Primate microbiomes over time: Longitudinal answers to standing questions in microbiome research

Abstract

To date, most insights into the processes shaping vertebrate gut microbiomes have emerged from studies with cross-sectional designs. While this approach has been valuable, emerging time series analyses on vertebrate gut microbiomes show that gut microbial composition can change rapidly from 1 day to the next, with consequences for host physical functioning, health, and fitness. Hence, the next frontier of microbiome research will require longitudinal perspectives. Here we argue that primatologists, with their traditional focus on tracking the lives of individual animals and familiarity with longitudinal fecal sampling, are well positioned to conduct research at the forefront of gut microbiome dynamics. We begin by reviewing some of the most important ecological processes governing microbiome change over time, and briefly summarizing statistical challenges and approaches to microbiome time series analysis. We then introduce five questions of general interest to microbiome science where we think fieldbased primate studies are especially well positioned to fill major gaps: (a) Do early life events shape gut microbiome composition in adulthood? (b) Do shifting social landscapes cause gut microbial change? (c) Are gut microbiome phenotypes heritable across variable environments? (d) Does the gut microbiome show signs of host aging? And (e) do gut microbiome composition and dynamics predict host health and fitness?For all of these questions, we highlight areas where primatologists are uniquely positioned to make substantial contributions. We review preliminary evidence, discuss possible study designs, and suggest future directions. Research Highlights• To date nearly all insights into the processes shaping vertebrate gut microbiomes have emerged from studies that have cross-sectional designs, but emerging time series analyses show that gut microbiomes can change rapidly from 1 day to the next.• Field-based primate studies, owing to their focus on the lives of individual animals, and the relative ease of collecting longitudinal fecal samples from known animals, are better positioned to collect these data than studies of humans or other species.• We propose five questions of general interest to microbiome science where fieldbased primate studies are especially well positioned to fill major gaps. We review preliminary evidence, discuss possible study designs, and suggest future directions.Am J Primatol. 2019;81:e22970.wileyonlinelibrary.com/journal/ajp

Temporal Dynamics of Cloacal Microbiota in Adult Laying Chickens With and Without Access to an Outdoor Range

“…Here, we studied the effect of temporal changes in a secondary environment in adult layers (i.e., indoor or outdoor range), where the effect of the outdoor range was likely dampened by the adults’ host homeostatic responses. As an animal host ages, its influence on microbial selection in the development of the intestinal microbiota increases ( Björk et al, 2019 ). Indeed, layers above the age of 25 weeks ( Ngunjiri et al, 2019 ) or 28 weeks ( Videnska et al, 2014 ) reach an adult microbial equilibrium ( Videnska et al, 2014 ).…”

“…Changes in the chickens’ microbiota have been linked to many factors ( Kers et al, 2018 ), including host related factors such as age ( Cox et al, 2014 ; Videnska et al, 2014 ; Jurburg et al, 2019 ; Ngunjiri et al, 2019 ) and breed ( Schokker et al, 2015 ; Richards et al, 2019 ). Outside of the host, differences in climate, soil, litter, and feed affect the host’s exposure to other microbes, which may colonize the animal’s intestinal tract ( Björk et al, 2019 ). Indeed, under controlled settings, housing conditions have been found to modulate the chickens’ microbiota ( Hubert et al, 2019 ; Kers et al, 2019 ).…”

“…However, adult chickens have fully developed microbiota, which are more stable than microbial communities of young layers ( Videnska et al, 2014 ; Ngunjiri et al, 2019 ). It has been proposed that as an animal ages, the host’s influence on microbial selection increases due to physiochemical maturation of the gut and the ability of the host to curate its microbiota ( Björk et al, 2019 ), likely making the microbiota of adult layers less prone to external perturbations or changes ( Schreuder et al, 2019 ).…”

Interactions between social groups of colobus monkeys (Colobus vellerosus) explain similarities in their gut microbiomes

“…The divergence in gut microbiomes with home range separation could potentially be due to dietary differences, lower degrees of relatedness, or lack of shared social environments Björk, Dasari, Grieneisen, & Archie, 2019). Diet is suggested to be one of the most important factors affecting the gut microbiome (Voreades, Kozil, & Weir, 2014).…”

Long-term storage of feces at −80 °C versus −20 °C is negligible for 16S rRNA amplicon profiling of the equine bacterial microbiome

“…In addition to general relevance, our findings are especially pertinent to clinicians and researchers conducting field or community-based studies where access to −80 °C storage is limited or absent. Wider adoption and acceptance of storage at −20 °C for amplicon-based microbiome research should greatly increase total storage space, encourage the re-use of samples, and promote longitudinal sampling ( Björk et al, 2019 ). Increased reliance on −20 °C freezers, at least for storage up to a few years, may also help reduce drop-out rates in microbiome studies by alleviating the logistical burden of rapidly transferring samples to −80 °C ( Vandeputte et al, 2017 ).…”