Flexibility and resilience of Great tit (Parus major) gut microbiomes to changing diets

Abstract

Background: Gut microbial communities play important roles in nutrient management and can change in response to host diets. The extent of this flexibility and the concomitant resilience is largely unknown in wild animals. To begin untangling the dynamics of avian-gut microbiome symbiosis associated with diet changes, we exposed Parus major (Great tits) fed with a standard diet (seeds and mealworms) to either a mixed (seeds, mealworms and fruits), a seed, or a mealworm diet for four weeks, and examined the flexibility of gut microbiomes to these compositionally different diets. To assess microbiome resilience (recovery potential), all individuals were subsequently reversed to a standard diet for another four weeks. Cloacal microbiomes were collected weekly and characterised through sequencing the v4 region of the 16S rRNA gene using Illumina MiSeq. Results: Initial microbiomes changed significantly with the diet manipulation but the communities did not differ significantly between the three diet groups (mixed, seed and mealworm), despite multiple diet-specific changes of specific bacterial genera. Reverting birds to the standard diet led to only a partial recovery in gut community compositions. The majority of the bacterial taxa that increased significantly during diet manipulation decreased in relative abundances after reversion to the standard diet; however, bacterial taxa that decreased during the manipulation rarely increased after diet reversal.Conclusions: The gut microbial response and partial resilience to dietary changes support that gut bacterial communities of P. major play a role in accommodating dietary changes experienced by wild avian hosts. This may be a contributing factor to the relaxed association between microbiome composition and bird phylogeny. Our findings further imply that interpretations of wild bird gut microbiome analyses from single-time point sampling, especially for omnivorous species or species that have changing seasonal diets, should be done with caution. The partial community recovery implies that ecologically relevant diet changes (e.g., seasonality and migration) open up gut niches that may be filled by previously abundant microbes or replaced by different symbiont lineages, which has important implications for the integrity and specificity of long-term avian-symbiont associations.

Habitat shapes diversity of gut microbiomes in a wild population of blue tits Cyanistes caeruleus

“…In general, the link between withinspecies/genus diet differences and microbiome is already well established in the literature (Davidson et al 2019, Loo et al 2019. Experimental manipulation of great tit diets by shifting them into more insect-larvae-based led to an increase in the proportion of Firmicutes and a drop in the proportion of Proteobacteria in bird microbiomes (Bodawatta et al 2020b) -a trend seen in our study in the case of deciduous forest birds. Also, a comparative study of several insectivorous and omnivorous species indicated that insectivorous species tended to have more Gammaproteobacteria and Enterobacteriaceae than omnivorous taxa.…”

“…We predicted that in our study system, younger individuals would be characterized by less diverse microbiomes than older (reflecting microbiome development and maturation), that sexes should have similar microbiome profiles (as sexes in blue tits have similar mobility, exploratory behaviour and diet) and finally, that birds from richer deciduous forest habitats would significantly differ in terms of microbiome complexity and composition from birds from more open, forest-meadow habitats. We also expected that blue tit microbiomes will be similar to those of the closely related great tits (which are composed mostly of Firmicutes and Proteobacteria (Kropáčková et al 2017, Teyssier et al 2018, Davidson et al 2019, Bodawatta et al 2020b, contrary to many scavenging and omnivorous species, where other bacteria phyla such as Bacteroidetes, Tenericutes and Actinobcateria dominate (Bodawatta et al 2018, Wu et al 2018).…”

Habitat shapes diversity of gut microbiomes in a wild population of blue tits (Cyanistes caeruleus)

“…In general, the link between within-species/genus diet differences is already well established in the literature (Davidson et al, 2019;Loo et al, 2019). Experimental manipulation of great tit diets by shifting them into more insect-larvae based led to an increase in the proportion of Firmicutes and drop in the proportion of Proteobacteria in bird microbiomes (Bodawatta et al, 2020) -a trend seen in our study in case of deciduous forest birds. Also, a comparative study of several insectivorous and omnivorous species indicated that insectivorous species tended to have more Gammaproteobacteria and Enterobacteriaceae than omnivorous taxa.…”

“…We predicted, that in our study system younger individuals would be characterised by less diverse microbiomes than older (reflecting microbiome development and maturation), that sexes should have similar microbiome profiles (as sexes in blue tits have similar mobility, exploratory behaviour and diet), and finally -that birds from richer forest habitats would significantly differ in terms of microbiome complexity and composition from birds from more open, meadow habitats. We also expected, that blue tit microbiomes will be similar to those of the closely related great tits (which are composed mostly of Firmicutes and Proteobacteria (Kropáčková et al, 2017;Davidson et al, 2019;Bodawatta et al, 2020), contrary to many scavenging and omnivorous species, where other bacteria phyla, such as Bacteroidetes, Tenericutes and Actinobcateria dominate (Bodawatta et al, 2018;Wu et al, 2018)).…”

Gut microbiome disturbances of altricial Blue and Great tit nestlings are countered by continuous microbial inoculations from parental microbiomes

“…5C). The smaller core microbiomes in adults could be driven by environmental and dietary impacts on microbial variation and/or that fewer adults were examined than chicks [18, 70]. Despite small core microbiomes, chicks shared more core taxa with females (BT: 3 ASVs and GT: 5 ASVs) than males (1 ASV in both BT and GT) (Fig.…”