Abstract
Despite the increasing knowledge on the processes involved in the acquisition and development of the gut microbiota in model organisms, the factors influencing early microbiota successions in natural populations remain poorly understood. In particular, little is known on the role of the rearing environment in the establishment of the gut microbiota in wild birds. Here, we examined the influence of the nesting environment on the gut microbiota of Great tits (Parus major) by performing a partial cross-fostering experiment during the intermediate stage of nestling development. We found that the cloacal microbiota of great tit nestlings underwent substantial changes between 8 and 15 days of age, with a strong decrease in diversity, an increase in the relative abundance of Firmicutes and a shift in the functional features of the community. Second, the nesting environment significantly influenced community composition, with a divergence among separated true siblings and a convergence among foster siblings. Third, larger shifts in both microbiota diversity and composition correlated with lower nestling body condition. Our results shed new light on the dynamics of microbial diversity during the ontogeny of avian hosts, indicating that the nest environment continues to shape the gut microbiota during the later stages of nestling development and that the increase in gut diversity between hatching and adulthood may not be as linear as previously suspected. Lastly, the microbiota changes incurred during this period may have implications for nestling body condition which can lead to long-term consequences for host fitness.
Highlights
The digestive tract of all vertebrates harbor microbial communities comprised of diverse bacterial taxa varying in abundance and functional traits (Zilber-Rosenberg and Rosenberg, 2008; McFallNgai et al, 2013)
Age had a major impact of cloacal diversity with significant decreases in operational taxonomic units (OTUs) richness (LogOTU, GLMM, F1,141 = 21.9, p < 0.0001; day 8 (D8): 50.51 ± 2.26 OTUs, day 15 (D15): 36.09 ± 1.92 OTUs), evenness (GLMM, F1,141 = 6.8, p < 0.0001), and Shannon index (GLMM, F1,141 = 59.7, p < 0.0001, Figure 1) between D8 and D15
D8 nestlings whereas those associated with carbohydrate and nucleotide metabolism were more abundant in D15 nestlings (Welch’s t-test, corrected p-value < 0.0001 for all above features, Figure 3 and Supplementary Figures S4, S5 for the other significantly different functional features)
Summary
The digestive tract of all vertebrates harbor microbial communities comprised of diverse bacterial taxa varying in abundance and functional traits (Zilber-Rosenberg and Rosenberg, 2008; McFallNgai et al, 2013). These gut microbiota play a fundamental role for host health and fitness, as they mediate processes such as digestion and nutrient synthesis (Cummings and Macfarlane, 1997), immunomodulation (Round and Mazmanian, 2009), and pathogen defense (Fukuda et al, 2011) and more widely influence life-history traits (Sison-Mangus et al, 2015) or even behavior (Ezenwa et al, 2012). After the first years of life, the maturation of the microbiota leads to an increase in stability, with adults hosting a well-established microbiota that is less sensitive to modifications (Kostic et al, 2013)
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