Maternal effects shape scale-dependent convergence in gut microbial responses to environmental change

Abstract

Animals can experience environmental variability across multiple temporal scales, from predictable within-year seasonal fluctuations to rarer, irregular resource pulses that occur across generations. While gut microbiome responses to seasonal changes are well documented, far less is understood about how host-associated microbiomes respond to episodic environmental resource pulses, and whether such responses can persist across generations. Here, we investigate how gut microbial communities of wild North American red squirrels (Tamiasciurus hudsonicus) respond to intra-annual seasonal variation and episodic resource pulses happening years apart (specifically, seed masting). We then test the hypothesis that these responses are shared by mothers and their offspring. In line with prior work across mammals, we found that seasonal variation strongly structured gut microbiomes, driving widespread and convergent shifts in composition across the year. However, episodic resource pulses predicted microbial scatter such that gut microbiomes became more dissimilar across individuals in resource pulse years compared to typical years. Despite this population-level divergence, mothers and their adult offspring exhibited microbial convergence when encountering resource pulses occurring years apart, whereas seasonal responses were shared across the population and not unique to mother-offspring pairs. Overall, our results highlight the mammalian gut microbiome as a flexible component of the host phenotype, capable of adjusting to both predictable seasonal variation and large-scale, episodic resource pulses. Patterns of mother-offspring similarity across resource pulse years further provide evidence that some host-microbial responses to environmental change may be transmitted across generations.