Rapid divergence in independent aspects of the compatibility phenotype in a Spiroplasma–Drosophila interaction

Abstract

Heritable symbionts represent important components of the biology, ecology and evolution of their arthropod hosts. Particular microbial taxa have become common across arthropods as a consequence of their ability to establish in new host species. For a host shift to occur, the symbiont must be exposed to a novel host and then be compatible: it must not cause excess pathology, must have good vertical transmission and must possess a drive phenotype that enables spread. Here we investigate the lability of compatibility to symbiosis with Spiroplasma . We used transinfection to establish the protective Spiroplasma symbiont from Drosophila hydei in two closely related novel hosts, Drosophila simulans and Drosophila melanogaster. The Spiroplasma had contrasting compatibility in the two species, exhibiting pathology and low vertical transmission but delivering protection from wasp attack in D. melanogaster but being asymptomatic and transmitted with high efficiency but with lower protection in D. simulans. Further work indicated that pathological interactions occurred in two other members of the melanogaster species group, such that D. simulans was unusual in being able to carry the symbiont without damage. The differing compatibility of the symbiont with these closely related host species emphasizes the rapidity with which host–symbiont compatibility evolves, despite compatibility itself not being subject to direct selection. Further, the requirement to fit three independent components of compatibility (pathology, transmission, protection) is probably to be a major feature limiting the rate of host shifts that will likely impact on the utility of Spiroplasma in pest and vector control. Moving forward, the variation between sibling species pairs provides an opportunity to identify the mechanisms behind variable compatibility, which will drive hypotheses as to the evolutionary drivers of compatibility variation.

Species identification of livefood flightless fly (Torinido‐shoujoubae) through DNA barcoding

“…hydei as a model organism (Hennig, 1985 ; Neesen et al., 1994 ). Additionally, in ecological studies, interactions with symbiotic bacteria (Gerth et al., 2021 ; Griffin et al., 2022 ; Kageyama et al., 2006 ), roles as mediators of yeast (Lam & Howell, 2015 ) and parasitic relationship with mites and parasitoid wasps (Corbin et al., 2021 ; Michalska et al., 2023 ; Perez‐Leanos et al., 2017 ) have been studied. Furthermore, D .…”

“…In genetics, D. hydei is used for comparative studies of gene functions with representative models such as D. melanogaster and other Drosophila species (Akhmanova et al, 1995;Templeton et al, 1989) and for genetic studies based on D. hydei as a model organism (Hennig, 1985;Neesen et al, 1994). Additionally, in ecological studies, interactions with symbiotic bacteria (Gerth et al, 2021;Griffin et al, 2022;Kageyama et al, 2006), roles as mediators of yeast (Lam & Howell, 2015) and parasitic relationship with mites and parasitoid wasps (Corbin et al, 2021;Michalska et al, 2023;Perez-Leanos et al, 2017) have been studied. Furthermore, D. hydei, as one of the flightless flies, is preferred by researchers for use in laboratories as feeds for predating species such as spiders and beetles (Takasuka & Arakawa, 2023) due to its ease of maintenance and provision.…”