Host-associated microbial communities can influence physiological processes of macroorganisms, including contributing to infectious disease resistance. For instance, some bacteria that live on amphibian skin produce antifungal compounds that inhibit two lethal fungal pathogens, Batrachochytrium dendrobatidis (Bd) and Batrachochytrium salamandrivorans (Bsal). Therefore, differences in microbiome composition among host species or populations within a species can contribute to variation in susceptibility to Bd/Bsal. This study applies 16S rRNA sequencing to characterize the skin bacterial microbiomes of three widespread terrestrial salamander genera native to the western United States. Using a metacommunity structure analysis, we identified dispersal barriers for these influential bacteria between salamander families and localities. We also analysed the effects of habitat characteristics such as percent natural cover and temperature seasonality on the microbiome. We found that certain environmental variables may influence the skin microbial communities of some salamander genera more strongly than others. Each salamander family had a somewhat distinct community of putative anti-Bd skin bacteria, suggesting that salamanders may select for a functional assembly of cutaneous symbionts that could differ in its ability to protect these amphibians from disease. Our observations raise the need to consider host identity and environmental heterogeneity during the selection of probiotics to treat wildlife diseases.
The movement of organisms across habitat boundaries has important consequences for populations, communities, and ecosystems. However, because most species are not well adapted to all habitat types, dispersal into suboptimal habitats could induce physiological changes associated with persistence strategies that influence community assembly. For example, high rates of cross‐boundary dispersal are thought to maintain sink populations of terrestrial bacteria in aquatic habitats, but these bacteria may also persist by lowering their metabolic activity, introducing metabolic heterogeneity that buffers the population against species sorting. To differentiate between these assembly processes, we analyzed bacterial composition along a hydrological flow path from terrestrial soils through an aquatic reservoir by sequencing the active and total (active + inactive) portions of the community. When metabolic heterogeneity was ignored, our data were consistent with views that cross‐boundary dispersal is important for structuring aquatic bacterial communities. In contrast, we found evidence for strong species sorting in the active portion of the aquatic community, suggesting that dispersal may have a weaker effect than persistence strategies on aquatic community assembly. By accounting for metabolic heterogeneity in complex communities, our findings clarify the roles of local‐ and regional‐scale assembly processes in terrestrial‐aquatic meta‐ecosystems.
more » « less- NSF-PAR ID:
- 10456289
- Publisher / Repository:
- Wiley Blackwell (John Wiley & Sons)
- Date Published:
- Journal Name:
- Ecology
- Volume:
- 101
- Issue:
- 4
- ISSN:
- 0012-9658
- 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 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 howβ ‐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.
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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.
