Effects of past and present habitat on the gut microbiota of a wild rodent

Abstract

The response of the gut microbiota to changes in the host environment can be influenced by both the host's past and present habitats. To quantify their contributions for two different life stages, we studied the gut microbiota of wild bank voles (Clethrionomys glareolus) by performing a reciprocal transfer experiment with adults and their newborn offspring between urban and rural forests in a boreal ecosystem. Here, we show that the post-transfer gut microbiota in adults did not shift to resemble the post-transfer gut microbiota of animals 'native' to the present habitat. Instead, their gut microbiota appear to be structured by both their past and present habitat, with some features of the adult gut microbiota still determined by the past living environment (e.g. alpha diversity, compositional turnover). By contrast, we did not find evidence of the maternal past habitat (maternal effects) affecting the post-transfer gut microbiota of the juvenile offspring, and only a weak effect of the present habitat. Our results show that both the contemporary living environment and the past environment of the host organism can structure the gut microbiota communities, especially in adult individuals. These data are relevant for decision-making in the field of conservation and wildlife translocations.

Keywords: flexibility; gut microbiota; reciprocal transfer experiment; resistance; translocation; urban.

Figure 1.

Experimental design of the reciprocal transfer (RT) experiment on wild bank voles. The experiment was carried out in Jyväskylä, situated in central Finland (a) and used 20 urban and 20 rural forest sites around the city (pink areas represent urban zones) as experimental forest patches (b). The schematic overview of the reciprocal transfer experiment shows that wild gravid bank voles were sourced from urban and rural forests (referred to as 'past habitat') and released in a new urban or rural forest patch (referred to as 'present habitat') with their newborn offspring (c). Data from pre-transfer gut microbiota are based on faecal samples derived from bank voles upon initial capture, while the post-transfer microbiota were obtained from animals after spending four weeks in their new forest patch after translocation.

Figure 2.

Change in the alpha diversity of the gut microbiota of bank voles in terms of past habitat. The alpha diversity (ASV richness) of the post-transfer gut microbiota was significantly higher for animals that originated from urban forests in comparison with rural forests, irrespective of their site of translocation (a). Connected bar plots show the increase or decrease in alpha diversity in the gut microbiota (paired-differences in alpha diversity) for each individual bank vole between their pre-transfer and post-transfer gut microbiota. Bank voles originating from rural (b) and urban (c) forests are shown in separate plots. The asterisk corresponds to a significant p-value (*p < 0.05).

Figure 3.

Post-transfer gut microbiota compositions of bank voles in terms of past and present habitat. The ordination plots for adults (a) and juvenile offspring (b) are based upon the Bray–Curtis metric while the R² values and statistical significance values for adults (c) and juvenile offspring (d) are based upon the output from adonis2 tests. Overall, the plots show that clustering of the adult post-transfer gut microbiota occurs according to the past and present habitat (p < 0.05) while the juvenile post-transfer gut microbiota has no significant influence from either. However, there is a trend towards clustering according to the present habitat. The asterisk corresponds to a significant p-value (*p < 0.05). CAP, constrained analysis of principal coordinates.