Early sexual dimorphism in the developing gut microbiome of northern elephant seals

Abstract

34The gut microbiome is an integral part of a species' ecology, but we know little about how host characteristics 35 impact its development in wild populations. Here, we explored the role of such intrinsic factors in shaping the gut 36 microbiome of northern elephant seals during a critical developmental window of six weeks after weaning, when 37 the pups stay ashore without feeding. We show that the early-life gut microbiome is already substantially different 38 in male and female pups, even though males and females cannot yet be distinguished morphologically. Sex and 39 age both explain around 15% of the variation in gut microbial beta diversity, while microbial communities sampled 40 from the same individual show high levels of similarity across time, explaining another 40% of the variation. Only 41 a small proportion of the variation in beta diversity is explained by health status, but healthy individuals have a 42 greater microbial alpha diversity than their non-healthy peers. Across the post-weaning period, the elephant seal 43 gut microbiome is highly dynamic. We found evidence for several colonisation and extinction events as well as a 44 decline in Bacteriodes and an increase in Prevotella, a pattern that has previously been associated with the 45 transition from nursing to solid food. Lastly, we show that genetic relatedness is correlated with gut microbiome 46 similarity in males but not females, again reflecting substantial early sex-differences. Our study represents a 47 naturally diet-controlled and longitudinal investigation of how intrinsic factors shape the early gut microbiome in 48 a species with extreme sex differences in morphology and life history. 49 50 51 promoting the development of organs, assisting nutrient uptake and priming and modulating the immune system 57

Patterns of the fecal microbiota in the Juan Fernández fur seal (Arctocephalus philippii)

“…Cluster 2 shows patterns similar to those observed in females. It seems that the microbial community diverges early in life based on sex as reported in northern elephant seal pups under a naturally controlled diet (Stoffel et al, 2020). Sexual dimorphism is a common mating strategy in otariids.…”

“…For example, following its initial acquisition during birth and lactation, the microbiome is constantly modified by factors such as age, sex, and diet (Ley et al, 2008a, 2008b; Nicholson et al, 2012). Similar factors shaping the gut microbiome in terrestrial mammals influence that of marine mammals (Nelson et al, 2013; Pacheco‐Sandoval et al, 2019; Smith et al, 2013; Stoffel et al, 2020). However, studies have also shown substantial differences between marine and terrestrial mammal gut microbiomes, even when these two groups share a similar diet (e.g., herbivore, carnivore) (Bik et al, 2016; Nelson et al, 2013).…”

Gut microbiome composition, not alpha diversity, is associated with survival in a natural vertebrate population

“…Previous studies investigating the relationship between GM alpha diversity and individual condition have shown mixed results, with both positive [23,31,77] and negative [32,33,78] relationships, as well the absence of an association [79,80] being identified across various wild and captive vertebrate host species. However, these studies often focus on early life stages, despite the fact that body mass can be an important predictor of fitness in adult individuals [63,81,82].…”

“…The emergence of high-throughput sequencing technologies, in combination with the development of effective, non-invasive sampling techniques, has resulted in a recent proliferation of studies investigating the GM of wild animals. Several studies have demonstrated interspecific differences in GM characteristics [17][18][19], and also variation between groups [20][21][22] or individuals [23][24][25] within the same natural population. Most of these studies have focussed on investigating the drivers of intraspecific variation in the bacterial component of the GM, identifying a suite of environmental factors that can influence this, including habitat quality and dietary differences [24][25][26], as well as host-related traits, such as age, sex, and host genotype [23,27,28].…”

“…Several studies have demonstrated interspecific differences in GM characteristics [17][18][19], and also variation between groups [20][21][22] or individuals [23][24][25] within the same natural population. Most of these studies have focussed on investigating the drivers of intraspecific variation in the bacterial component of the GM, identifying a suite of environmental factors that can influence this, including habitat quality and dietary differences [24][25][26], as well as host-related traits, such as age, sex, and host genotype [23,27,28]. However, very few studies have investigated the consequences of individual GM variation for host health and fitness (survival and/or reproductive success) in natural populations.…”