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

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.

Lack of population genetic structure and host specificity in the bat fly, Cyclopodia horsfieldi, across species of Pteropus bats in Southeast Asia

“…While we cannot rule out this possibility, it seems unlikely that this selective pressure has influenced the demographic history of each bat fly population sampled. Also, even in the case of Wolbachia infection in insects, high levels of migration may still be a more prominent factor reducing genetic differentiation in species with potential to disperse long distances [83]. Third, demographic factors, i.e.…”

The global impact ofWolbachiaon mitochondrial diversity and evolution

“…A number of case studies have demonstrated that the spread of Wolbachia can indeed affect the mtDNA polymorphism (Turelli et al 1992;Solignac et al 1994;Ballard et al 1996;Jiggins 2003;Charlat et al 2009;Graham and Wilson 2012;Obbard et al 2012;Richardson et al 2012;Schuler et al 2016). Shoemaker (2004) also provided evidence for an elevated 70 non-synonymous substitution rate in an infected Drosophila species compared to its uninfected sister species, making Wolbachia and reduction in Ne a very plausible explanation.…”

Local coexistence and genetic isolation of three pollinator species on the same fig tree species

“…While molecular taxonomy may reveal cryptic lineages, the reliability of mtDNA for species delimitation has been criticised for various reasons (Rubinoff et al, 2006), including the persistence of genetic structure after resumption of gene flow due to lack of mtDNA recombination (for example, Lausen et al, 2008;Ruskey and Taylor, 2016), hybrid introgression (for example, Chen et al, 2009;MachadoSchiaffino et al, 2010) and selective sweeps caused by maternally inherited endosymbionts that can drive divergence and homogenisation across species (for example, Graham and Wilson, 2012;Xiao et al, 2012;Jäckel et al, 2013). These issues raise significant concerns when mtDNA is used in isolation, but they are likely to be resolved with further study of nuclear loci.…”