Abstract Microbial diversity positively influences community resilience of the host microbiome. However, extinction risk factors such as habitat specialization, narrow environmental tolerances, and exposure to anthropogenic disturbance may homogenize host-associated microbial communities critical for stress responses including disease defense. In a dataset containing 43 threatened and 90 non-threatened amphibian species across two biodiversity hotspots (Brazil’s Atlantic Forest and Madagascar), we found that threatened host species carried lower skin bacterial diversity, after accounting for key environmental and host factors. The consistency of our findings across continents suggests the broad scale at which low bacteriome diversity may compromise pathogen defenses in species already burdened with the threat of extinction.
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Abstract Background Host microbiomes may differ under the same environmental conditions and these differences may influence susceptibility to infection. Amphibians are ideal for comparing microbiomes in the context of disease defense because hundreds of species face infection with the skin-invading microbe
Batrachochytrium dendrobatidis (Bd), and species richness of host communities, including their skin bacteria (bacteriome), may be exceptionally high. We conducted a landscape-scale Bd survey of six co-occurring amphibian species in Brazil’s Atlantic Forest. To test the bacteriome as a driver of differential Bd prevalence, we compared bacteriome composition and co-occurrence network structure among the six focal host species.Results Intensive sampling yielded divergent Bd prevalence in two ecologically similar terrestrial-breeding species, a group with historically low Bd resistance. Specifically, we detected the highest Bd prevalence in
Ischnocnema henselii but no Bd detections inHaddadus binotatus .Haddadus binotatus carried the highest bacteriome alpha and common core diversity, and a modular network partitioned by negative co-occurrences, characteristics associated with community stability and competitive interactions that could inhibit Bd colonization.Conclusions Our findings suggest that community structure of the bacteriome might drive Bd resistance in
H. binotatus , which could guide microbiome manipulation as a conservation strategy to protect diverse radiations of direct-developing species from Bd-induced population collapses. -
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Abstract The host‐associated microbiome plays a significant role in health. However, the roles of factors such as host genetics and microbial interactions in determining microbiome diversity remain unclear. We examined these factors using amplicon‐based sequencing of 175
Thoropa taophora frog skin swabs collected from a naturally fragmented landscape in southeastern Brazil. Specifically, we examined (1) the effects of geography and host genetics on microbiome diversity and structure; (2) the structure of microbial eukaryotic and bacterial co‐occurrence networks; and (3) co‐occurrence between microeukaryotes with bacterial OTUs known to affect growth of the fungal pathogenBatrachochytrium dendrobatidis (Bd ). While bacterial alpha diversity varied by both site type and host MHC IIB genotype, microeukaryotic alpha diversity varied only by site type. However, bacteria and microeukaryote composition showed variation according to both site type and host MHC IIB genotype. Our network analysis showed the highest connectivity when both eukaryotes and bacteria were included, implying that ecological interactions may occur among domains. Lastly, anti‐Bd bacteria were not broadly negatively co‐associated with the fungal microbiome and were positively associated with potential amphibian parasites. Our findings emphasize the importance of considering both domains in microbiome research and suggest that for effective probiotic strategies for amphibian disease management, considering potential interactions among all members of the microbiome is crucial. -
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ABSTRACT Anthropogenic habitat disturbance is fundamentally altering patterns of disease transmission and immunity across the vertebrate tree of life. Most studies linking anthropogenic habitat change and disease focus on habitat loss and fragmentation, but these processes often lead to a third process that is equally important:
habitat split . Defined as spatial separation between the multiple classes of natural habitat that many vertebrate species require to complete their life cycles, habitat split has been linked to population declines in vertebrates, e.g. amphibians breeding in lowland aquatic habitats and overwintering in fragments of upland terrestrial vegetation. Here, we link habitat split to enhanced disease risk in amphibians (i ) by reviewing the biotic and abiotic forces shaping elements of immunity and (ii ) through a spatially oriented field study focused on tropical frogs. We propose a framework to investigate mechanisms by which habitat split influences disease risk in amphibians, focusing on three broad host factors linked to immunity: (i ) composition of symbiotic microbial communities, (ii ) immunogenetic variation, and (iii ) stress hormone levels. Our review highlights the potential for habitat split to contribute to host‐associated microbiome dysbiosis, reductions in immunogenetic repertoire, and chronic stress, that often facilitate pathogenic infections and disease in amphibians and other classes of vertebrates. We highlight that targeted habitat‐restoration strategies aiming to connect multiple classes of natural habitats (e.g. terrestrial–freshwater, terrestrial–marine, marine–freshwater) could enhance priming of the vertebrate immune system through repeated low‐load exposure to enzootic pathogens and reduced stress‐induced immunosuppression. -
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Abstract Aim We combine phylogenetic and point locality data from selected lineages of the Atlantic Forest flora and fauna to compare spatial patterns of biodiversity sustained by the current configuration of forest remnants to a scenario of complete forest preservation. We then ask the question how much biodiversity is likely lost, already? Specifically, we assess how habitat loss likely impacted the climatic spaces occupied by the local species, the inferred composition of local communities and the spatial distribution of phylogenetic diversity and endemism.
Location Atlantic Forest, Brazil.
Methods Using carefully curated point localities, phylogenetic data and parameterized models of species distributions, we generate maps of phylogenetic diversity, phylogenetic endemism and phylogenetic turnover for the entire Atlantic Forest. We map patterns of clade‐specific diversity under complete preservation of forest and then incorporate present‐day deforestation patterns to provide a more realistic scenario.
Results Instead of a singular pattern, three different reoccurring syndromes described the flora and fauna of the Atlantic Forest. These patterns emerged irrespectively of clade age and life history traits. General turnover patterns were highly consistent with previous analyses of species composition and panbiogeographical studies. Deforestation has altered the availability of climatic spaces in the Atlantic Forest, its biological communities and the distribution of evolutionary lineages in space. However, approximately 60% of the pre‐Columbian climatic space persists in forest remnants, and today's biological communities are estimated to be 45% similar to pre‐deforestation times.
Main conclusions The Atlantic Forest has been reduced to 8% of its once largely continuous range. However, the disproportionately large amounts of climate, community and lineage diversity that persist in remnants provide hope and support for conservation efforts that combine species occurrence and phylogenetic data. Inclusion of evolutionary thinking into strategic approaches to restoring Brazilian ecosystems could further conservation effectiveness by incorporating the adaptive potential of local assemblages in the face of further environmental shifts.
