A time-lagged association between the gut microbiome, nestling weight and nestling survival in wild great tits

Abstract

1. Natal body mass is a key predictor of viability and fitness in many animals. While variation in body mass and therefore viability of juveniles may be explained by genetic and environmental factors, emerging evidence points to the gut microbiota as an important factor influencing host health. The gut microbiota is known to change during development, but it remains unclear whether the microbiome predicts fitness, and if it does, at which developmental stage it affects fitness traits. 2. We collected data on two traits associated with fitness in wild nestling great tits (Parus major): weight and survival to fledging. We characterised the gut microbiome using 16S rRNA sequencing from nestling faeces and investigated temporal associations between the gut microbiome and fitness traits across development at day 8 (D8) and day 15 (D15) post-hatching. We also explored whether particular microbial taxa were indicator species that reflected whether nestlings survived or not. 3. There was no link between mass and microbial diversity on D8 or D15. However, we detected a time-lagged relationship whereby the microbial diversity at D8 was negatively associated with weight at D15, while controlling for weight at D8, therefore reflecting weight gain over the intervening period. Indicator species analysis revealed that while several taxa were unique to birds that either survived or did not survive, there were no universal taxa that were consistently found across all birds within either survival group. This suggests that the presence of particular bacterial taxa may be sufficient, but not necessary for determining future survival, perhaps owing to functional overlap in microbiota. 4. We highlight that measuring microbiome-fitness relationships at just one time point may be misleading, especially early in life. Instead, microbial-host fitness effects should be investigated longitudinally as there may be critical development windows in which key microbiota are established and prime host traits associated with nestling growth. Pinpointing which features of the gut microbial community impact on host fitness, and when during development this occurs, will shed light on population level processes and has the potential to support conservation.

Early life gut microbiome dynamics mediate maternal effects on infant growth in vervet monkeys

“…In support of this hypothesis, low alpha diversity at T1 predicted greater body mass at T3 in vervets, independent of maternal parity. These results are in line with studies on birds showing an association between reduced early life alpha diversity on future weight gain [23,24].…”

“…In humans and rodent models, reduced alpha diversity has been associated with growth deficits [20]; however, the effects have not been consistent, with other studies finding no relationship between microbial community diversity and growth [21]. In other animals, such as birds, the effects appear more consistent and with an opposite pattern: poultry birds with experimentally-reduced alpha diversity grew faster [22], and lower diversity during early life predicts faster later-life growth among free-living birds [23,24]. Beyond community diversity, experimental rodent models of the human microbiome have identified specific taxa are causally related to infant growth.…”

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

“…At the genus level, the dominant bacteria noted in this study were also identified as highly prevalent in our population (Ureaplasma, Chryseobacterium, Carnobacterium). Similar microbiome compositions were reported for great tits in several other studies (Davidson et al, 2019(Davidson et al, , 2020, but population differences may paly role to some extent (e.g., Teyssier et al (2018) reported great tit microbiomes dominated by Firmicutes and Actinobacteria, with only small prevalence of Proteobacteria; notably, their analyses were done on fledglings, contrary to our study and other cited studies which used at least 1-year old adults). Blue tit microbiomes do significantly differ from microbiomes of other bird species (e.g., Darwin's finchesdomination of Firmicutes and Actinobacteria (Loo et al, 2019); swan geese -domination of Firmicutes (Wu et al, 2018); white ibises -domination of Firmicutes (Murray et al, 2020); great bastards -domination of Firmicutes and Bacteroidetes (Liu et al, 2020)), which may reflect general differences due to different dietary niches (Waite & Taylor, 2015;Grond et al, 2018).…”

A time‐lagged association between the gut microbiome, nestling weight and nestling survival in wild great tits

“…Our metadata is deposited at Dryad https://doi.org/10.5061/dryad.bk3j9kd9g (Davidson, Somers, et al, 2020). Sequence data are available in the European Nucleotide Archive under access number PRJEB42330, and ERS5506097 ‐ ERS5506338.…”