Dynamics of Gut Microbiota Diversity During the Early Development of an Avian Host: Evidence From a Cross-Foster Experiment

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.

Significant Differences in the Gut Bacterial Communities of Hooded Crane (Grus monacha) in Different Seasons at a Stopover Site on the Flyway

“…Reaction conditions were as follows: 94 • C for 5 min, 94 • C for 45 s × 35 cycles, 55 • C for 45 s, 45 s at 72 • C, and 10 min final extension at 72 • C. PCRs were performed in triplicate on two independent occasions. Negative and positive controls were assessed to ensure accuracy [6]. Mis-tagging was controlled using blank tag combinations [24].…”

“…Gut bacterial taxa play an important role in organismal health, including regulating digestion [1], nutrient uptake [2], fat metabolism [3], and vitamin synthesis [4]. A range of factors influence gut bacterial community composition and diversity, including diet [5], environment [6,7], and seasons [8]. However, the unique life cycle of birds, especially migratory birds, makes it interesting to study their gut bacterial community [9].…”

Evolutionary signal in the gut microbiomes of 74 bird species from Equatorial Guinea

“…Unsurprisingly, they also exhibit diversity in their microbiomes. Bird microbiomes appear to be dominated by a small number of bacterial phyla, namely Proteobacteria, Firmicutes, and Bacteroidetes (Grond, Sandercock, Jumpponen, & Zeglin, ; Hird et al, ; Waite & Taylor, ) and are influenced by environment (Wienemann et al, ), geographic location (Hird, Carstens, Cardiff, Dittmann, & Brumfield, ), diet (Rubio et al, ), age (Grond, Lanctot, Jumpponen, & Sandercock, ; Teyssier et al, ; Van Dongen et al, ), and host genetics (Kropáčková et al, ). Despite this, little is known about the role of the microbiome in avian evolution.…”

“…The nest, eggs, nestlings and parents form a complex and unique microbial network: nest building influences parental feather microbiome (Kilgas, Saag, Mägi, Tilgar, & Mänd, 2012) and nest materials influence eggshell microbiomes and nestling development (Jacob et al, 2015). Cross-fostering experiments show that the nest can significantly affect nestling microbiome (Teyssier, Lens, Matthysen, & White, 2018). Parental care by birds also regulates microbes: egg incubation influences bacterial pathogen load on eggs (Brandl et al, 2014); nestling faecal sacs are coated in a mucus that allows parents to easily remove nestling faeces and prevents contamination of the nest with harmful bacteria (Ibáñez-Álamo, Ruiz-Rodríguez, & Soler, 2014) and parental saliva (during feeding) can vertically transmit essential microbes to offspring (Kyle & Kyle, 2004).…”

Major shifts in gut microbiota during development and its relationship to growth in ostriches

“…In birds, studies examining age-related changes in gut microbial diversity are limited and show conflicting results, potentially due to differences in parental and environmental transmission of microbes across species (Dewar et al, 2017;Godoy-Vitorino et al, 2010;Grond, Lanctot, Jumpponen, & Sandercock, 2017;van Dongen et al, 2013;Yin et al, 2010). For example, older nestlings of great tits (Parus major) had lower cloacal microbial diversity than younger nestlings (Teyssier, Lens, Matthysen, & White, 2018), while the opposite was found in tree swallows (Tachycineta bicolor; Mills, Lombardo, & Thorpe, 1999), and in house sparrows (Passer domesticus) age did not have any effect on microbial diversity or community structure (Kohl, Brun, Caviedes-Vidal, & Karasov, 2019). In turkeys (Meleagris gallopavo) it has been found that gut microbial diversity initially increases and then subsequently decreases during development (Danzeisen et al, 2015;Wilkinson et al, 2017), while in chickens (Gallus gallus) there is often a successional increase in diversity with age (Ballou et al, 2016;Lu et al, 2003;Oakley et al, 2014;van der Wielen, Keuzenkamp, Lipman, van Knapen, & Biesterveld, 2002).…”