Male-killing Wolbachia and mitochondrial selective sweep in a migratory African insect

Robert I Graham,Kenneth Wilson

doi:10.1186/1471-2148-12-204

Abstract

BackgroundNumerous recent studies have shown that resident symbiotic microorganisms of insects play a fundamental role in host ecology and evolution. The lepidopteran pest, African armyworm (Spodoptera exempta), is a highly migratory and destructive species found throughout sub-Saharan Africa, that can experience eruptive outbreaks within the space of a single generation, making predicting population dynamics and pest control forecasting extremely difficult. Three strains of Wolbachia have recently been identified infecting this species in populations sampled from Tanzania. In this study, we examined the interaction between Wolbachia pipiensis infections and the co-inherited marker, mtDNA, within populations of armyworm, as a means to investigate the population biology and evolutionary history of Wolbachia and its host.ResultsA Wolbachia-infected isofemale line was established in the laboratory. Phenotypic studies confirmed the strain wExe1 as a male-killer. Partial sequencing of the mitochondrial COI gene from 164 individual field-collected armyworm of known infection status revealed 17 different haplotypes. There was a strong association between Wolbachia infection status and mtDNA haplotype, with a single dominant haplotype, haplo1 (90.2% prevalence), harbouring the endosymbiont. All three Wolbachia strains were associated with this haplotype. This indicates that Wolbachia may be driving a selective sweep on armyworm haplotype diversity. Despite very strong biological and molecular evidence that the samples represent a single species (including from nuclear 28S gene markers), the 17 haplotypes did not fall into a monophyletic clade within the Spodoptera genus; with six haplotypes (2 each from 3 geographically separate populations) differing by >11% in their nucleotide sequence to the other eleven.ConclusionsThis study suggests that three strains of Wolbachia may be driving a selective sweep on armyworm haplotype diversity, and that based on COI sequence data, S. exempta is not a monophyletic group within the Spodoptera genus. This has clear implications for the use of mtDNA as neutral genetic markers in insects, and also demonstrates the impact of Wolbachia infections on host evolutionary genetics.

Highlights

Numerous recent studies have shown that resident symbiotic microorganisms of insects play a fundamental role in host ecology and evolution
We examined the diversity of mitochondrial haplotypes, and analysed mtDNA variation to explore the potential association with different Wolbachia infection statuses
Phenotypic effects of wolbachia infection Two wExe1-infected and several uninfected isofemale lines were established from field-collected pupae, and maintained under laboratory conditions for >4 generations

Summary

Introduction

Numerous recent studies have shown that resident symbiotic microorganisms of insects play a fundamental role in host ecology and evolution. Recent studies into resident heritable symbiotic microorganisms have highlighted the central role they play in their insect host’s ecology and evolution [1,2]. These symbionts can be classified as either obligate or facultative for host survival. Wolbachia have the ability to induce a number of reproductive manipulations of their hosts, such as feminisation of genetic males, induction of sperm-egg incompatibilities, thelytokous parthenogenesis, and male-killing [1,15] Through these processes, Wolbachia provides infected host-females with a relative reproductive advantage over uninfected females [16]. A single insect or population may be infected with more than one symbiotic microorganism and different populations may have different infection statuses [17,18]

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