Specific gut bacterial responses to natural diets of tropical birds

The composition of gut bacterial communities is strongly influenced by the host diet in many animal taxa. For birds, the effect of diet on the microbiomes has been documented through diet manipulation studies. However, for wild birds, most studies have drawn on literature-based information to decipher the dietary effects, thereby, overlooking individual variation in dietary intake. Here we examine how naturally consumed diets influence the composition of the crop and cloacal microbiomes of twenty-one tropical bird species, using visual and metabarcoding-based identification of consumed diets and bacterial 16S rRNA microbiome sequencing. We show that diet intakes vary markedly between individuals of the same species and that literature-based dietary guilds grossly underestimate intraspecific diet variability. Furthermore, despite an effect of literature-based dietary guild assignment of host taxa, the composition of natural diets does not align with crop and cloacal microbiome similarity. However, host-taxon specific gut bacterial lineages are positively correlated with specific diet items, indicating that certain microbes associate with different diet components in specific avian hosts. Consequently, microbiome composition is not congruent with the overall consumed diet composition of species, but specific components of a consumed diet lead to host-specific effects on gut bacterial taxa.

Global Patterns of the Fungal Pathogen Batrachochytrium dendrobatidis Support Conservation Urgency

The amphibian chytrid fungus Batrachochytrium dendrobatidis (Bd) is a skin pathogen that can cause the emerging infectious disease chytridiomycosis in susceptible species. It has been considered one of the most severe threats to amphibian biodiversity. We aimed to provide an updated compilation of global Bd occurrences by host taxon and geography, and with the larger global Bd dataset we reanalyzed Bd associations with environmental metrics at the world and regional scales. We also compared our Bd data compilation with a recent independent assessment to provide a more comprehensive count of species and countries with Bd occurrences. Bd has been detected in 1,375 of 2,525 (55%) species sampled, more than doubling known species infections since 2013. Bd occurrence is known from 93 of 134 (69%) countries at this writing; this compares to known occurrences in 56 of 82 (68%) countries in 2013. Climate-niche space is highly associated with Bd detection, with different climate metrics emerging as key predictors of Bd occurrence at regional scales; this warrants further assessment relative to climate-change projections. The accretion of Bd occurrence reports points to the common aims of worldwide investigators to understand the conservation concerns for amphibian biodiversity in the face of potential disease threat. Renewed calls for better mitigation of amphibian disease threats resonate across continents with amphibians, especially outside Asia. As Bd appears to be able to infect about half of amphibian taxa and sites, there is considerable room for biosecurity actions to forestall its spread using both bottom-up community-run efforts and top-down national-to-international policies. Conservation safeguards for sensitive species and biodiversity refugia are continuing priorities.

Patterns of infection, origins and transmission of ranaviruses among the ectothermic vertebrates of Asia

Ranaviral infections, a malady of ectothermic vertebrates, are becoming frequent, severe, and widespread, causing mortality among both native and cultured species, raising odds of species extinctions and economic losses. This turn of events is possibly due to the broad host range of ranaviruses and the transmission of these pathogens through regional and international trade in Asia, where outbreaks have been increasingly reported over the past decade. Here we focus attention on the origins, means of transmission, and patterns of spread of this infection within the region. Infections have been recorded in both cultured and wild populations in at least twelve countries/administrative regions, together with mass die-offs in some regions. Despite the imminent seriousness of the disease in Asia, surveillance efforts are still incipient. Some of the infections transmitted within Asia may transmit across host-taxon barriers, posing a significant risk to native species. Factors such as rising temperatures due to global climate change seem to exacerbate ranaviral activity, as most known outbreaks have been recorded during summer; however, data are still inadequate to verify this for Asia. Import risk analysis, using protocols such as Pandora+, pre-border pathogen screening, and effective biosecurity measures, can be used to mitigate introduction to uninfected areas and curb transmission within Asia. Comprehensive surveillance using molecular diagnostic tools for ranavirus species and variants will help in understanding the prevalence and disease burden in the region. This is an important step towards conserving native biodiversity and safeguarding the aquaculture industry.

Disentangling the Relative Roles of Vertical Transmission, Subsequent Colonizations, and Diet on Cockroach Microbiome Assembly

ABSTRACT A multitude of factors affect the assemblies of complex microbial communities associated with animal hosts, with implications for community flexibility, resilience, and long-term stability; however, their relative effects have rarely been deduced. Here, we use a tractable lab model to quantify the relative and combined effects of parental transmission (egg case microbiome present/reduced), gut inocula (cockroach versus termite gut provisioned), and varying diets (matched or unmatched with gut inoculum source) on gut microbiota structure of hatchlings of the omnivorous cockroach Shelfordella lateralis using 16S rRNA gene (rDNA) amplicon sequencing. We show that the presence of a preexisting bacterial community via vertical transmission of microbes on egg cases reduces subsequent microbial invasion, suggesting priority effects that allow initial colonizers to take a strong hold and which stabilize the microbiome. However, subsequent inoculation sources more strongly affect ultimate community composition and their ecological networks, with distinct host-taxon-of-origin effects on which bacteria establish. While this is so, communities respond flexibly to specific diets in ways that consequently impact predicted community functions. In conclusion, our findings suggest that inoculations drive communities toward different stable states depending on colonization and extinction events, through ecological host-microbe relations and interactions with other gut bacteria, while diet in parallel shapes the functional capabilities of these microbiomes. These effects may lead to consistent microbial communities that maximize the extended phenotype that the microbiota provides the host, particularly if microbes spend most of their lives in host-associated environments. IMPORTANCE When host fitness is dependent on gut microbiota, microbial community flexibility and reproducibility enhance host fitness by allowing fine-tuned environmental tracking and sufficient stability for host traits to evolve. Our findings lend support to the importance of vertically transmitted early-life microbiota as stabilizers, through interactions with potential colonizers, which may contribute to ensuring that the microbiota aligns within host fitness-enhancing parameters. Subsequent colonizations are driven by microbial composition of the sources available, and we confirm that host-taxon-of-origin affects stable subsequent communities, while communities at the same time retain sufficient flexibility to shift in response to available diets. Microbiome structure is thus the result of the relative impact and combined effects of inocula and fluctuations driven by environment-specific microbial sources and digestive needs. These affect short-term community structure on an ecological time scale but could ultimately shape host species specificities in microbiomes across evolutionary time, if environmental conditions prevail.

Genotypic similarity among algal symbionts corresponds to associations with closely related coral hosts

Mutualisms where hosts are coupled metabolically to their symbionts often exhibit high partner fidelity. Most reef-building corals form obligate symbioses with specific species of photosymbionts, dinoflagellates in the family Symbiodiniaceae, despite needing to acquire symbionts early in their development from environmental sources. Three Caribbean acroporids (Acropora palmata, A. cervicornis, and their hybrid A. prolifera) are geographically sympatric across much of their range in the greater Caribbean, but often occupy different depth and light habitats. Both species and their hybrid associate with Symbiodinium ‘fitti’, a genetically diverse species of symbiont that is specific to these hosts. Since the physiology of the dinoflagellate partner is strongly influenced by light (and therefore depth), we investigated whether S. ‘fitti’ populations from each host source were differentiated genetically. We generated shallow genome sequences of acroporid colonies sampled from across the Caribbean. Single Nucleotide Polymorphisms (SNPs) among S. ‘fitti’ strains were identified by aligning sequences to a ~600 Mb draft assembly of the S. ‘fitti’ genome, assembled from an A. cervicornis metagenome. Phylogenomic and multivariate analyses revealed that allelic variation among S. ‘fitti’ partitioned to each host species, as well as their hybrid, rather than by biogeographic origin. This is particularly noteworthy because the hybrid, A. prolifera, has a sparse fossil record and may be of relatively recent origin. Many of the SNPs putatively under selection were non-synonymous mutations predicted to alter protein efficiency. Differences in allele frequency among S. ‘fitti’ populations from each host taxon may correspond to distinct phenotypes that thrive in the different cellular environments found in each acroporid. The non-random sorting among genetically diverse strains, or genotypes, to different hosts could be the basis for lineage diversification via disruptive selection, leading to ecological specialization and ultimately speciation.

Disentangling the relative roles of vertical transmission, subsequent colonizations and diet on cockroach microbiome assembly

A multitude of factors affect the assemblies of complex microbial communities associated with animal hosts, with implications for community flexibility, resilience and long-term stability; however, their relative effects have rarely been deduced. Here, we use a tractable lab model to quantify the relative and combined effects of parental transmission (egg case microbiome present/reduced), gut inocula (cockroach vs. termite gut provisioned), and varying diets (matched with gut inoculum source) on gut microbiota structure of hatchlings of the omnivorous cockroach Shelfordella lateralis using 16S rDNA amplicon sequencing. We show that the presence of a pre-existing bacterial community via vertical transmission of microbes on egg cases reduces subsequent microbial invasion, suggesting priority effects that allow initial colonizers to take a stronghold and which stabilize the microbiome. However, the subsequent inoculation sources more strongly affect ultimate community composition, with distinct host-taxon-of-origin effects on which bacteria establish. While this is so, communities respond flexibly to specific diets that consequently strongly impact community functions predicted using PICRUSt2. In conclusion, our findings suggest that inoculations drive communities towards different stable states depending on colonization and extinction events, through ecological host-microbe relations and interactions with other gut bacteria, while diet in parallel shapes the functional capabilities of these microbiomes. These effects may lead to consistent microbial communities that maximize the extended phenotype that the microbiota provides the host, particularly if microbes spend most of their lives in host-associated environments.Contribution to the fieldWhen host fitness is dependent on gut microbiota, microbial community flexibility and reproducibility enhance host fitness by allowing fine-tuned environmental tracking and sufficient stability for host traits to evolve. Our findings lend support to the importance of vertically transmitted early-life microbiota as stabilizers through interactions with potential colonizers that may contribute to ensuring that the microbiota aligns within host fitness-enhancing parameters. Subsequent colonizations are driven by microbial composition of the sources available, and we confirm that host-taxon-of-origin affects stable subsequent communities, while communities at the same time retain sufficient flexibility to shift in response to available diets. Microbiome structure is thus the result of the relative impact and combined effects of inocula and fluctuations driven by environment-specific microbial sources and digestive needs. These affect short-term community structure on an ecological time scale, but could ultimately shape host species specificities in microbiomes across evolutionary time, if environmental conditions prevail.

Gut Bacteria in the Holometabola: A Review of Obligate and Facultative Symbionts

The diversity and ecological variety of Holometabola foregrounds a wide array of dynamic symbiotic relationships with gut-dwelling bacteria. A review of the literature highlights that holometabolous insects rely on both obligate bacteria and facultative bacteria living in their guts to satisfy a number of physiological needs. The driving forces behind these differing relationships can be hypothesized through the scrutiny of bacterial associations with host gut morphology, and transmission of bacteria within a given host taxon. Our knowledge of the evolution of facultative or obligate symbiotic bacteria in holometabolan systems is further enhanced by an assessment of the various services the bacteria provide, including nutrition, immune system health, and development. The diversity of Holometabola can thus be examined through an assessment of known bacterial partnerships within the orders of Holometabola.

Into the wild: microbiome transplant studies need broader ecological reality

Gut microbial communities (microbiomes) profoundly shape the ecology and evolution of multicellular life. Interactions between host and microbiome appear to be reciprocal, and ecological theory is now being applied to better understand how hosts and their microbiome influence each other. However, some ecological processes that underlie reciprocal host–microbiome interactions may be obscured by the current convention of highly controlled transplantation experiments. Although these approaches have yielded invaluable insights, there is a need for a broader array of approaches to fully understand host–microbiome reciprocity. Using a directed review, we surveyed the breadth of ecological reality in the current literature on gut microbiome transplants with non-human recipients. For 55 studies, we categorized nine key experimental conditions that impact the ecological reality (EcoReality) of the transplant, including host taxon match and donor environment. Using these categories, we rated the EcoReality of each transplant. Encouragingly, the breadth of EcoReality has increased over time, but some components of EcoReality are still relatively unexplored, including recipient host environment and microbiome state. The conceptual framework we develop here maps the landscape of possible EcoReality to highlight where fundamental ecological processes can be considered in future transplant experiments.