Evolutionary Significance of Wolbachia-to-Animal Horizontal Gene Transfer: Female Sex Determination and the f Element in the Isopod Armadillidium vulgare.

Clément Gilbert,Richard Cordaux

doi:10.3390/genes8070186

Abstract

An increasing number of horizontal gene transfer (HGT) events from bacteria to animals have been reported in the past years, many of which involve Wolbachia bacterial endosymbionts and their invertebrate hosts. Most transferred Wolbachia genes are neutrally-evolving fossils embedded in host genomes. A remarkable case of Wolbachia HGT for which a clear evolutionary significance has been demonstrated is the “f element”, a nuclear Wolbachia insert involved in female sex determination in the terrestrial isopod Armadillidium vulgare. The f element represents an instance of bacteria-to-animal HGT that has occurred so recently that it was possible to infer the donor (feminizing Wolbachia closely related to the wVulC Wolbachia strain of A. vulgare) and the mechanism of integration (a nearly complete genome inserted by micro-homology-mediated recombination). In this review, we summarize our current knowledge of the f element and discuss arising perspectives regarding female sex determination, unstable inheritance, population dynamics and the molecular evolution of the f element. Overall, the f element unifies three major areas in evolutionary biology: symbiosis, HGT and sex determination. Its characterization highlights the tremendous impact sex ratio distorters can have on the evolution of sex determination mechanisms and sex chromosomes in animals and plants.

Highlights

It is well-established knowledge that the horizontal transfer of genetic material (i.e., DNA acquired by an organism in the absence of reproduction) is an important driver of prokaryote evolution [1,2]
We first provide a background for the A. vulgare/Wolbachia model; we offer an account of the current state of knowledge on the f element; and, we identify outstanding questions to further our understanding of this topic
The f element of A. vulgare is a remarkable case of bacteria-to-animal horizontal gene transfer (HGT) as it has occurred so recently that it was possible to infer the donor of the transfer, the mechanism of integration and the evolutionary significance of the transferred sequence [36]

Summary

Introduction

It is well-established knowledge that the horizontal transfer of genetic material (i.e., DNA acquired by an organism in the absence of reproduction) is an important driver of prokaryote evolution [1,2]. It is noteworthy that many of the incidences of bacteria-to-animal HGT reported so far involve intracellular bacterial endosymbionts [9] Some of these bacteria are maternally transmitted through oocytes, implying that they reside for at least part of the time in the female germline of their animal hosts. There are several examples of Wolbachia-like transferred genes leading to new functions in the nuclear genomes of an aphid [27], a mealybug [28] and a stink bug [29]; in all of these cases, it is unclear whether HGT involved Wolbachia per se or a member of the Rickettsiales related to Wolbachia. HGT meeting the gold standard proposed by Dunning Hotopp [9] has recently been characterized This nuclear Wolbachia insert, termed the “f element”, is involved in female sex determination in the terrestrial isopod crustacean Armadillidium vulgare [36] (Figure 1).

Feminizing Wolbachia and Sex Determination in Armadillidium vulgare

Wolbachia offspring at are assumed to be

Characterization of the f Element of Armadillidium vulgare

Outstanding Questions Regarding the f Element

What Is the Molecular Genetic Basis of Feminization Induced by the f Element?

How to Explain the Unstable Inheritance of the f Element?

What Is the Population Dynamics of the f Element?

What Are the Patterns of Molecular Evolution of the f Element?

Findings

Conclusions and Perspectives