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1. Cloacal microbiomes of sympatric and allopatric Sceloporus lizards vary with environment and host relatedness

   https://doi.org/10.1371/journal.pone.0279288  

   Bunker, Marie E. ; Weiss, Stacey L. ( December 2022 , PLOS ONE)

   Ruiz-Rodriguez, Magdalena (Ed.)

   Animals and their microbiomes exert reciprocal influence; the host’s environment, physiology, and phylogeny can impact the composition of the microbiome, while the microbes present can affect host behavior, health, and fitness. While some microbiomes are highly malleable, specialized microbiomes that provide important functions can be more robust to environmental perturbations. Recent evidence suggests Sceloporus virgatus has one such specialized microbiome, which functions to protect eggs from fungal pathogens during incubation. Here, we examine the cloacal microbiome of three different Sceloporus species (spiny lizards; Family Phrynosomatidae)– Sceloporus virgatus , Sceloporus jarrovii , and Sceloporus occidentalis . We compare two species with different reproductive modes (oviparous vs. viviparous) living in sympatry: S . virgatus and S . jarrovii . We compare sister species living in similar habitats (riparian oak-pine woodlands) but different latitudes: S . virgatus and S . occidentalis . And, we compare three populations of one species ( S . occidentalis ) living in different habitat types: beach, low elevation forest, and the riparian woodland. We found differences in beta diversity metrics between all three comparisons, although those differences were more extreme between animals in different environments, even though those populations were more closely related. Similarly, alpha diversity varied among the S . occidentalis populations and between S . occidentalis and S . virgatus , but not between sympatric S . virgatus and S . jarrovii . Despite these differences, all three species and all three populations of S . occcidentalis had the same dominant taxon, Enterobacteriaceae . The majority of the variation between groups was in low abundance taxa and at the ASV level; these taxa are responsive to habitat differences, geographic distance, and host relatedness. Uncovering what factors influence the composition of wild microbiomes is important to understanding the ecology and evolution of the host animals, and can lead to more detailed exploration of the function of particular microbes and the community as a whole. 

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2. The reproductive microbiome and maternal transmission of microbiota via eggs in Sceloporus virgatus

   https://doi.org/10.1093/femsec/fiae011  

   Bunker, Marie E. ; Weiss, Stacey L. ( February 2024 , FEMS Microbiology Ecology)

   Maternal transmission of microbes occurs across the animal kingdom and is vital for offspring development and long-term health. The mechanisms of this transfer are most well-studied in humans and other mammals but are less well-understood in egg-laying animals, especially those with no parental care. Here, we investigate the transfer of maternal microbes in the oviparous phrynosomatid lizard, Sceloporus virgatus. We compared the microbiota of three maternal tissues—oviduct, cloaca, and intestine—to three offspring sample types: egg contents and eggshells on the day of oviposition, and hatchling intestinal tissue on the day of hatching. We found that maternal identity is an important factor in hatchling microbiome composition, indicating that maternal transmission is occurring. The maternal cloacal and oviductal communities contribute to offspring microbiota in all three sample types, with minimal microbes sourced from maternal intestines. This indicates that the maternal reproductive microbiome is more important for microbial inheritance than the gut microbiome, and the tissue-level variation of the adult S. virgatus microbiota must develop as the hatchling matures. Despite differences between adult and hatchling communities, offspring microbiota were primarily members of the Enterobacteriaceae and Yersiniaceae families (Phylum Proteobacteria), consistent with this and past studies of adult S. virgatus microbiomes.

    

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3. Recovered microbiome of an oviparous lizard differs across gut and reproductive tissues, cloacal swabs, and faeces

   https://doi.org/10.1111/1755-0998.13573  

   Bunker, Marie E. ; Martin, Mark O. ; Weiss, Stacey L. ( December 2021 , Molecular Ecology Resources)

   Microbial diversity and community function are related, and can be highly specialized in different gut regions. The cloacal microbiome ofSceloporus virgatusfemales provides antifungal protection to eggshells, a specialized function that suggests a specialized microbiome. Here, we describe the cloacal, intestinal, and oviductal microbiome fromS.virgatusgravid females, adding to growing evidence of microbiome localization in reptiles and other taxa. We further assessed whether common methods for sampling gastrointestinal (GI) microbes – cloacal swabs and faeces – provide accurate representations of these microbial communities. We found that different regions of the gut had unique microbial communities. The cloacal microbiome showed extreme specialization averaging 99% Proteobacteria (Phylum) and 83%Enterobacteriacaea(Family).Enterobacteriacaeadecreased up the GI and reproductive tracts. Cloacal swabs recovered communities similar to that of lower intestine and cloacal tissues. In contrast, faecal samples had much higher diversity and a distinct composition (common Phyla: 62% Firmicutes, 18% Bacteroidetes, 10% Proteobacteria; common families: 39%Lachnospiraceae, 11%Ruminococcaceae, 11%Bacteroidaceae) relative to all gut regions. The common families in faecal samples made up <1% of cloacal tissue samples, increasing to 43% at the upper intestine. Similarly, the common families in gut tissue (EnterobacteriaceaeandHelicobacteraceae) made up <1% of the faecal microbiome. Further, we found that cloacal swabs taken shortly after defaecation may be contaminated with faecal matter. Our results serve as a caution against using faeces as a proxy for GI microbes, and may help explain high between‐sample variation seen in some studies using cloacal swabs.

    

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4. Geography and elevation as drivers of cloacal microbiome assemblages of a passerine bird distributed across Sulawesi, Indonesia

   https://doi.org/10.1186/s42523-022-00219-3  

   Joakim, Rachael L. ; Irham, Mohammad ; Haryoko, Tri ; Rowe, Karen M. C. ; Dalimunthe, Yohanna ; Anita, Syahfitri ; Achmadi, Anang S. ; McGuire, Jimmy A. ; Perkins, Susan ; Bowie, Rauri C. K. ( January 2023 , Animal Microbiome)

   Empirical field studies allow us to view how ecological and environmental processes shape the biodiversity of our planet, but collecting samples in situ creates inherent challenges. The majority of empirical vertebrate gut microbiome research compares multiple host species against abiotic and biotic factors, increasing the potential for confounding environmental variables. To minimize these confounding factors, we focus on a single species of passerine bird found throughout the geologically complex island of Sulawesi, Indonesia. We assessed the effects of two environmental factors, geographic Areas of Endemism (AOEs) and elevation, as well as host sex on the gut microbiota assemblages of the Sulawesi Babbler,Pellorneum celebense,from three different mountains across the island. Using cloacal swabs, high-throughput-amplicon sequencing, and multiple statistical models, we identified the core microbiome and determined the signal of these three factors on microbial composition.

   The five most prevalent bacterial phyla within the gut microbiome ofP. celebensewereProteobacteria(32.6%),Actinobacteria(25.2%),Firmicutes(22.1%),Bacteroidetes(8.7%), andPlantomycetes(2.6%). These results are similar to those identified in prior studies of passeriform microbiomes. Overall, microbiota diversity decreased as elevation increased, irrespective of sex or AOE. A single ASV ofClostridiumwas enriched in higher elevation samples, while lower elevation samples were enriched with the generaPerlucidibaca(FamilyMoraxellaceae),Lachnoclostridium(FamilyLachnospiraceae), and an unidentified species in the FamilyPseudonocardiaceae.

   While the core microbiota families recovered here are consistent with other passerine studies, the decreases in diversity as elevation increases has only been seen in non-avian hosts. Additionally, the increased abundance ofClostridiumat high elevations suggests a potential microbial response to lower oxygen levels. This study emphasizes the importance of incorporating multiple statistical models and abiotic factors such as elevation in empirical microbiome research, and is the first to describe an avian gut microbiome from the island of Sulawesi.

    

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5. Sustained Drought, but Not Short-Term Warming, Alters the Gut Microbiomes of Wild Anolis Lizards

   https://doi.org/10.1128/aem.00530-22  

   Williams, Claire E. ; Kueneman, Jordan G. ; Nicholson, Daniel J. ; Rosso, Adam A. ; Folfas, Edita ; Casement, Brianna ; Gallegos-Koyner, Maria A. ; Neel, Lauren K. ; Curlis, John David ; McMillan, W. Owen ; et al ( October 2022 , Applied and Environmental Microbiology)

   Rudi, Knut (Ed.)

   ABSTRACT As rising temperatures threaten biodiversity across the globe, tropical ectotherms are thought to be particularly vulnerable due to their narrow thermal tolerance ranges. Nevertheless, physiology-based models highlighting the vulnerability of tropical organisms rarely consider the contributions of their gut microbiota, even though microbiomes influence numerous host traits, including thermal tolerance. We combined field and lab experiments to understand the response of the slender anole lizard ( Anolis apletophallus ) gut microbiome to climatic shifts of various magnitude and duration. First, to examine the effects of long-term climate warming in the wild, we transplanted lizards from the mainland Panama to a series of warmer islands in the Panama Canal and compared their gut microbiome compositions after three generations of divergence. Next, we mimicked the effects of a short-term “heat-wave” by using a greenhouse experiment and explored the link between gut microbiome composition and lizard thermal physiology. Finally, we examined variation in gut microbiomes in our mainland population in the years both before and after a naturally occurring drought. Our results suggest that slender anole microbiomes are surprisingly resilient to short-term warming. However, both the taxonomic and predicted functional compositions of the gut microbiome varied by sampling year across all sites, suggesting that the drought may have had a regional effect. We provide evidence that short-term heat waves may not substantially affect the gut microbiota, while more sustained climate anomalies may have effects at broad geographic scales. IMPORTANCE As climate change progresses, it is crucial to understand how animals will respond to shifts in their local environments. One component of this response involves changes in the microbial communities living in and on host organisms. These “microbiomes” can affect many processes that contribute to host health and survival, yet few studies have measured changes in the microbiomes of wild organisms experiencing novel climatic conditions. We examined the effects of shifting climates on the gut microbiome of the slender anole lizard ( Anolis apletophallus ) by using a combination of field and laboratory studies, including transplants to warm islands in the Panama Canal. We found that slender anole microbiomes remain stable in response to short-term warming but may be sensitive to sustained climate anomalies, such as droughts. We discuss the significance of these findings for a species that is considered highly vulnerable to climate change. 

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