Dataset Information

Fifty-year trend towards suppression of Wolbachia-induced male-killing by its butterfly host, Hypolimnas bolina.

ABSTRACT: Some intracellular symbionts of arthropods induce a variety of reproductive alterations in their hosts, and the alterations tend to spread easily within the host populations. A few cases involving the spread of alteration-inducing Wolbachia bacteria in natural populations with time have been reported, but the investigations on the increasing trend in counteracting the bacterial effect on hosts in natural populations (i.e., increased resistance in hosts against the alterations) have been limited. In the present study, the prevalence of an alteration, killing of male Hypolimnas bolina (L.) (Lepidoptera: Nymphalidae) butterflies by their inherited Wolbachia strain in the wild in Japan, was surveyed over a continuous 50-year period, which is far longer than ever before analyzed in studies of dynamics between reproductive alteration-inducing symbionts and their host arthropods. Thus, the results in this study provide the first instance of a long-term trend involving a change in reproductive alteration; and it strongly suggests a change in the opposite direction (i.e., suppression of male-killing) in natural populations. This change in the current combination of the Wolbachia and butterflies appears to be dependent upon the host taxon (race).

SUBMITTER: Mitsuhashi W

PROVIDER: S-EPMC3281488 | biostudies-literature | 2011

REPOSITORIES: biostudies-literature

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Fifty-year trend towards suppression of Wolbachia-induced male-killing by its butterfly host, Hypolimnas bolina.

Mitsuhashi Wataru W Ikeda Hiroshi H Muraji Masahiko M

Journal of insect science (Online) 20110101

Some intracellular symbionts of arthropods induce a variety of reproductive alterations in their hosts, and the alterations tend to spread easily within the host populations. A few cases involving the spread of alteration-inducing Wolbachia bacteria in natural populations with time have been reported, but the investigations on the increasing trend in counteracting the bacterial effect on hosts in natural populations (i.e., increased resistance in hosts against the alterations) have been limited. ...[more]

PMID: 21870980

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Project description: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.

Project description:The small brown planthopper Laodelphax striatellus (Hemiptera: Delphacidae) is reported to have the endosymbiont Wolbachia, which shows a strong cytoplasmic incompatibility (CI) between infected males and uninfected females. In the 2000s, female-biased L. striatellus populations were found in Taiwan, and this sex ratio distortion was the result of male-killing induced by the infection of another endosymbiont, Spiroplasma. Spiroplasma infection is considered to negatively affect both L. striatellus and Wolbachia because the male-killing halves the offspring of L. striatellus and hinders the spread of Wolbachia infection via CI. Spiroplasma could have traits that increase the fitness of infected L. striatellus and/or coexisting organisms because the coinfection rates of Wolbachia and Spiroplasma were rather high in some areas. In this study, we investigated the influences of the infection of these two endosymbionts on the development, reproduction, and insecticide resistance of L. striatellus in the laboratory. Our results show that the single-infection state of Spiroplasma had a negative influence on the fertility of L. striatellus, while the double-infection state had no significant influence. At late nymphal and adult stages, the abundance of Spiroplasma was lower in the double-infection state than in the single-infection state. In the double-infection state, the reduction of Spiroplasma density may be caused by competition between the two endosymbionts, and the negative influence of Spiroplasma on the fertility of host may be relieved. The resistance of L. striatellus to four insecticides was compared among different infection states of endosymbionts, but Spiroplasma infection did not contribute to increase insecticide resistance. Because positive influences of Spiroplasma infection were not found in terms of the development, reproduction, and insecticide resistance of L. striatellus, other factors improving the fitness of Spiroplasma-infected L. striatellus may be related to the high frequency of double infection in some L. striatellus populations.

Dataset Information

Fifty-year trend towards suppression of Wolbachia-induced male-killing by its butterfly host, Hypolimnas bolina.

Publications

Fifty-year trend towards suppression of Wolbachia-induced male-killing by its butterfly host, Hypolimnas bolina.

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