Heritability of symbiont density reveals distinct regulatory mechanisms in a tripartite symbiosis.

Jasmine F Parkinson,Bruno Gobin,William O H Hughes

doi:10.1002/ece3.2005

Abstract

Beneficial eukaryotic–bacterial partnerships are integral to animal and plant evolution. Understanding the density regulation mechanisms behind bacterial symbiosis is essential to elucidating the functional balance between hosts and symbionts. Citrus mealybugs, Planococcus citri (Risso), present an excellent model system for investigating the mechanisms of symbiont density regulation. They contain two obligate nutritional symbionts, Moranella endobia, which resides inside Tremblaya princeps, which has been maternally transmitted for 100–200 million years. We investigate whether host genotype may influence symbiont density by crossing mealybugs from two inbred laboratory‐reared populations that differ substantially in their symbiont density to create hybrids. The density of the M. endobia symbiont in the hybrid hosts matched that of the maternal parent population, in keeping with density being determined either by the symbiont or the maternal genotype. However, the density of the T. princeps symbiont was influenced by the paternal host genotype. The greater dependency of T. princeps on its host may be due to its highly reduced genome. The decoupling of T. princeps and M. endobia densities, in spite of their intimate association, suggests that distinct regulatory mechanisms can be at work in symbiotic partnerships, even when they are obligate and mutualistic.

Highlights

Symbiotic associations are extremely widespread in nature, and beneficial eukaryotic–bacterial partnerships have shaped the very foundations of plant and animal evolution (Schwartz and Dayhoff 1978)
Symbiosis creates an overlap of selective interests between partners, which will increase with the degree to which symbiont transmission is vertical rather than horizontal, and will be strongest in the hosts that vertically transmit the symbiont
The same pattern did not follow for the T. princeps symbiont (Fig. 1B)

Summary

Introduction

Symbiotic associations are extremely widespread in nature, and beneficial eukaryotic–bacterial partnerships have shaped the very foundations of plant and animal evolution (Schwartz and Dayhoff 1978). Even mutualistic symbiotic associations are inherently selfish, with benefits given only so long as they are reciprocated and, as well as selection for cooperation, there is selection pressure to cheat and exploit the partnership (Bennett and Moran 2015). As they coevolve, hosts will be selected to increase their own fecundity, with or without symbionts, whereas symbionts will be selected to maximize their transmission to new hosts, while simultaneously outcompeting other strains and species of symbiont for the limited resources provided by the host (Frank 1996). Symbiont dependency upon the host increases following symbiont genome reduction – a common result of the symbiont lifestyle (Moran and Bennett 2014; Bennett and Moran 2015)

Methods

Results

Conclusion