jointly determined by environmental filtering and landscape, but not by host phylogeny. Our results show that integrating host traits, host ancestry, bioclimatic data and microhabitat characteristics that are important for vector reproduction are imperative to understand and predict infection prevalence and diversity of vector‐transmitted parasites. Unlike other vector‐transmitted diseases, our results show thatLeucocytozoondiversity and prevalence will likely decrease with warming temperatures.

     
    more » « less
  3. Abstract

    Predation on parasites is a common interaction with multiple, concurrent outcomes. Free‐living stages of parasites can comprise a large portion of some predators' diets and may be important resources for population growth. Predation can also reduce the density of infectious agents in an ecosystem, with resultant decreases in infection rates. While predator–parasite interactions likely vary with parasite transmission strategy, few studies have examined how variation in transmission mode influences contact rates with predators and the associated changes in consumption risk.

    To understand how transmission mode mediates predator–parasite interactions, we examined associations between an oligochaete predatorChaetogaster limnaeithat lives commensally on freshwater snails and nine trematode taxa that infect snails.Chaetogasteris hypothesized to consume active (i.e. mobile), free‐living stages of trematodes that infect snails (miracidia), but not the passive infectious stages (eggs); it could thus differentially affect transmission and infection prevalence of parasites, including those with medical or veterinary importance. Alternatively, when infection does occur,Chaetogastercan consume and respond numerically to free‐living trematode stages released from infected snails (cercariae). These two processes lead to contrasting predictions about whetherChaetogasterand trematode infection of snails correlate negatively (‘protective predation’) or positively (‘predator augmentation’).

    Here, we tested how parasite transmission mode affectedChaetogaster–trematode relationships using data from 20,759 snails collected across 4 years from natural ponds in California. Based on generalized linear mixed modelling, snails with moreChaetogasterwere less likely to be infected by trematodes that rely on active transmission. Conversely, infections by trematodes with passive infectious stages were positively associated with per‐snailChaetogasterabundance.

    Our results suggest that trematode transmission mode mediates the net outcome of predation on parasites. For trematodes with active infectious stages, predatoryChaetogasterlimited the risk of snail infection and its subsequent pathology (i.e. castration). For taxa with passive infectious stages, no such protective effect was observed. Rather, infected snails were associated with higherChaetogasterabundance, likely owing to the resource subsidy provided by cercariae. These findings highlight the ecological and epidemiological importance of predation on free‐living stages while underscoring the influence of parasite life history in shaping such interactions.

     
    more » « less
  4. The scaling relationship observed between species richness and the geographical area sampled (i.e. the species-area relationship (SAR)) is a widely recognized macroecological relationship. Recently, this theory has been extended to trophic interactions, suggesting that geographical area may influence the structure of species interaction networks (i.e. network-area relationships (NARs)). Here, we use a global dataset of host–helminth parasite interactions to test existing predictions from macroecological theory. Scaling between single locations to the global host–helminth network by sequentially adding networks together, we find support that geographical area influences species richness and the number of species interactions in host–helminth networks. However, species-area slopes were larger for host species relative to their helminth parasites, counter to theoretical predictions. Lastly, host–helminth network modularity—capturing the tendency of the network to form into separate subcommunities—decreased with increasing area, also counter to theoretical predictions. Reconciling this disconnect between existing theory and observed SAR and NAR will provide insight into the spatial structuring of ecological networks, and help to refine theory to highlight the effects of network type, species distributional overlap, and the specificity of trophic interactions on NARs. 
    more » « less
  5. Bik, Holly (Ed.)
    ABSTRACT The complex network of associations between corals and their dinoflagellates (family Symbiodiniaceae) are the basis of coral reef ecosystems but are sensitive to increasing global temperatures. Coral-symbiont interactions are restricted by ecological and evolutionary determinants that constrain partner choice and influence holobiont response to environmental stress; however, little is known about how these processes shape thermal resilience of the holobiont. Here, we built a network of global coral-Symbiodiniaceae associations, mapped species traits (e.g., symbiont transmission mode and biogeography) and phylogenetic relationships of both partners onto the network, and assigned thermotolerance to both host and symbiont nodes. Using network analysis and phylogenetic comparative methods, we determined the contribution of species traits to thermal resilience of the holobiont, while accounting for evolutionary patterns among species. We found that the network shows nonrandom interactions among species, which are shaped by evolutionary history, symbiont transmission mode (horizontally transmitted [HT] or vertically transmitted [VT] corals) and biogeography. Coral phylogeny, but not Symbiodiniaceae phylogeny, symbiont transmission mode, or biogeography, was a good predictor of thermal resilience. Closely related corals have similar Symbiodiniaceae interaction patterns and bleaching susceptibilities. Nevertheless, the association patterns that explain increased host thermal resilience are not generalizable across the entire network but are instead unique to HT and VT corals. Under nonstress conditions, thermally resilient VT coral species associate with thermotolerant phylotypes and limit their number of unique symbionts and overall symbiont thermotolerance diversity, while thermally resilient HT coral species associate with a few host-specific symbiont phylotypes. IMPORTANCE Recent advances have revealed a complex network of interactions between coral and Symbiodiniaceae. Specifically, nonrandom association patterns, which are determined in part by restrictions imposed by symbiont transmission mode, increase the sensitivity of the overall network to thermal stress. However, little is known about the extent to which coral-Symbiodiniaceae network resistance to thermal stress is shaped by host and symbiont species phylogenetic relationships and host and symbiont species traits, such as symbiont transmission mode. We built a frequency-weighted global coral-Symbiodiniaceae network and used network analysis and phylogenetic comparative methods to show that evolutionary relatedness, but not transmission mode, predicts thermal resilience of the coral-Symbiodiniaceae holobiont. Consequently, thermal stress events could result in nonrandom pruning of susceptible lineages and loss of taxonomic diversity with catastrophic effects on community resilience to future events. Our results show that inclusion of the contribution of evolutionary and ecological processes will further our understanding of the fate of coral assemblages under climate change. 
    more » « less