Dynamics of the continent‐wide spread of a Drosophila defensive symbiont

Abstract

Facultative symbionts can represent important sources of adaptation for their insect hosts and thus have the potential for rapid spread. Drosophila neotestacea harbours a heritable symbiont, Spiroplasma, that confers protection against parasitic nematodes. We previously found a cline in Spiroplasma prevalence across central Canada, ending abruptly at the Rocky Mountains. Resampling these populations 9 years later revealed that Spiroplasma had increased substantially across the region, resembling a Fisherian wave of advance. Associations between Spiroplasma infection and host mitochondrial DNA indicate that the increase was due to local increase of Spiroplasma-infected flies. Finally, we detected Spiroplasma west of the Rocky Mountains for the first time and showed that defence against nematodes occurs in flies with a western genetic background. Because nematode infection is common throughout D. neotestacea's range, we expect Spiroplasma to spread to the Pacific coast.

A ribosome-inactivating protein in a Drosophila defensive symbiont

“…In D. neotestacea, we have observed no fitness costs associated with Spiroplasma (e.g., ref. 21), and population cage experiments also suggest that direct costs of Spiroplasma-toxin-induced or otherwise-are negligible or context-dependent in this symbiosis (47).…”

“…Infection normally sterilizes flies (20); however, when flies harbor a strain of the inherited symbiont Spiroplasma-a Gram-positive bacterium in the class Mollicutes-they remarkably tolerate Howardula infection without loss of fecundity, and infection intensity is substantially reduced (13). The benefit conferred by this protection lends a substantial selective advantage to Spiroplasma-infected flies and has led to Spiroplasma's recent spread across North America, with symbiont-infected flies rapidly replacing uninfected ones (21). Spiroplasma is a diverse and widespread lineage of arthropod-associated bacteria that can be commensal, pathogenic,…”

Nonrandom associations of maternally transmitted symbionts in insects: The roles of drift versus biased cotransmission and selection

“…As discussed by Jaenike (), such associations could be driven by symbiont hitchhiking, if one of the two symbionts is beneficial and spreads in the population from a matriline also containing another symbiont. Spiroplasma has actually undergone such a spread (Cockburn et al, ; Jaenike, Unckless, et al, ), probably because of the protection it provides against the parasitic nematode Howardula aoronymphium (Jaenike, Unckless, et al, ). This spread could strongly decrease the female effective population size, which was only partially accounted for in our ABC analysis since we assumed that males and females have the same effective population sizes.…”

Host Defense via Symbiosis in Drosophila

“…In Drosophila neotestacea , Spiroplasma decreases the size and transmission of a common and virulent nematode parasite of the fly, and restores the fertility of nematode-parasitized flies that are normally sterilized by infection [27]. This strong protective effect has lead to Spiroplasma 's rapid continent-wide spread through North American D. neotestacea in recent decades [29]. This Spiroplasma strain causes no reproductive manipulation, apparently relying solely on the selective advantage of the defense it confers to spread, providing one of the more compelling examples of the importance of defensive symbioses in the wild.…”