Abstract

Animals have been developing key associations with micro-organisms through evolutionary processes and ecological diversification. Hence, in some host clades, phylogenetic distance between hosts is correlated to dissimilarity in microbiomes, a pattern called phylosymbiosis. Teleost fishes, despite being the most diverse and ancient group of vertebrates, have received little attention from the microbiome perspective and our understanding of its determinants is currently limited. In this study, we assessed the gut microbiome of 12 co-occurring species of teleost representing a large breadth of ecological diversity and originating from a single family (i.e., the Sparidae). We tested how host evolutionary history, diet composition and morphological traits are related to fish gut microbiome. Despite fish species having different microbiomes, there is no phylosymbiosis signal in this fish family, but gut length and diet had a strong influence on the microbiome. We revealed that the only species with a specialized herbivorous diet, Sarpa salpa had a 3.3 times longer gut than carnivorous species and such a long gut favor the presence of anaerobic bacteria typical of herbivorous gut microbiomes. Hence, dietary uniqueness is paired with both unique gut anatomy and unique microbiome.

Highlights

  • All animals evolved and diversified within a microbial world, and developed a myriad of associations with micro-organisms (McFall-Ngai et al, 2013)

  • Phylosymbiosis has been evidenced in many animals, notably those for which vertical transmission of the microbiome has been reported, such as in the gut of insects (Brucker and Bordenstein, 2012; Haddow et al, 2013; Sanders et al, 2014; Brooks et al, 2016), and mammals (Phillips et al, 2012; Sanders et al, 2014), or on the skin of mammals (Ross et al, 2018) and elasmobranchs (Doane et al, 2020)

  • The 12 studied Sparidae species shared a common ancestor around 60 million years ago and separated in two main branches which do not contain recent (

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Summary

Introduction

All animals evolved and diversified within a microbial world, and developed a myriad of associations with micro-organisms (McFall-Ngai et al, 2013). The abundant and diverse microbial communities present within and on the surface of animal bodies, i.e., the microbiomes, play a central role in the fitness of their host, providing benefits that include successful development of the immune system and protection against pathogens, and enhanced food processing and nutrient absorption (McKenney et al, 2018a; Moran et al, 2019). These long histories of animalmicrobes interactions resulted for many clades in phylosymbiosis, i.e., the eco-evolutionary pattern where phylogenetically related hosts tend to have more similar microbiomes than distantly related ones (Brooks et al, 2016; Lim and Bordenstein, 2019). Evidences are far less pronounced in animals with horizontal microbiome transmission, with the report of weak to no support for skin phylosymbiosis in amphibians (Bletz et al, 2017) and marine fishes (Chiarello et al, 2018, 2019; Doane et al, 2020)

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