Rapid Spread of a Bacterial Symbiont in an Invasive Whitefly Is Driven by Fitness Benefits and Female Bias

Himler, Anna G.; Adachi-Hagimori, Tetsuya; Bergen, Jacqueline E.; Kozuch, Amaranta; Kelly, Suzanne E.; Tabashnik, Bruce E.; Chiel, Elad; Duckworth, Victoria E.; Dennehy, Timothy J.; Zchori-Fein, Einat; Hunter, Martha S.

doi:10.1126/science.1199410

Cited by 415 publications

(451 citation statements)

References 30 publications

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“…Invasions of Wolbachia in Drosophila simulans in California and Rickettsia in Bemisia tabaci in Arizona have been reported in which the infection frequency increased from 0% to near fixation in o100 generations (Turelli and Hoffmann, 1991;Himler et al, 2011). The mitochondrial variation among the five thelytokous strains suggests that multiple infection events have occurred and that the Wolbachia infection has spread (partly) via horizontal transmission.…”

Section: Mtdna Analysismentioning

confidence: 98%

Occasional males in parthenogenetic populations of Asobara japonica (Hymenoptera: Braconidae): low Wolbachia titer or incomplete coadaptation?

2011

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Wolbachia are endosymbiotic bacteria known to manipulate the reproduction of their hosts. Some populations of the parasitoid wasp Asobara japonica are infected with Wolbachia and reproduce parthenogenetically, while other populations are not infected and reproduce sexually. Wolbachia-infected A. japonica females regularly produce small numbers of male offspring. Because all females in the field are infected and infected females are not capable of sexual reproduction, male production seems to be maladaptive. We investigated why these females nevertheless produce males. We tested three hypotheses: high rearing temperatures could result in higher offspring sex ratios (more males), low Wolbachia titer of the mother could lead to higher offspring sex ratios and/or the Wolbachia infection is of relatively recent origin and not enough time has passed to allow complete coadaptation between Wolbachia and host. In all, 33% of the Wolbachia-infected females produced males and 56% of these males were also infected with Wolbachia. Neither offspring sex ratio nor male infection frequency was significantly affected by rearing temperature or Wolbachia concentration of the mother. The mitochondrial DNA sequence of one of the uninfected populations was identical to that of two of the infected populations. Therefore, the initial Wolbachia infection of A. japonica must have occurred recently. Mitochondrial sequence variation among the infected populations suggests that the spread of Wolbachia through the host populations involved horizontal transmission. We conclude that the occasional male production by Wolbachia-infected females is most likely a maladaptive side effect of incomplete coevolution between symbiont and host in this relatively young infection.

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Section: Mtdna Analysismentioning

confidence: 98%

Occasional males in parthenogenetic populations of Asobara japonica (Hymenoptera: Braconidae): low Wolbachia titer or incomplete coadaptation?

2011

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“…For example, a strain of Wolbachia was observed to spread through populations of D. simulans on the west coast of the USA at a rate of 100 km yr -1 [54]. Similarly, a strain of Spiroplasma has been observed to be sweeping through populations of Drosophila neotesteca in North America [55], and in the whitefly Bemisia tabaci from the Southwestern US, a strain of Rickettsia swept from 1 per cent to close to 100 per cent in just 6 years [56]. In D. melanogaster, one strain of Wolbachia has spread through global populations in the last century, replacing all other strains [57].…”

Section: Population Dynamics and The Cost Of Infectionmentioning

confidence: 99%

Vertically transmitted viral endosymbionts of insects: do sigma viruses walk alone?

Longdon

Jiggins

2012

Proc. R. Soc. B.

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Insects are host to a wide range of vertically transmitted bacterial endosymbionts, but we know relatively little about their viral counterparts. Here, we discuss the vertically transmitted viral endosymbionts of insects, firstly examining the diversity of this group, and then focusing on the well-studied sigma viruses that infect dipterans. Despite limited sampling, evidence suggests that vertically transmitted viruses may be common in insects. Unlike bacteria, viruses can be transmitted through sperm and eggs, a trait that allows them to rapidly spread through host populations even when infection is costly to the host. Work on Drosophila melanogaster has shown that sigma viruses and their hosts are engaged in a coevolutionary arms race, in which the spread of resistance genes in the host population is followed by the spread of viral genotypes that can overcome host resistance. In the long-term, associations between sigma viruses and their hosts are unstable, and the viruses persist by occasionally switching to new host species. It therefore seems likely that viral endosymbionts have major impacts on the evolution and ecology of insects.

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“…Indeed, the use of CI and protection against RNA viruses, by Wolbachia in dipterans (Hedges et al, 2008;Teixeira et al, 2008;Moreira et al, 2009;Osborne et al, 2009;Glaser and Meola, 2010;Walker et al, 2011), may explain the recent spread of Wolbachia in natural populations of D. melanogaster (Riegler et al, 2005;Nunes et al, 2008;Richardson et al, 2012), and makes Wolbachia a promising agent for the control of dengue (IturbeOrmaetxe et al, 2011;Walker et al, 2011), a human pathogen transmitted by mosquitoes. Similarly, Rickettsia bacteria associated with whiteflies (order Hemiptera) directly enhance host fitness and also bias sex ratio toward female offspring (Himler et al, 2011). The fitness of Drosophila innubila infected with a male-killing Wolbachia strain is enhanced by both male-killing-dependent (i.e., resource reallocation due to death of male siblings) and male-killing-independent mechanisms (i.e., enhanced fecundity of nutrient-deprived hosts and increased survival to RNA virus infection; Unckless and Jaenike, 2012).…”

Section: Introductionmentioning

confidence: 99%

Male killing Spiroplasma protects Drosophila melanogaster against two parasitoid wasps

et al. 2013

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Maternally transmitted associations between endosymbiotic bacteria and insects are diverse and widespread in nature. Owing to imperfect vertical transmission, many heritable microbes have evolved compensational mechanisms to enhance their persistence in host lineages, such as manipulating host reproduction and conferring fitness benefits to host. Symbiont-mediated defense against natural enemies of hosts is increasingly recognized as an important mechanism by which endosymbionts enhance host fitness. Members of the genus Spiroplasma associated with distantly related Drosophila hosts are known to engage in either reproductive parasitism (i.e., male killing) or defense against natural enemies (the parasitic wasp Leptopilina heterotoma and a nematode). A male-killing strain of Spiroplasma (strain Melanogaster Sex Ratio Organism (MSRO)) co-occurs with Wolbachia (strain wMel) in certain wild populations of the model organism Drosophila melanogaster. We examined the effects of Spiroplasma MSRO and Wolbachia wMel on Drosophila survival against parasitism by two common wasps, Leptopilina heterotoma and Leptopilina boulardi, that differ in their host ranges and host evasion strategies. The results indicate that Spiroplasma MSRO prevents successful development of both wasps, and confers a small, albeit significant, increase in larva-toadult survival of flies subjected to wasp attacks. We modeled the conditions under which defense can contribute to Spiroplasma persistence. Wolbachia also confers a weak, but significant, survival advantage to flies attacked by L. heterotoma. The host protective effects exhibited by Spiroplasma and Wolbachia are additive and may provide the conditions for such cotransmitted symbionts to become mutualists. Occurrence of Spiroplasma-mediated protection against distinct parasitoids in divergent Drosophila hosts suggests a general protection mechanism.

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Rapid Spread of a Bacterial Symbiont in an Invasive Whitefly Is Driven by Fitness Benefits and Female Bias

Cited by 415 publications

References 30 publications

Occasional males in parthenogenetic populations of Asobara japonica (Hymenoptera: Braconidae): low Wolbachia titer or incomplete coadaptation?

Occasional males in parthenogenetic populations of Asobara japonica (Hymenoptera: Braconidae): low Wolbachia titer or incomplete coadaptation?

Vertically transmitted viral endosymbionts of insects: do sigma viruses walk alone?

Male killing Spiroplasma protects Drosophila melanogaster against two parasitoid wasps

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