Abstract
Studies in multiple host species have shown that gut microbial diversity and composition change during pregnancy and lactation. However, the specific mechanisms underlying these shifts are not well understood. Here, we use longitudinal data from wild Phayre’s leaf monkeys to test the hypothesis that fluctuations in reproductive hormone concentrations contribute to gut microbial shifts during pregnancy. We described the microbial taxonomic composition of 91 fecal samples from 15 females (n = 16 cycling, n = 36 pregnant, n = 39 lactating) using 16S rRNA gene amplicon sequencing and assessed whether the resulting data were better explained by overall reproductive stage or by fecal estrogen (fE) and progesterone (fP) concentrations. Our results indicate that while overall reproductive stage affected gut microbiome composition, the observed patterns were driven by reproductive hormones. Females had lower gut microbial diversity during pregnancy and fP concentrations were negatively correlated with diversity. Additionally, fP concentrations predicted both unweighted and weighted UniFrac distances, while reproductive state only predicted unweighted UniFrac distances. Seasonality (rainfall and periods of phytoprogestin consumption) additionally influenced gut microbial diversity and composition. Our results indicate that reproductive hormones, specifically progestagens, contribute to the shifts in the gut microbiome during pregnancy and lactation.
Highlights
The gut microbiome interacts closely with host physiological processes, including growth, metabolism, and immunity[1]
Building on existing research on the reproductive endocrinology of this population, we examined how the composition of the gut microbiome varied across reproductive stages and tested whether observed patterns were associated with differences in fecal estrogen and progestagen concentrations
This study examined how gut microbiome composition varied across reproductive stages in Phayre’s leaf monkeys and whether this variation was correlated with fecal hormone concentrations
Summary
The gut microbiome interacts closely with host physiological processes, including growth, metabolism, and immunity[1]. Because many of these processes dynamically change in response to reproduction, alterations in the female gut microbiome are expected across reproductive stages In support of this expectation, shifts in gut microbial diversity and composition during pregnancy and lactation have been reported in a number of vertebrates[2,3,4,5], including humans[6,7,8] and nonhuman primates[9,10]. Reproductive hormones - including progestagens and estrogens - orchestrate a number of physiological changes during pregnancy, including alterations in inflammatory immune responses, as well as changes in maternal metabolism and cardiovascular function[15] These hormones are likely candidates for mediating changes in the gut microbiome. Few studies have simultaneously measured reproductive hormone concentrations and gut microbial community composition across cycling, pregnant, and lactating individuals[5] Knowledge of these interactions is critical for our understanding of host physiology, health, ecology and evolution. We hypothesized that variations in reproductive hormone concentrations would better predict shifts in the gut microbiome than coarse categories of reproductive state (cycling, pregnant, lactating) in adult female Phayre’s leaf monkeys
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