Shades of Grey: Host Phenotype Dependent Effect of Urbanization on the Bacterial Microbiome of a Wild Mammal

Abstract

Background Host-associated microbiota are integral to the ecology of their host and may help wildlife species cope with rapid environmental change. Urbanization is a globally replicated form of severe environmental change which we can leverage to better understand wildlife microbiomes. Does the colonization of separate cities result in parallel changes in the intestinal microbiome of wildlife, and if so, does within-city habitat heterogeneity matter? Using 16S rRNA gene amplicon sequencing, we quantified the effect of urbanization on the microbiome of eastern grey squirrels (Sciurus carolinensis). Eastern grey squirrels are ubiquitous in rural and urban environments throughout their native range, across which they display an apparent coat colour polymorphism (agouti, black, intermediate). Results Grey squirrel microbiomes differed between rural and city environments; however, comparable variation was explained by habitat heterogeneity within cities. Our analyses suggest that operational taxonomic unit (OTU) community structure was more strongly influenced by local environmental conditions (rural and city forests versus human built habitats) than urbanization of the broader landscape (city versus rural). The bacterial genera characterizing the microbiomes of built-environment squirrels are thought to specialize on host-derived products and have been linked in previous research to low fibre diets. However, despite an effect of urbanization at fine spatial scales, phylogenetic patterns in the microbiome were coat colour phenotype dependent. City and built environment agouti squirrels displayed greater phylogenetic beta-dispersion than those in rural or forest environments, and null modelling results indicated that the phylogenetic structure of urban agouti squirrels did not differ greatly from stochastic expectations. Conclusions Habitat heterogeneity at fine spatial scales affects host-associated microbiomes, however, we found little evidence that this pattern was the result of similar selective pressures acting on the microbiome within environments. Further, this result, those of phylogeny-independent analyses, and patterns of beta-dispersion lead us to suggest that microbiota dispersal and ecological drift are integral to shaping the inter-environmental differences we observed. These patterns were partly mediated by squirrel coat colour phenotype. Given a well-known urban cline in squirrel coat colour melanism, grey squirrels provide a useful free-living system with which to study how host genetics mediate environment x microbiome interactions.

Parallel evolution of urban–rural clines in melanism in a widespread mammal

“…including mechanisms involving correlated traits 25 . For example, melanic squirrels have less phylogenetically variable microbiomes than the gray morph in cities 26 . A more complete picture of the selective mechanisms driving urban-rural clines will require linking trait variation to fitness differences between squirrel color morphs in urban and rural areas.…”

Parallel evolution of urban-rural clines in melanism in a widespread mammal

“…Additional selective mechanisms may play a role in maintaining urban melanism (e.g., parasite pressure, pollution) 24 , including mechanisms involving correlated traits 25 . For example, melanic squirrels have less phylogenetically variable microbiomes than the gray morph in cities 26 . A more complete picture of the selective mechanisms driving urban-rural clines will require linking trait variation to fitness differences between squirrel color morphs in urban and rural areas.…”