Positive selection on mitochondria may eliminate heritable microbes from arthropod populations.

Andy Fenton,Gregory D D Hurst,M Florencia Camus

doi:10.1098/rspb.2021.1735

Andy Fenton, Gregory D D Hurst + Show 1 more

Open Access

https://doi.org/10.1098/rspb.2021.1735

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Abstract

Diverse eukaryotic taxa carry facultative heritable symbionts, microbes that are passed from mother to offspring. These symbionts are coinherited with mitochondria, and selection favouring either new symbionts, or new symbiont variants, is known to drive loss of mitochondrial diversity as a correlated response. More recently, evidence has accumulated of episodic directional selection on mitochondria, but with currently unknown consequences for symbiont evolution. We therefore employed a population genetic mean field framework to model the impact of selection on mitochondrial DNA (mtDNA) upon symbiont frequency for three generic scenarios of host–symbiont interaction. Our models predict that direct selection on mtDNA can drive symbionts out of the population where a positively selected mtDNA mutation occurs initially in an individual that is uninfected with the symbiont, and the symbiont is initially at low frequency. When, by contrast, the positively selected mtDNA mutation occurs in a symbiont-infected individual, the mutation becomes fixed and in doing so removes symbiont variation from the population. We conclude that the molecular evolution of symbionts and mitochondria, which has previously been viewed from a perspective of selection on symbionts driving the evolution of a neutral mtDNA marker, should be reappraised in the light of positive selection on mtDNA.

Highlights

Inherited microbes—bacteria, viruses and fungi that pass from a female to her progeny—are found commonly in eukaryotic hosts
Heritable microbial symbionts and mitochondria are both inherited through the female line, connecting the dynamics t 0.20 0.15 0.10 0.05 b = 0.02 t 0.20 0.15 0.10 0.05 b = 0.04
The relationship between microbial symbionts and the mitochondria with which they are coinherited has been well explored in terms of the impact of selection on symbionts driving the evolution of mitochondria [9,23]

Summary

Introduction

Inherited microbes—bacteria, viruses and fungi that pass from a female to her progeny—are found commonly in eukaryotic hosts. Reproductive parasitism is a consequence of the exclusive maternal inheritance of the microbe, which selects for strains that bias investment towards the production and survival of female offspring over male and for incompatibility between infected males and uninfected females [8] These individual impacts affect population and community dynamics and are important drivers of host evolution. We provide the recursion equations for each model; other mathematical details can be found in the electronic supplementary material For this scenario, we assume a weakly beneficial symbiont, such that offspring of infected mothers receive a net fitness benefit (1 + B); this benefit is a composite of the fixed benefit supplied and the fixed costs of symbiont carriage. We consider a symbiont under positive frequencydependent selection, like one that confers CI In such a model, it is assumed that crosses between uninfected females and infected males reduce offspring fitness by a factor (1 – h).

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