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1. Microbiota Perturbation or Elimination Can Inhibit Normal Development and Elicit a Starvation-Like Response in an Omnivorous Model Invertebrate

   https://doi.org/10.1128/mSystems.00802-21  

   Vera-Ponce de León, Arturo ; Jahnes, Benjamin C. ; Otero-Bravo, Alejandro ; Sabree, Zakee L. ( August 2021 , mSystems)

   Klassen, Jonathan L. (Ed.)

   ABSTRACT Omnivorous animals, including humans, harbor diverse, species-rich gut communities that impact their growth, development, and homeostasis. Model invertebrates are broadly accessible experimental platforms that enable linking specific species or species groups to host phenotypes, yet often their specialized diets and distinct gut microbiota make them less comparable to human and other mammalian and gut communities. The omnivorous cockroach Periplaneta americana harbors ∼4 × 10 2 bacterial genera within its digestive tract and is enriched with taxa commonly found in omnivorous mammals (i.e., Proteobacteria, Bacteroidetes , and Firmicutes ). These features make P. americana a valuable platform for identifying microbe-mediated host phenotypes with potential translations to mammals. Rearing P. americana insects under germfree conditions resulted in prolonging development time by ∼30% and an up to ∼8% reduction in body size along three dimensions. Germfree rearing resulted in downregulation of gene networks involved in growth, energy homeostasis, and nutrient availability. Reintroduction of a defined microbiota comprised of a subset of P. americana commensals to germfree insects did not recover normal growth and developmental phenotypes or transcriptional profiles observed in conventionally reared insects. These results are in contrast with specialist-feeding model insects (e.g., Drosophila ), where introduction of a single endemic bacterial species to germfree condition-reared specimens recovered normal host phenotypes. These data suggest that understanding microbe-mediated host outcomes in animals with species-rich communities should include models that typically maintain similarly diverse microbiomes. The dramatic transcriptional, developmental, and morphological phenotypes linked to gut microbiome status in this study illustrates how microbes are key players in animal growth and evolution. IMPORTANCE Broadly accessible model organisms are essential for illustrating how microbes are engaged in the growth, development, and evolution of animals. We report that germfree rearing of omnivorous Periplaneta americana cockroaches resulted in growth defects and severely disrupted gene networks that regulate development, which highlights the importance of gut microbiota in these host processes. Absence of gut microbiota elicited a starvation-like transcriptional response in which growth and development were inhibited while nutrient scavenging was enhanced. Additionally, reintroduction of a subset of cockroach gut bacterial commensals did not broadly recover normal expression patterns, illustrating that a particular microbiome composition may be necessary for normal host development. Invertebrate microbiota model systems that enable disentangling complex, species-rich communities are essential for linking microbial taxa to specific host phenotypes. 

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2. Protective microbiomes can limit the evolution of host pathogen defense

   https://doi.org/10.1002/evl3.140  

   Metcalf, C. Jessica E. ; Koskella, Britt ( October 2019 , Evolution Letters)

   The evolution of host immunity occurs in the context of the microbiome, but little theory exists to predict how resistance against pathogens might be influenced by the need to tolerate and regulate commensal microbiota. We present a general model to explore the optimal investment in host immunity under conditions in which the host can, versus cannot easily distinguish among commensal versus pathogenic bacteria, and when commensal microbiota can, versus cannot protect the host against the impacts of pathogen infection. We find that a loss of immune vigilance associated with innate immunity over evolutionary time can occur due to the challenge of discriminating between pathogenic and other microbe species. Further, we find the greater the protective effect of microbiome species, acting either directly or via competition with a pathogen, or the higher the costs of immunity, the more likely the loss of immune vigilance is. Conversely, this effect can be reversed when pathogens increase host mortality. Generally, the magnitude of costs of immunity required to allow evolution of decreased immune vigilance are predicted to be lowest when microbiome and pathogen species most resemble each other (in terms of host recognition), and when immune effects on the pathogen are weak. Our model framework makes explicit the core trade-offs likely to shape the evolution of immunity in the context of microbiome/pathogen discrimination. We discuss how this informs interpretation of patterns and process in natural systems, including vulnerability to pathogen emergence.

    

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3. Effect of urbanization and parasitism on the gut microbiota of Darwin's finch nestlings

   https://doi.org/10.1111/mec.17164  

   Solomon, Gabrielle ; Love, Ashley C. ; Vaziri, Grace J. ; Harvey, Johanna ; Verrett, Taylor ; Chernicky, Kiley ; Simons, Shelby ; Albert, Lauren ; Chaves, Jaime A. ; Knutie, Sarah A. ( October 2023 , Molecular Ecology)

   Host‐associated microbiota can be affected by factors related to environmental change, such as urbanization and invasive species. For example, urban areas often affect food availability for animals, which can change their gut microbiota. Invasive parasites can also influence microbiota through competition or indirectly through a change in the host immune response. These interacting factors can have complex effects on host fitness, but few studies have disentangled the relationship between urbanization and parasitism on an organism's gut microbiota. To address this gap in knowledge, we investigated the effects of urbanization and parasitism by the invasive avian vampire fly (Philornis downsi) on the gut microbiota of nestling small ground finches (Geospiza fuliginosa) on San Cristóbal Island, Galápagos. We conducted a factorial study in which we experimentally manipulated parasite presence in an urban and nonurban area. Faeces were then collected from nestlings to characterize the gut microbiota (i.e. bacterial diversity and community composition). Although we did not find an interactive effect of urbanization and parasitism on the microbiota, we did find main effects of each variable. We found that urban nestlings had lower bacterial diversity and different relative abundances of taxa compared to nonurban nestlings, which could be mediated by introduction of the microbiota of the food items or changes in host physiology. Additionally, parasitized nestlings had lower bacterial richness than nonparasitized nestlings, which could be mediated by a change in the immune system. Overall, this study advances our understanding of the complex effects of anthropogenic stressors on the gut microbiota of birds.

    

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4. Temperature dependence of parasitic infection and gut bacterial communities in bumble bees

   https://doi.org/10.1111/1462-2920.14805  

   Palmer‐Young, Evan C. ; Ngor, Lyna ; Burciaga Nevarez, Rodrigo ; Rothman, Jason A. ; Raffel, Thomas R. ; McFrederick, Quinn S. ( November 2019 , Environmental Microbiology)

   High temperatures (e.g., fever) and gut microbiota can both influence host resistance to infection. However, effects of temperature‐driven changes in gut microbiota on resistance to parasites remain unexplored. We examined the temperature dependence of infection and gut bacterial communities in bumble bees infected with the trypanosomatid parasiteCrithidia bombi. Infection intensity decreased by over 80% between 21 and 37°C. Temperatures of peak infection were lower than predicted based on parasite growthin vitro, consistent with mismatches in thermal performance curves of hosts, parasites and gut symbionts. Gut bacterial community size and composition exhibited slight but significant, non‐linear, and taxon‐specific responses to temperature. Abundance of total gut bacteria and of Orbaceae, both negatively correlated with infection in previous studies, were positively correlated with infection here. Prevalence of the bee pathogen‐containing family Enterobacteriaceae declined with temperature, suggesting that high temperature may confer protection against diverse gut pathogens. Our results indicate that resistance to infection reflects not only the temperature dependence of host and parasite performance, but also temperature‐dependent activity of gut bacteria. The thermal ecology of gut parasite‐symbiont interactions may be broadly relevant to infectious disease, both in ectothermic organisms that inhabit changing climates, and in endotherms that exhibit fever‐based immunity.

    

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5. Partitioning variance in immune traits in a zooplankton host—Fungal parasite system

   https://doi.org/10.1002/ece3.9640  

   Westphal, Grace H. ; Stewart Merrill, Tara E. ( December 2022 , Ecology and Evolution)

   Host immune traits arise from both genetic and environmental sources of variation. When immune traits have a strong genetic basis, the presence and severity of disease in a population may influence the distribution of those traits. Our study addressed how two immune‐related traits (gut penetrability and the hemocyte response) are shaped by genetic and environmental sources of variation, and how the presence of a virulent disease altered the relative frequency of these traits in natural populations.Daphnia dentiferahosts were sampled from five Indiana lakes between June and December 2017 before and during epidemics of their fungal pathogen,Metschnikowia bicuspidata. CollectedDaphniawere experimentally exposed toMetschnikowiaand assayed for their gut penetrability, hemocyte response, and multi‐locus genotype. Mixed‐effects models were constructed to partition variance in immune traits between genetic and environmental sources. We then isolated the genetic sources to produce genotype‐specific estimates of immune traits for each multi‐locus genotype. Finally, we assessed the relative frequency and dynamics of genotypes during epidemics and asked whether genotypes with more robust immune responses increased in frequency during epidemics. Although genotype was an important source of variation for both gut penetrability and the hemocyte response, environmental factors (e.g., resource availability,Metschnikowiaprevalence, and co‐infection) still explained a large portion of observed variation, suggesting a high degree of flexibility inDaphniaimmune traits. Additionally, no significant associations were detected between a genotype's immune traits and its frequency in a population. Our study highlights the power of variance partitioning in understanding the factors driving variation inDaphniatraits and motivates further research on immunological flexibility and the ecological drivers of immune variation.

    

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