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 To examine factors driving parasite community composition, we quantified the parasite communities of 959 amphibian hosts representing two species (the Pacific chorus frog, 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 high 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.
- PAR ID:
- 10457632
- Publisher / Repository:
- Wiley-Blackwell
- Date Published:
- Journal Name:
- Journal of Animal Ecology
- Volume:
- 89
- Issue:
- 6
- ISSN:
- 0021-8790
- Page Range / eLocation ID:
- p. 1532-1542
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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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 high 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.more » « less
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Abstract Metacommunity theory predicts that the relative importance of regional and local processes structuring communities will change over ecological succession. Determining effects of these processes on taxonomic and evolutionary diversity in spatially structured freshwater habitats of different successional stages may greatly improve understanding of the maintenance of diversity across temporal and spatial scales. In this study, we evaluated crayfish diversity at local and regional scales in pond metacommunities undergoing secondary succession from beaver (
Castor canadensis ) disturbance. Following theoretical predictions from metacommunity ecology of the increasing importance of local processes over succession, we hypothesised a decline in crayfish local and β diversity over succession from stronger local structuring as the older ponds may provide less suitable habitat than streams.Crayfish species and phylogenetic diversity were evaluated in beaver pond metacommunities and reference headwater streams located in three catchment regions. DNA sequences from the mitochondrial cytochrome oxidase I gene were used to assign crayfish to species for community and phylogenetic diversity tests. Local and β diversity were contrasted across beaver ponds ranging in age from 24 to 70 years and as a function of metacommunity processes.
Counter to predictions, local species diversity among streams and the successional stages of ponds categorised by age class (24–39 years; 42–57 years; 60–70 years) did not differ, but community and phylogenetic convergence occurred in the oldest pond ecosystems. Crayfish community composition differed between the youngest and oldest ponds, resulting from higher abundance in the youngest ponds and community convergence in the oldest ponds. The association between community composition and the environment was strongest in streams and decoupled with pond age. In contrast, the correlation between intraspecific haplotype composition and the environment increased over succession. Among the three metacommunities, the regional crayfish species diversity arose from a combination of the temporal and environmental drivers from beaver‐constructed ecosystems and dispersal limitation within catchments.
This study represents the first investigation of the taxonomic and phylogenetic diversity response to the successional stages of beaver pond metacommunities. The detection of differential crayfish composition and haplotype sorting to pond age suggests a role for local structuring and further indicates that future studies should acknowledge succession in shaping species diversity at local and regional scales. Dispersal limitation within catchment regions probably contributes to the evolution of crayfish species diversity in metacommunities and the overall maintenance of biodiversity.
The results support a transition in community and freshwater ecology from a recent emphasis on spatial processes towards the integration of temporal drivers to better identify regulators of taxonomic and phylogenetic diversity across scales.
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Abstract Understanding how ecology and phylogeny shape parasite communities can inform parasite control and wildlife conservation initiatives while contributing to the study of host species evolution.
We tested the relative strengths of phylogeny and ecology in driving parasite community structure in a host whose ecology diverges significantly from that of its closest phylogenetic relatives.
We characterized the gastrointestinal (GI) parasite community of wild geladas
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Oesophagostomum andTrichostrongylus ) were identified across 305 samples. This is far below the diversity reported for baboons (Papio spp.) and at the low end of the range of domestic grazers (e.g.Bos taurus ,Ovis aries ) inhabiting the same region and ecological niche.Using deep amplicon sequencing, we identified 15 amplicon sequence variants (ASVs) within the two genera, seven of which matched to
Oesophagostomum sp., seven toTrichostrongylus sp., and one toT. vitrinus .Population was an important predictor of ASV richness. Geladas in the most ecologically disturbed area of the national park exhibited approximately four times higher ASV richness than geladas at a less disturbed location within the park.
In this system, ecology was a stronger predictor of parasite community structure than was phylogeny, with geladas sharing more elements of their parasite communities with other grazers in the same area than with closely related sister taxa.
A free
Plain Language Summary can be found within the Supporting Information of this article. -
Abstract Understanding what processes drive community structure is fundamental to ecology. Many wild animals are simultaneously infected by multiple parasite species, so host–parasite communities can be valuable tools for investigating connections between community structures at multiple scales, as each host can be considered a replicate parasite community. Like free‐living communities, within‐host–parasite communities are hierarchical; ecological interactions between hosts and parasites can occur at multiple scales (e.g., host community, host population, parasite community within the host), therefore, both extrinsic and intrinsic processes can determine parasite community structure. We combine analyses of community structure and assembly at both the host population and individual scales using extensive datasets on wild wood mice (
Apodemus sylvaticus ) and their parasite community. An analysis of parasite community nestedness at the host population scale provided predictions about the order of infection at the individual scale, which were then tested using parasite community assembly data from individual hosts from the same populations. Nestedness analyses revealed parasite communities were significantly more structured than random. However, observed nestedness did not differ from null models in which parasite species abundance was kept constant. We did not find consistency between observed community structure at the host population scale and within‐host order of infection. Multi‐state Markov models of parasite community assembly showed that a host's likelihood of infection with one parasite did not consistently follow previous infection by a different parasite species, suggesting there is not a deterministic order of infection among the species we investigated in wild wood mice. Our results demonstrate that patterns at one scale (i.e., host population) do not reliably predict processes at another scale (i.e., individual host), and that neutral or stochastic processes may be driving the patterns of nestedness observed in these communities. We suggest that experimental approaches that manipulate parasite communities are needed to better link processes at multiple ecological scales. -
Abstract Hosts and parasites are embedded in communities where species richness and composition can influence disease outcomes (diversity–disease relationships). The direction and magnitude of diversity–disease relationships are influenced by variation in competence (ability to support and transmit infections) of hosts in a community. However, host susceptibility to parasites, which mediates host competence, is not static and is influenced by environmental factors, including pollutants. Despite the role that pollutants can play in augmenting host susceptibility, how pollutants influence diversity–disease dynamics is not well understood.
Using an amphibian–trematode model, we tested how NaCl influences diversity–disease dynamics. We predicted that NaCl exposure can alter relative susceptibility of host species to trematodes, leading to cascading effects on the diversity–disease relationship. To test these predictions, we exposed hosts to benign or NaCl environments and generated communities that differed in number and composition of host species. We exposed these communities to trematodes and measured disease outcomes at the community (total infections across all hosts within a community) and species levels (average number of infections per host species within a community).
Host species differed in their relative susceptibility to trematodes when exposed to NaCl. Consequently, at the community level (total infections across all hosts within a community), we only detected diversity–disease relationships (dilution effects) in communities where hosts were exposed to NaCl. At the species level, disease outcomes (average number of infections/species) and whether multi‐species communities supported lower number of infections relative to single‐species communities depended on community composition. Notably, however, as with overall community infection, diversity–disease relationships only emerged when hosts were exposed to NaCl.
Synthesis. Pollutants are ubiquitous in nature and can influence disease dynamics across a number of host–parasite systems. Here, we show that NaCl exposure can alter the relative susceptibility of host species to parasites, influencing the relationship between biodiversity and disease at both community and species levels. Collectively, our study contributes to the limited knowledge surrounding environmental mediators of host susceptibility and their influence on diversity–disease dynamics.