Parental Microbiota Modulates Offspring Development, Body Mass and Fecundity in a Polyphagous Fruit Fly.

Binh Nguyen,Hue Dinh,Anh Than,Juliano Morimoto,Fleur Ponton

doi:10.3390/microorganisms8091289

Abstract

The commensal microbiota is a key modulator of animal fitness, but little is known about the extent to which the parental microbiota influences fitness-related traits of future generations. We addressed this gap by manipulating the parental microbiota of a polyphagous fruit fly (Bactrocera tryoni) and measuring offspring developmental traits, body composition, and fecundity. We generated three parental microbiota treatments where parents had a microbiota that was non-manipulated (control), removed (axenic), or removed-and-reintroduced (reinoculation). We found that the percentage of egg hatching, of pupal production, and body weight of larvae and adult females were lower in offspring of axenic parents compared to that of non-axenic parents. The percentage of partially emerged adults was higher, and fecundity of adult females was lower in offspring of axenic parents relative to offspring of control and reinoculated parents. There was no significant effect of parental microbiota manipulation on offspring developmental time or lipid reserve. Our results reveal transgenerational effects of the parental commensal microbiota on different aspects of offspring life-history traits, thereby providing a better understanding of the long-lasting effects of host–microbe interactions.

Highlights

The experience of parents can influence the behaviour, performance, and fitness of future generations [1,2,3,4]
Manipulation of parental microbiota affected the percentage of partially emerged adults (Kruskal–Wallis: χ2 = 6.521, df = 2, p = 0.038)
Reinoculating axenic parents with a microbiota harvested from control parents restored, some traits in offspring that were negatively affected by microbiota depletion in parents

Summary

Introduction

The experience of parents can influence the behaviour, performance, and fitness of future generations [1,2,3,4]. Parental effects can be paternal and/or maternal and have been reported widely in plants [7], insects [8], and vertebrates [5]. Molecular mechanisms responsible for parental effects likely involve epigenetic modifications such as DNA methylation, chromatin modification, and noncoding RNA [9]. In particular, in tephritid fruit fly species, adult females possess a symbiont-rich organ called the ovipositor diverticulum, which smears the egg surface with symbionts before the eggs are deposited [19]. Females of the Mediterranean fruit fly Ceratitis capitata deposit bacteria over the surface of freshly produced eggs and provide eggs with lysozyme and antibacterial polypeptides which eliminate pathogens while facilitating the development of beneficial bacteria [20,21,22]

Methods

Results

Conclusion