It's what's on the inside that counts: stress physiology and the bacterial microbiome of a wild urban mammal

Abstract

The microbiome's capacity to shape the host phenotype and its mutability underlie theorization that the microbiome might facilitate host acclimation to rapid environmental change. However, when environmental change occurs, it is unclear whether resultant microbiome restructuring is proximately driven by this changing external environment or by the host's physiological response to this change. We leveraged urbanization to compare the ability of host environment (urban or forest) versus multi-scale biological measures of host hypothalamic–pituitary–adrenal (HPA) axis physiology (neutrophil : lymphocyte ratio, faecal glucocorticoid metabolites, hair cortisol) to explain variation in the eastern grey squirrel ( Sciurus carolinensis ) faecal microbiome. Urban and forest squirrels differed across all three of the interpretations of HPA axis activity we measured. Direct consideration of these physiological measures better explained greater phylogenetic turnover between squirrels than environment. This pattern was strongly driven by trade-offs between bacteria which specialize on metabolizing digesta versus host-derived nutrient sources. Drawing on ecological theory to explain patterns in intestinal bacterial communities, we conclude that although environmental change can affect the microbiome, it might primarily do so indirectly by altering host physiology. We demonstrate that the inclusion and careful consideration of dynamic, rather than fixed (e.g. sex), dimensions of host physiology are essential for the study of host–microbe symbioses at the micro-evolutionary scale.

Into the wild: microbiome transplant studies need broader ecological reality

“…Yet, these interrelated processes across scales are inherent in host-microbiome relationships (e.g. [34]), and thus further integration of ecology, evolution and physiology with microbiology will be crucial for unlocking important insights about the interactions between hosts and Box 2. Ecological reasoning for each experimental condition within a transplant.…”

Application of ecological and evolutionary theory to microbiome community dynamics across systems

“…Such advances require the development of theoretical and conceptual frameworks such as those discussed in §3 to drive hypothesis generation and predictions that can be tested through the careful design of empirical studies. The field of microbiome research therefore transcends disciplines, as exemplified by the diversity of methodological and analytical approaches described in the contributions to the special feature, including mathematical modelling [9,[16][17][18], DNA and RNA sequencing [7,10,14,18], flow cytometry [14], infection tests in model and non-model pathosystems [7,18], physico-chemical and volatile analysis [7], and measures of hormone activity to assess host physiological responses to its environment [10]. A major theme pervading this special feature is the link between mathematical model simulations and empirical studies [9,11,16,17].…”

“…Links between the microbiome and host phenotype influence how hosts might respond to environmental change and stress, especially in terms of how quickly the host can alter its physiology. Stothart et al [10] tested this idea by comparing the gut microbiomes of eastern grey squirrels in urban versus forest environments. They find that, although environment itself is important, variation in the microbiome is more strongly explained by measures of the hypothalamicpituitary-adrenal hormonal system, which is indicative of recent stress in the host.…”

“…Changes in a host's environment may also influence its microbiome; however, a key question in microbiome research is whether microbiome restructuring is driven predominantly by the external environment changes, or the host's physiological response to this change. Stothart et al [10] test this hypothesis in by analysing the impact of urbanization on grey squirrel populations, suggesting that impacts of environmental change on the microbiome occur indirectly through altered effects on host physiology. Perry et al [21] provide an insightful discussion of the deterministic forces that drive microbiome dynamics and function in sustainable teleost aquaculture and highlight research gaps and future opportunities for microbiome manipulation.…”

Into the wild: microbiome transplant studies need broader ecological reality

“…Yet, these interrelated processes across scales are inherent in host-microbiome relationships (e.g. Stothart et al (34)), and thus further integration of ecology, evolution, and physiology with microbiology will be crucial for unlocking important insights about the interactions between hosts and their microbiome. As microbiome research expands further to include ecological processes that are well established in traditional ecosystems, studies that can capture these processes will be necessary.…”