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1. How host-microbiome/holobiont evolution depends on whether the microbiome affects host lifespan or fecundity

   https://doi.org/10.1093/jeb/voae127  

   Brown, Alexandra L; Koskella, Britt; Boots, Mike (January 2025, Journal of Evolutionary Biology)

   Li_Richter, Xiang-Yi; Jain, Kavita (Ed.)

   Abstract There is overwhelming evidence that the microbiome can be important to host physiology and fitness. As such, there is interest in and some theoretical work on understanding when hosts and microbiomes (co)evolve so that microbes benefit hosts and hosts favour beneficial microbes. However, the outcome of evolution likely depends on how microbes benefit hosts. Here, we use adaptive dynamics to investigate how host and symbiont evolution depend on whether symbionts increase host lifespan or host reproduction in a simple model of host and symbiont dynamics. In addition, we investigate 2 ways hosts release (and transmit) symbionts: by releasing symbionts steadily during their lifetime or by releasing them at reproduction, potentially increasing symbionts’ chances of infecting the host’s offspring. The former is strict horizontal transmission, whereas the latter is also a form of indirect or “pseudovertical” transmission. Our first key result is that the evolution of symbionts that benefit host fecundity requires pseudovertical transmission, while the evolution of symbionts that benefit host lifespan does not. Furthermore, our second key result is that when investing in host benefits is costly to the free-living symbiont stage, intermediate levels of pseudovertical transmission are needed for selection to favour beneficial symbionts. This is true regardless of fitness effects because release at reproduction increases the free-living symbiont population, which increases competition for hosts. Consequently, hosts could evolve away from traits that favour beneficial symbionts. Generally, our work emphasizes the importance of different forms of vertical transmission and fitness benefits in host, microbiome, and holobiont evolution as highlighted by our prediction that the evolution of fecundity-increasing symbionts requires parent-to-offspring transmission. 

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2. Mobile genetic elements exhibit associated patterns of host range variation and sequence diversity within the gut microbiome of the European Honey bee

   https://doi.org/10.1101/2025.01.31.635958  

   Robinson, Chris_R P; Dolezal, Adam G; Liachko, Ivan; Newton, Irene_L G (February 2025, bioRxiv)

   Abstract Mobile genetic elements (MGEs), such as plasmids and bacteriophages, are major contributors to the ecology and evolution of host-associated microbes due to a continuum of symbiotic interactions and by mediating gene flow via horizontal gene transmission. However, while myriad studies have investigated relationships between MGEs and variation in fitness among microbial and eukaryotic hosts, few studies have incorporated this variation into the context of MGE evolution and ecology. Combining HiC-resolved metagenomics with the model honey bee worker gut microbiome, we show that the worker gut contains a dense, nested MGE community that exhibits a wide degree of host range variation among microbial hosts. Using measures of gene similarity and syntenty, we show that plasmids likely mediate gene flow between individual honey bee colonies, though these plasmids exhibit broad host range variation within their individual microbiomes. We further show that phage-microbe networks exhibit high variation among individual metagenomes, and that phages show broad host range with respect to both the number and phylogenetic distance of their hosts. Finally, we provide evidence that measures of nucleotide variation positively correlate with host range in bee-associated phages, and that functional targets of diversifying selection are partitioning differently between broad or narrow host range phages. Our work underscores the variability of MGE x microbial interactions within host-associated microbial communities and highlights the genomic variation associated with MGE host range diversity. 

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3. Large Comparative Analyses of Primate Body Site Microbiomes Indicate that the Oral Microbiome Is Unique among All Body Sites and Conserved among Nonhuman Primates

   https://doi.org/10.1128/spectrum.01643-21  

   Asangba, Abigail E.; Mugisha, Lawrence; Rukundo, Joshua; Lewis, Rebecca J.; Halajian, Ali; Cortés-Ortiz, Liliana; Junge, Randall E.; Irwin, Mitchell T.; Karlson, Johan; Perkin, Andrew; et al (June 2022, Microbiology Spectrum)

   Kormas, Konstantinos Aristomenis (Ed.)

   ABSTRACT The study of the mammalian microbiome serves as a critical tool for understanding host-microbial diversity and coevolution and the impact of bacterial communities on host health. While studies of specific microbial systems (e.g., in the human gut) have rapidly increased, large knowledge gaps remain, hindering our understanding of the determinants and levels of variation in microbiomes across multiple body sites and host species. Here, we compare microbiome community compositions from eight distinct body sites among 17 phylogenetically diverse species of nonhuman primates (NHPs), representing the largest comparative study of microbial diversity across primate host species and body sites. Analysis of 898 samples predominantly acquired in the wild demonstrated that oral microbiomes were unique in their clustering, with distinctive divergence from all other body site microbiomes. In contrast, all other body site microbiomes clustered principally by host species and differentiated by body site within host species. These results highlight two key findings: (i) the oral microbiome is unique compared to all other body site microbiomes and conserved among diverse nonhuman primates, despite their considerable dietary and phylogenetic differences, and (ii) assessments of the determinants of host-microbial diversity are relative to the level of the comparison (i.e., intra-/inter-body site, -host species, and -individual), emphasizing the need for broader comparative microbial analyses across diverse hosts to further elucidate host-microbial dynamics, evolutionary and biological patterns of variation, and implications for human-microbial coevolution. IMPORTANCE The microbiome is critical to host health and disease, but much remains unknown about the determinants, levels, and evolution of host-microbial diversity. The relationship between hosts and their associated microbes is complex. Most studies to date have focused on the gut microbiome; however, large gaps remain in our understanding of host-microbial diversity, coevolution, and levels of variation in microbiomes across multiple body sites and host species. To better understand the patterns of variation and evolutionary context of host-microbial communities, we conducted one of the largest comparative studies to date, which indicated that the oral microbiome was distinct from the microbiomes of all other body sites and convergent across host species, suggesting conserved niche specialization within the Primates order. We also show the importance of host species differences in shaping the microbiome within specific body sites. This large, comparative study contributes valuable information on key patterns of variation among hosts and body sites, with implications for understanding host-microbial dynamics and human-microbial coevolution. 

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4. Selection of an anti-pathogen skin microbiome following prophylaxis treatment in an amphibian model system

   https://doi.org/10.1098/rstb.2022.0126  

   Siomko, Samantha A.; Greenspan, Sasha E.; Barnett, K. M.; Neely, Wesley J.; Chtarbanova, Stanislava; Woodhams, Douglas C.; McMahon, Taegan A.; Becker, C. Guilherme (July 2023, Philosophical Transactions of the Royal Society B: Biological Sciences)

   With emerging diseases on the rise, there is an urgent need to identify and understand novel mechanisms of prophylactic protection in vertebrate hosts. Inducing resistance against emerging pathogens through prophylaxis is an ideal management strategy that may impact pathogens and their host-associated microbiome. The host microbiome is recognized as a critical component of immunity, but the effects of prophylactic inoculation on the microbiome are unknown. In this study, we investigate the effects of prophylaxis on host microbiome composition, focusing on the selection of anti-pathogenic microbes contributing to host acquired immunity in a model host–fungal disease system, amphibian chytridiomycosis. We inoculated larval Pseudacris regilla against the fungal pathogen Batrachochytrium dendrobatidis ( Bd ) with a Bd metabolite-based prophylactic. Increased prophylactic concentration and exposure duration were associated with significant increases in proportions of putatively Bd -inhibitory host-associated bacterial taxa, indicating a protective prophylactic-induced shift towards microbiome members that are antagonistic to Bd. Our findings are in accordance with the adaptive microbiome hypothesis, where exposure to a pathogen alters the microbiome to better cope with subsequent pathogen encounters. Our study advances research on the temporal dynamics of microbiome memory and the role of prophylaxis-induced shifts in microbiomes contributing to prophylaxis effectiveness. This article is part of the theme issue ‘Amphibian immunity: stress, disease and ecoimmunology’. 

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5. A ridge-to-reef ecosystem microbial census reveals environmental reservoirs for animal and plant microbiomes

   https://doi.org/10.1073/pnas.2204146119  

   Amend, Anthony S.; Swift, Sean O.; Darcy, John L.; Belcaid, Mahdi; Nelson, Craig E.; Buchanan, Joshua; Cetraro, Nicolas; Fraiola, Kauaoa M.; Frank, Kiana; Kajihara, Kacie; et al (August 2022, Proceedings of the National Academy of Sciences)

   Microbes are found in nearly every habitat and organism on the planet, where they are critical to host health, fitness, and metabolism. In most organisms, few microbes are inherited at birth; instead, acquiring microbiomes generally involves complicated interactions between the environment, hosts, and symbionts. Despite the criticality of microbiome acquisition, we know little about where hosts’ microbes reside when not in or on hosts of interest. Because microbes span a continuum ranging from generalists associating with multiple hosts and habitats to specialists with narrower host ranges, identifying potential sources of microbial diversity that can contribute to the microbiomes of unrelated hosts is a gap in our understanding of microbiome assembly. Microbial dispersal attenuates with distance, so identifying sources and sinks requires data from microbiomes that are contemporary and near enough for potential microbial transmission. Here, we characterize microbiomes across adjacent terrestrial and aquatic hosts and habitats throughout an entire watershed, showing that the most species-poor microbiomes are partial subsets of the most species-rich and that microbiomes of plants and animals are nested within those of their environments. Furthermore, we show that the host and habitat range of a microbe within a single ecosystem predicts its global distribution, a relationship with implications for global microbial assembly processes. Thus, the tendency for microbes to occupy multiple habitats and unrelated hosts enables persistent microbiomes, even when host populations are disjunct. Our whole-watershed census demonstrates how a nested distribution of microbes, following the trophic hierarchies of hosts, can shape microbial acquisition. 

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