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Low-load pathogen spillover predicts shifts in skin microbiome and survival of a terrestrial-breeding amphibian.

ABSTRACT: Wildlife disease dynamics are strongly influenced by the structure of host communities and their symbiotic microbiota. Conspicuous amphibian declines associated with the waterborne fungal pathogen Batrachochytrium dendrobatidis (Bd) have been observed in aquatic-breeding frogs globally. However, less attention has been given to cryptic terrestrial-breeding amphibians that have also been declining in tropical regions. By experimentally manipulating multiple tropical amphibian assemblages harbouring natural microbial communities, we tested whether Bd spillover from naturally infected aquatic-breeding frogs could lead to Bd amplification and mortality in our focal terrestrial-breeding host: the pumpkin toadlet Brachycephalus pitanga. We also tested whether the strength of spillover could vary depending on skin bacterial transmission within host assemblages. Terrestrial-breeding toadlets acquired lethal spillover infections from neighbouring aquatic hosts and experienced dramatic but generally non-protective shifts in skin bacterial composition primarily attributable to their Bd infections. By contrast, aquatic-breeding amphibians maintained mild Bd infections and higher survival, with shifts in bacterial microbiomes that were unrelated to Bd infections. Our results indicate that Bd spillover from even mildly infected aquatic-breeding hosts may lead to dysbiosis and mortality in terrestrial-breeding species, underscoring the need to further investigate recent population declines of terrestrial-breeding amphibians in the tropics.

SUBMITTER: Becker CG

PROVIDER: S-EPMC6710587 | biostudies-literature | 2019 Aug

REPOSITORIES: biostudies-literature

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Low-load pathogen spillover predicts shifts in skin microbiome and survival of a terrestrial-breeding amphibian.

Becker C Guilherme CG Bletz Molly C MC Greenspan Sasha E SE Rodriguez David D Lambertini Carolina C Jenkinson Thomas S TS Guimarães Paulo R PR Assis Ana Paula A APA Geffers Robert R Jarek Michael M Toledo Luís Felipe LF Vences Miguel M Haddad Célio F B CFB

Proceedings. Biological sciences 20190814 1908

Wildlife disease dynamics are strongly influenced by the structure of host communities and their symbiotic microbiota. Conspicuous amphibian declines associated with the waterborne fungal pathogen Batrachochytrium dendrobatidis (Bd) have been observed in aquatic-breeding frogs globally. However, less attention has been given to cryptic terrestrial-breeding amphibians that have also been declining in tropical regions. By experimentally manipulating multiple tropical amphibian assemblages harbouri ...[more]

PMID: 31409249

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Project description:Symbiotic microbial communities play key roles in the health and development of their multicellular hosts. Understanding why microbial communities vary among different host species or individuals is an important step toward understanding the diversity and function of the microbiome. The amphibian skin microbiome may affect resistance to the fungal pathogen Batrachochytrium dendrobatidis (Bd). Still, the factors that determine the diversity and composition of the amphibian skin microbiome, and therefore may ultimately contribute to disease resistance, are not well understood. We conducted a two-phase experiment to first test how host and environment shape the amphibian skin microbiome, and then test if the microbiome affects or is affected by Bd infection. Most lab experiments testing assembly of the amphibian skin microbiome so far have compared sterile to non-sterile environments or heavily augmented to non-augmented frogs. A goal of this study was to evaluate, in an experimental setting, realistic potential drivers of microbiome assembly that would be relevant to patterns observed in nature. We tested effects of frog genetic background (2 source populations) and 6 natural lake water sources in shaping the microbiome of the frog Rana sierrae. Water in which frogs were housed affected the microbiome in a manner that partially mimicked patterns observed in natural populations. In particular, frogs housed in water from disease-resistant populations had greater bacterial richness than frogs housed in water from populations that died out due to Bd. However, in the experiment this difference in microbiomes did not lead to differences in host mortality or rates of pathogen load increase. Frog source population also affected the microbiome and, although none of the frogs in this study showed true resistance to infection, host source population had a small effect on the rate of pathogen load increase. This difference in infection trajectories could be due to the observed differences in the microbiome, but could also be due to other traits that differ between frogs from the two populations. In addition to examining effects of the microbiome on Bd, we tested the effect of Bd infection severity on the microbiome. Specifically, we studied a time series of the microbiome over the course of infection to test if the effects of Bd on the microbiome are dependent on Bd infection severity. Although limited to a small subset of frogs, time series analysis suggested that relative abundances of several bacterial phylotypes changed as Bd loads increased through time, indicating that Bd-induced disturbance of the R. sierrae microbiome is not a binary effect but instead is dependent on infection severity. We conclude that both host and aquatic environment help shape the R. sierrae skin microbiome, with links to small changes in disease resistance in some cases, but in this study the effect of Bd on the microbiome was greater than the effect of the microbiome on Bd. Assessment of the microbiome differences between more distantly related populations than those studied here is needed to fully understand the role of the microbiome in resistance to Bd.

Project description:Predicting pathogen spillover requires counting spillover events and aligning such counts with process-related covariates for each spillover event. How can we connect our analysis of spillover counts to simple, mechanistic models of pathogens jumping from reservoir hosts to recipient hosts? We illustrate how the pathways to pathogen spillover can be represented as a directed graph connecting reservoir hosts and recipient hosts and the number of spillover events modelled as a percolation of infectious units along that graph. Percolation models of pathogen spillover formalize popular intuition and management concepts for pathogen spillover, such as the inextricably multilevel nature of cross-species transmission, the impact of covariance between processes such as pathogen shedding and human susceptibility on spillover risk, and the assumptions under which the effect of a management intervention targeting one process, such as persistence of vectors, will translate to an equal effect on the overall spillover risk. Percolation models also link statistical analysis of spillover event datasets with a mechanistic model of spillover. Linear models, one might construct for process-specific parameters, such as the log-rate of shedding from one of several alternative reservoirs, yield a nonlinear model of the log-rate of spillover. The resulting nonlinearity is approximately piecewise linear with major impacts on statistical inferences of the importance of process-specific covariates such as vector density. We recommend that statistical analysis of spillover datasets use piecewise linear models, such as generalized additive models, regression clustering or ensembles of linear models, to capture the piecewise linearity expected from percolation models. We discuss the implications of our findings for predictions of spillover risk beyond the range of observed covariates, a major challenge of forecasting spillover risk in the Anthropocene. This article is part of the theme issue 'Dynamic and integrative approaches to understanding pathogen spillover'.

Project description:The loss of hearing structures and loss of advertisement calls in many terrestrial breeding frogs (Strabomantidae) living at high elevations in South America are common and intriguing phenomena. The Andean frog genus Phrynopus Peters, 1873 has undergone an evolutionary radiation in which most species lack the tympanic membrane and tympanic annulus, yet the phylogenetic relationships among species in this group remain largely unknown. Here, we present an expanded molecular phylogeny of Phrynopus that includes 24 nominal species. Our phylogeny includes Phrynopus peruanus, the type species of the genus, and 10 other species for which genetic data were previously unavailable. We found strong support for monophyly of Phrynopus, and that two nominal species-Phrynopus curator and Phrynopus nicoleae-are junior synonyms of Phrynopus tribulosus. Using X-ray computed tomography (CT) imaging, we demonstrate that the absence of external hearing structures is associated with complete loss of the auditory skeletal elements (columella) in at least one member of the genus. We mapped the tympanum condition on to a species tree to infer whether the loss of hearing structures took place once or multiple times. We also assessed whether tympanum condition, body size, and body shape are associated with the elevational distribution and habitat use. We identified a single evolutionary transition that involved the loss of both the tympanic membrane and tympanic annulus, which in turn is correlated with the absence of advertisement calls. We also identified several species pairs where one species inhabits the Andean grassland and the other montane forest. When accounting for phylogenetic relatedness among species, we detected a significant pattern of increasing body size with increasing elevation. Additionally, species at higher elevations tend to develop shorter limbs, shorter head, and shorter snout than species living at lower elevations. Our findings strongly suggest a link between ecological divergence and morphological diversity of terrestrial breeding frogs living in montane gradients.

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Low-load pathogen spillover predicts shifts in skin microbiome and survival of a terrestrial-breeding amphibian.

Publications

Low-load pathogen spillover predicts shifts in skin microbiome and survival of a terrestrial-breeding amphibian.

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