Does diet breadth affect the complexity of the phytophagous insect microbiota? The case study ofChrysomelidae.

Matteo Brunetti,Fabrizia Gionechetti,Giulia Magoga,Alessio De Biase,Matteo Montagna

doi:10.1111/1462-2920.15847

Abstract

SummaryChrysomelidae is a family of phytophagous insects with a highly variable degree of trophic specialization. The aim of this study is to test whether species feeding on different plants (generalists) harbour more complex microbiotas than those feeding on a few or a single plant species (specialists). The microbiota of representative leaf beetle species was characterized with a metabarcoding approach targeting V1–V2 and V4 regions of the bacterial 16S rRNA. Almost all the analysed species harbour at least one reproductive manipulator bacteria (e.g., Wolbachia, Rickettsia). Two putative primary symbionts, previously isolated only from a single species (Bromius obscurus), have been detected in two species of the same subfamily, suggesting a widespread symbiosis in Eumolpinae. Surprisingly, the well‐known aphid symbiont Buchnera is well represented in the microbiota of Orsodacne humeralis. Moreover, in this study, using Hill numbers to dissect the components of the microbiota diversity (abundant and rare bacteria), it has been demonstrated that generalist insect species harbour a more diversified microbiota than specialists. The higher microbiota diversity associated with a wider host‐plant spectrum could be seen as an adaptive trait, conferring new metabolic potential useful to expand the diet breath, or as a result of environmental stochastic acquisition conveyed by diet.

Highlights

Insects are colonized by a variety of microorganisms, prevalently living as commensals, but which in many cases can confer either beneficial or detrimental effects to their host (e.g., Douglas, 2009; Kikuchi et al, 2012; Engel and Moran, 2013; Clay, 2014; Douglas, 2015; Hurst and Frost, 2015; Wang et al, 2020)
The higher microbiota diversity associated with a wider host-plant spectrum could be seen as an adaptive trait, conferring new metabolic potential useful to expand the diet breath, or as a result of environmental stochastic acquisition conveyed by diet
Other bacteria are able to colonize insect cells, such as the reproductive manipulators belonging to the so-called male-killing group that can manipulate the host reproduction to maintain their infection across generations and spread within the population (Harris et al, 2010; Correa and Ballard, 2016; Larracuente and Meller, 2016)

Summary

Introduction

Insects are colonized by a variety of microorganisms, prevalently living as commensals, but which in many cases can confer either beneficial or detrimental effects to their host (e.g., Douglas, 2009; Kikuchi et al, 2012; Engel and Moran, 2013; Clay, 2014; Douglas, 2015; Hurst and Frost, 2015; Wang et al, 2020). More recently the advent of next-generation sequencing techniques coupled with the 16S rRNAbased approach for the bacterial taxonomy has greatly facilitated the characterization of the full microbiota associated with non-model organisms, allowing to expand the experimental scale (e.g., Montagna et al, 2015a; Mohammed et al, 2018; Ziganshina et al, 2018; Kolasa et al, 2019) This innovation opened the possibility to characterize the microbiota associated with several wild species and so to investigate the correlations between the composition of microbial communities and several ecological or physiological traits of the insect host, such as the breadth of the insect diet (Colman et al, 2012; Yun et al, 2014). The covariation of microbiota diversity and breadth of the animal diet has been investigated in non-insect taxa, usually achieving inconclusive results that do not support the hypothesis of a higher diversity in the microbiota of generalist species (e.g., Kartzinel et al, 2019; Chen et al, 2021)

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