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

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.

How to identify sex chromosomes and their turnover

“…Endosymbionts can have a similar impact, as illustrated by the Wolbachia feminizing element in populations of woodlice (Cordaux, Bouchon, & Grève, ). Increasing numbers of theoretical models outline the scenarios in which we might expect sex ratio selection to drive the evolution of new sex chromosome systems (Kozielska, Weissing, Beukeboom, & Pen, ; Úbeda, Patten, & Wild, ) and there is growing support from a few taxa (Badawi, Moumen, Giraud, Grève, & Cordaux, ; Becking et al, ; Chebbi et al, ; Cordaux et al, ; Cordaux & Gilbert, ; Leclercq et al, ; Miura, ). Similarly, a recent study outlined the role of haploid selection via gametic competition and meiotic drive in increasing the lability of sex determination systems (Scott et al, ).…”

Female-biased sex ratios unrelated to Wolbachia infection in European species of the Jaera albifrons complex (marine isopods)

“…It is predominantly transmitted via female gametes (Werren et al, 2008) and it often promotes its transmission by interfering in the process of reproduction of its host (Rousset et al, 1992;Werren, 1997). Wolbachia is notably known to be involved in the conversion of genetic males into functional phenotypic neo-females, a process called feminization (Bouchon et al, 2008;Cordaux and Gilbert, 2017;Rigaud et al, 1999;Werren et al, 2008). It can also induce parthenogenesis in several otherwise sexually reproducing species, or specifically kill the male offspring of infected females (Hurst et al, 1999).…”

Sex chromosomes control vertical transmission of feminizing Wolbachia symbionts in an isopod

“…Surprisingly, the Wolbachia -infected YY mother in the previous pedigree analysis produced an all-male progeny (I-F2-2) entirely lacking Wolbachia endosymbionts (Fig 2). This is unexpected because infection by feminizing Wolbachia endosymbionts is usually associated with highly female-biased progenies, due to the maternal transmission of Wolbachia to usually >80% of the offspring [10,24–26]. To test whether lack of Wolbachia transmission from mother to I-F2-2 progeny was a random event or was due to the unusual YY maternal genotype, we extended our previous pedigree analysis to span five generations (S3 Fig) and analysed a second, independent pedigree spanning four generations (S4 Fig).…”

“…Wolbachia are intracellular, maternally inherited endosymbionts of arthropods, often acting as reproductive parasites that manipulate host reproduction to favour infected females in host populations [23]. In terrestrial isopods, Wolbachia is best known as a sex ratio distorter due to its ability to feminize genetic males into phenotypic females [10,24–26]. For example, the presence of feminizing Wolbachia in Armadillidium vulgare leads to highly female-biased progenies [27, 28] because symbionts override the ZZ/ZW system of sex chromosomes [29, 30].…”