Phenotype and transmission efficiency of artificial and natural male-killing Spiroplasma infections in Drosophila melanogaster

Hutchence, Kate J.; Padé, Rémi; Swift, Heather L.; Bennett, Daimark; Hurst, Gregory D. D.

doi:10.1016/j.jip.2011.10.003

Cited by 9 publications

(5 citation statements)

References 24 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…For example, inherited Spiroplasma strains introduced into novel Drosophila species are often poorly transmitted from mother to offspring (35). S .…”

Section: Discussionmentioning

confidence: 99%

Vertical Transmission of a Drosophila Endosymbiont Via Cooption of the Yolk Transport and Internalization Machinery

Herren

Paredes

Schüpfer

et al. 2013

mBio

111

105

View full text Add to dashboard Cite

Spiroplasma is a diverse bacterial clade that includes many vertically transmitted insect endosymbionts, including Spiroplasma poulsonii, a natural endosymbiont of Drosophila melanogaster. These bacteria persist in the hemolymph of their adult host and exhibit efficient vertical transmission from mother to offspring. In this study, we analyzed the mechanism that underlies their vertical transmission, and here we provide strong evidence that these bacteria use the yolk uptake machinery to colonize the germ line. We show that Spiroplasma reaches the oocyte by passing through the intercellular space surrounding the ovarian follicle cells and is then endocytosed into oocytes within yolk granules during the vitellogenic stages of oogenesis. Mutations that disrupt yolk uptake by oocytes inhibit vertical Spiroplasma transmission and lead to an accumulation of these bacteria outside the oocyte. Impairment of yolk secretion by the fat body results in Spiroplasma not reaching the oocyte and a severe reduction of vertical transmission. We propose a model in which Spiroplasma first interacts with yolk in the hemolymph to gain access to the oocyte and then uses the yolk receptor, Yolkless, to be endocytosed into the oocyte. Cooption of the yolk uptake machinery is a powerful strategy for endosymbionts to target the germ line and achieve vertical transmission. This mechanism may apply to other endosymbionts and provides a possible explanation for endosymbiont host specificity.

show abstract

“…For example, inherited Spiroplasma strains introduced into novel Drosophila species are often poorly transmitted from mother to offspring (35). S .…”

Section: Discussionmentioning

confidence: 99%

Vertical Transmission of a Drosophila Endosymbiont Via Cooption of the Yolk Transport and Internalization Machinery

Herren

Paredes

Schüpfer

et al. 2013

mBio

111

105

View full text Add to dashboard Cite

show abstract

“…Having said that, the lower frequency of Spiroplasma transmission may have resulted from the poor adaptation of the isolates to the new host tick species. Spiroplasma strains introduced into other species are often poorly transmitted from the mother to offspring in Drosophila 33 . Spiroplasma citri , which normally infects leafhoppers, grows well in D. melanogaster haemolymph but cannot access the oocyte and, therefore, is not vertically transmitted 34 .…”

Section: Discussionmentioning

confidence: 99%

Investigation of vertical and horizontal transmission of Spiroplasma in ticks under laboratory conditions

Ogata,

Umemiya-Shirafuji,

Kusakisako

et al. 2023

Sci Rep

View full text Add to dashboard Cite

Many arthropods harbour bacterial symbionts, which are maintained by vertical and/or horizontal transmission. Spiroplasma is one of the most well-known symbionts of ticks and other arthropods. It is still unclear how Spiroplasma infections have spread in tick populations despite its high prevalence in some tick species. In this study, Ixodes ovatus, which has been reported to harbour Spiroplasma ixodetis at high frequencies, was examined for its vertical transmission potential under experimental conditions. Next, two isolates of tick-derived Spiroplasma, S. ixodetis and Spiroplasma mirum, were experimentally inoculated into Spiroplasma-free Haemaphysalis longicornis colonies and the presence of Spiroplasma in their eggs and larvae was tested. Our experimental data confirmed that S. ixodetis was transmitted to eggs and larvae in a vertical manner in the original host I. ovatus. In the second experiment, there was no significant difference in engorged weight, egg weight, and hatching rate between Spiroplasma-inoculated and control H. longicornis groups. This suggested that Spiroplasma infection does not affect tick reproduction. Spiroplasma DNA was only detected in the eggs and larvae derived from some individuals of S. ixodetis-inoculated groups. This has demonstrated the potential of horizontal transmission between different tick species. These findings may help understand the transmission dynamics of Spiroplasma in nature and its adaptation mechanism to host arthropod species.

show abstract

“…The D. melanogaster native Spiroplasma strain is most closely related to that found in Drosophila nebulosa , a willistoni group drosophilid that is sympatric with D. hydei and D. melanogaster in South America [48]. Transinfection from D. nebulosa to D. melanogaster is compatible, with high vertical transmission and low pathology, albeit a little less stable that the native Spiroplasma infection in D. melanogaster [49]. Whilst these experiments have been conducted at different times, it is clear that compatibility is an evolutionarily labile symbiont trait, with the Hy1 strain differing markedly from these Spiroplasma strains.…”

Section: Discussionmentioning

confidence: 99%

Rapid divergence in independent aspects of the compatibility phenotype in a Spiroplasma–Drosophila interaction

2022

View full text Add to dashboard Cite

Heritable symbionts represent important components of the biology, ecology and evolution of their arthropod hosts. Particular microbial taxa have become common across arthropods as a consequence of their ability to establish in new host species. For a host shift to occur, the symbiont must be exposed to a novel host and then be compatible: it must not cause excess pathology, must have good vertical transmission and must possess a drive phenotype that enables spread. Here we investigate the lability of compatibility to symbiosis with Spiroplasma . We used transinfection to establish the protective Spiroplasma symbiont from Drosophila hydei in two closely related novel hosts, Drosophila simulans and Drosophila melanogaster. The Spiroplasma had contrasting compatibility in the two species, exhibiting pathology and low vertical transmission but delivering protection from wasp attack in D. melanogaster but being asymptomatic and transmitted with high efficiency but with lower protection in D. simulans. Further work indicated that pathological interactions occurred in two other members of the melanogaster species group, such that D. simulans was unusual in being able to carry the symbiont without damage. The differing compatibility of the symbiont with these closely related host species emphasizes the rapidity with which host–symbiont compatibility evolves, despite compatibility itself not being subject to direct selection. Further, the requirement to fit three independent components of compatibility (pathology, transmission, protection) is probably to be a major feature limiting the rate of host shifts that will likely impact on the utility of Spiroplasma in pest and vector control. Moving forward, the variation between sibling species pairs provides an opportunity to identify the mechanisms behind variable compatibility, which will drive hypotheses as to the evolutionary drivers of compatibility variation.

show abstract

Phenotype and transmission efficiency of artificial and natural male-killing Spiroplasma infections in Drosophila melanogaster

Cited by 9 publications

References 24 publications

Vertical Transmission of a Drosophila Endosymbiont Via Cooption of the Yolk Transport and Internalization Machinery

Vertical Transmission of a Drosophila Endosymbiont Via Cooption of the Yolk Transport and Internalization Machinery

Investigation of vertical and horizontal transmission of Spiroplasma in ticks under laboratory conditions

Rapid divergence in independent aspects of the compatibility phenotype in a Spiroplasma–Drosophila interaction

Contact Info

Product

Resources

About