Mammals show distinct functional gut microbiome dynamics to identical series of environmental stressors.

IMPORTANCE: In our manuscript, we report the first interspecific comparative study about the plasticity of the gut microbiota. We conducted a captivity experiment that exposed wild-captured mammals to a series of environmental challenges over 45 days. We characterized their gut microbial communities using genome-resolved metagenomics and modeled how the taxonomic, phylogenetic, and functional microbial dynamics varied across a series of disturbances in both species. Our results indicate that the intrinsic properties (e.g., diversity and functional redundancy) of microbial communities coupled with physiological attributes (e.g., thermal plasticity) of hosts shape the taxonomic, phylogenetic, and functional response of gut microbiomes to environmental stressors, which might influence their contribution to the acclimation and adaptation capacity of animal hosts.

Enriching captivity conditions with natural elements does not prevent the loss of wild-like gut microbiota but shapes its compositional variation in two small mammals.

As continued growth in gut microbiota studies in captive and model animals elucidates the importance of their role in host biology, further pursuit of how to retain a wild-like microbial community is becoming increasingly important to obtain representative results from captive animals. In this study, we assessed how the gut microbiota of two wild-caught small mammals, namely Crocidura russula (Eulipotyphla, insectivore) and Apodemus sylvaticus (Rodentia, omnivore), changed when bringing them into captivity. We analyzed fecal samples of 15 A. sylvaticus and 21 C. russula, immediately after bringing them into captivity and 5 weeks later, spread over two housing treatments: a "natural" setup enriched with elements freshly collected from nature and a "laboratory" setup with sterile artificial elements. Through sequencing of the V3-V4 region of the 16S recombinant RNA gene, we found that the initial microbial diversity dropped during captivity in both species, regardless of treatment. Community composition underwent a change of similar magnitude in both species and under both treatments. However, we did observe that the temporal development of the gut microbiome took different trajectories (i.e., changed in different directions) under different treatments, particularly in C. russula, suggesting that C. russula may be more susceptible to environmental change. The results of this experiment do not support the use of microbially enriched environments to retain wild-like microbial diversities and compositions, yet show that specific housing conditions can significantly affect the drift of microbial communities under captivity.

Maladaptive plasticity facilitates evolution of thermal tolerance during an experimental range shift.

BACKGROUND: Many organisms are responding to climate change with dramatic range shifts, involving plastic and genetic changes to cope with novel climate regimes found at higher latitudes. Using experimental lineages of the seed beetle Callosobruchus maculatus, we simulated the initial phase of colonisation to progressively cooler and/or more variable conditions, to investigate how adaptation and phenotypic plasticity contribute to shifts in thermal tolerance during colonisation of novel climates. RESULTS: We show that heat and cold tolerance rapidly evolve during the initial stages of adaptation to progressively cooler and more variable climates. The evolved shift in cold tolerance is, however, associated with maladaptive plasticity under the novel conditions, resulting in a pattern of countergradient variation between the ancestral and novel, fluctuating thermal environment. In contrast, lineages exposed to progressively cooler, but constant, temperatures over several generations expressed only beneficial plasticity in cold tolerances and no evolved response. CONCLUSIONS: We propose that thermal adaptation during a range expansion to novel, more variable climates found at high latitudes and elevations may typically involve genetic compensation arising from maladaptive plasticity in the initial stages of adaptation, and that this form of (countergradient) thermal adaptation may represent an opportunity for more rapid and labile evolutionary change in thermal tolerances than via classic genetic assimilation models for thermal tolerance evolution (i.e., selection on existing reaction norms). Moreover, countergradient variation in thermal tolerances may typically mask cryptic genetic variability for these traits, resulting in apparent evolutionary stasis in thermal traits.