Dataset Information

Wolbachia-induced parthenogenesis in a genus of phytophagous mites.

ABSTRACT: The vertically transmitted endosymbiotic bacterium Wolbachia modifies host reproduction in several ways in order to enhance its own spread. One such modification results in the induction of parthenogenesis, where males, which are unable to transmit Wolbachia, are not produced. Interestingly, parthenogenesis-inducing Wolbachia have only been found within haplodiploid insects and it is not known whether this exclusivity is the result of functional constraints of Wolbachia. Here we find a unique pattern of Wolbachia infection that is associated with parthenogenesis in six species within the phytophagous mite genus Bryobia. Through antibiotic treatment we show that, in two species, Bryobia praetiosa and an unidentified species, the Wolbachia infection is strictly associated with parthenogenesis. Microsatellite loci show the mechanism of parthenogenesis to be functionally apomictic and not gamete duplication, with progeny identical to their infected mother. Crossing experiments within B. praetiosa showed no evidence of sexual reproduction. These results are discussed with reference to the distribution of parthenogenesis-inducing Wolbachia and the diversification of the Bryobia genus.

SUBMITTER: Weeks AR

PROVIDER: S-EPMC1088872 | biostudies-other | 2001 Nov

REPOSITORIES: biostudies-other

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Wolbachia-induced parthenogenesis in a genus of phytophagous mites.

Weeks A R AR Breeuwer J A JA

Proceedings. Biological sciences 20011101 1482

The vertically transmitted endosymbiotic bacterium Wolbachia modifies host reproduction in several ways in order to enhance its own spread. One such modification results in the induction of parthenogenesis, where males, which are unable to transmit Wolbachia, are not produced. Interestingly, parthenogenesis-inducing Wolbachia have only been found within haplodiploid insects and it is not known whether this exclusivity is the result of functional constraints of Wolbachia. Here we find a unique pa ...[more]

PMID: 11674872

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Project description:Intersex is an intermediate stage of sexual differentiation in insects. Determining intersex morphology and the cause of its production will aid in the understanding of the mechanism of sexual differentiation in insects. In this paper, Wolbachia-infected Trichogramma pretiosum (T. preW+ ) that shows thelytokous parthenogenesis were used as subjects. In order to determine the causes of the T. preW+ intersex and the influence of parental generation temperature on gradual changes in secondary masculinization in intersex offspring, we examined the occurrence of intersex offspring (F1 and F2 generation) after the parental generations were treated with high temperature (27, 29, 31, and 33 °C) and described the external morphology of the intersexes. The results showed that the T. preW+ parental generation temperature is positively correlated with the probability of intersex offspring. The probability of F1 intersex is significantly higher than that of F2 intersex in different high temperature. The degree of secondary masculinization in T. preW+ intersexes increases as parental generation temperature increases. In addition, our study first identified 11 intersex types in T. preW+ and found that the primary and secondary sexual characteristics showed a regular distribution. We also found that the D type and H type of intersex have the highest frequency of appearance. The external genitalia of most intersexes were female, and only three intersex types have male external genitalia. Conclusions were ultimately obtained: Wolbachia is a direct factor that causes the occurrence of intersexes, while high temperature is an indirect factor that determines the external morphology of intersexes. The effects of high temperature on T. preW+ intersexes is passed through the parental generation to offspring, and this maternal effect weakens as the number of generations increases. In T. preW+ intersex individuals, most exhibit female primary sexual characteristics, and secondary sexual characteristics exhibit signs of masculinization.

Project description:BACKGROUND: Wolbachia and Cardinium are endosymbiotic bacteria infecting many arthropods and manipulating host reproduction. Although these bacteria are maternally transmitted, incongruencies between phylogenies of host and parasite suggest an additional role for occasional horizontal transmission. Consistent with this view is the strong evidence for recombination in Wolbachia, although it is less clear to what extent recombination drives diversification within single host species and genera. Furthermore, little is known concerning the population structures of other insect endosymbionts which co-infect with Wolbachia, such as Cardinium. Here, we explore Wolbachia and Cardinium strain diversity within nine spider mite species (Tetranychidae) from 38 populations, and quantify the contribution of recombination compared to point mutation in generating Wolbachia diversity. RESULTS: We found a high level of genetic diversity for Wolbachia, with 36 unique strains detected (64 investigated mite individuals). Sequence data from four Wolbachia genes suggest that new alleles are 7.5 to 11 times more likely to be generated by recombination than point mutation. Consistent with previous reports on more diverse host samples, our data did not reveal evidence for co-evolution of Wolbachia with its host. Cardinium was less frequently found in the mites, but also showed a high level of diversity, with eight unique strains detected in 15 individuals on the basis of only two genes. A lack of congruence among host and Cardinium phylogenies was observed. CONCLUSIONS: We found a high rate of recombination for Wolbachia strains obtained from host species of the spider mite family Tetranychidae, comparable to rates found for horizontally transmitted bacteria. This suggests frequent horizontal transmission of Wolbachia and/or frequent horizontal transfer of single genes. Our findings strengthens earlier reports of recombination for Wolbachia, and shows that high recombination rates are also present on strains from a restrictive host range. Cardinium was found co-infecting several spider mite species, and phylogenetic comparisons suggest also horizontal transmission of Cardinium among hosts.

Project description:BackgroundThe maternally inherited, bacterial symbiont, parthenogenesis inducing (PI) Wolbachia, causes females in some haplodiploid insects to produce daughters from both fertilized and unfertilized eggs. The symbionts, with their maternal inheritance, benefit from inducing the production of exclusively daughters, however the optimal sex ratio for the nuclear genome is more male-biased. Here we examine through models how an infection with PI-Wolbachia in a previously uninfected population leads to a genomic conflict between PI-Wolbachia and the nuclear genome. In most natural populations infected with PI-Wolbachia the infection has gone to fixation and sexual reproduction is impossible, specifically because the females have lost their ability to fertilize eggs, even when mated with functional males.ResultsThe PI Wolbachia infection by itself does not interfere with the fertilization process in infected eggs, fertilized infected eggs develop into biparental infected females. Because of the increasingly female-biased sex ratio in the population during a spreading PI-Wolbachia infection, sex allocation alleles in the host that cause the production of more sons are rapidly selected. In haplodiploid species a reduced fertilization rate leads to the production of more sons. Selection for the reduced fertilization rate leads to a spread of these alleles through both the infected and uninfected population, eventually resulting in the population becoming fixed for both the PI-Wolbachia infection and the reduced fertilization rate. Fertilization rate alleles that completely interfere with fertilization ("virginity alleles") will be selected over alleles that still allow for some fertilization. This drives the final resolution of the conflict: the irreversible loss of sexual reproduction and the complete dependence of the host on its symbiont.ConclusionsThis study shows that dependence among organisms can evolve rapidly due to the resolution of the conflicts between cytoplasmic and nuclear genes, and without requiring a mutualism between the partners.

Dataset Information

Wolbachia-induced parthenogenesis in a genus of phytophagous mites.

Publications

Wolbachia-induced parthenogenesis in a genus of phytophagous mites.

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