Abstract

The gut microbiome is an integral part of a species' ecology, but we know little about how host characteristics impact its development in wild populations. Here, we explored the role of such intrinsic factors in shaping the gut microbiome of northern elephant seals (Mirounga angustirostris) during a critical developmental window of 6weeks after weaning, when the pups stay ashore without feeding. We found substantial sex differences in the early-life gut microbiome, even though males and females could not yet be distinguished morphologically. Sex and age both explained around 15% of the variation in gut microbial beta diversity, while microbial communities sampled from the same individual showed high levels of similarity across time, explaining another 40% of the variation. Only a small proportion of the variation in beta diversity was explained by health status, assessed by full blood counts, but clinically healthy individuals had a greater microbial alpha diversity than their clinically abnormal peers. Across the post-weaning period, the northern elephant seal gut microbiome was highly dynamic. We found evidence for several colonization and extinction events as well as a decline in Bacteroides and an increase in Prevotella, a pattern that has previously been associated with the transition from nursing to solid food. Lastly, we show that genetic relatedness was correlated with gut microbiome similarity in males but not females, again reflecting early sex differences. Our study represents a naturally diet-controlled and longitudinal investigation of how intrinsic factors shape the early gut microbiome in a species with extreme sex differences in morphology and life history.

Highlights

  • Vertebrates are inhabited by vast numbers of microbes that are increasingly emerging as key players in their host's biology and evolution (Bik et al, 2016; Ley et al, 2008; McFall-Ngai et al, 2013; Moeller et al, 2014)

  • We found that apparent sex differences in the alpha diversity of the gut microbiome were largely explained by a higher proportion of clinically healthy individuals in males than in females

  • Diet-controlled setting, we showed that gut microbiome composition is associated with host genetic relatedness in males and changes substantially within only a few weeks after the end of lactation, potentially anticipating the growing elephant seals' change in diet and lifestyle

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Summary

Introduction

Vertebrates are inhabited by vast numbers of microbes that are increasingly emerging as key players in their host's biology and evolution (Bik et al, 2016; Ley et al, 2008; McFall-Ngai et al, 2013; Moeller et al, 2014). The richest and arguably most complex microbial communities are those that populate the gastrointestinal tract and which are collectively termed the “gut microbiome.”. Gut microbes benefit their host in many ways, such as promoting the development of organs, assisting nutrient uptake, and priming and modulating the immune system (Cheesman, Neal, Mittge, Seredick, & Guillemin, 2011; Heijtz et al, 2011; Lathrop et al, 2011; Zhu, Wu, Dai, Zhang, & Wei, 2011). Relatively little is known about the composition, development and function of the gut microbiome in the wild, despite its potential to contribute to our fundamental understanding of the ecology and evolutionary biology of symbiotic relationships (Hird, 2017; Zilber-Rosenberg & Rosenberg, 2008)

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