Wolbachia density and virulence attenuation after transfer into a novel host

Section of Vector Biology, Department of Epidemiology and Public Health, Yale University School of Medicine, 60 College Street, New Haven, CT 06520, USA.
Proceedings of the National Academy of Sciences (Impact Factor: 9.67). 04/2002; 99(5):2918-23. DOI: 10.1073/pnas.052466499
Source: PubMed


The factors that control replication rate of the intracellular bacterium Wolbachia pipientis in its insect hosts are unknown and difficult to explore, given the complex interaction of symbiont and host genotypes. Using a strain of Wolbachia that is known to over-replicate and shorten the lifespan of its Drosophila melanogaster host, we have tracked the evolution of replication control in both somatic and reproductive tissues in a novel host/Wolbachia association. After transinfection (the transfer of a Wolbachia strain into a different species) of the over-replicating Wolbachia popcorn strain from D. melanogaster to Drosophila simulans, we demonstrated that initial high densities in the ovaries were in excess of what was required for perfect maternal transmission, and were likely causing reductions in reproductive fitness. Both densities and fitness costs associated with ovary infection rapidly declined in the generations after transinfection. The early death effect in D. simulans attenuated only slightly and was comparable to that induced in D. melanogaster. This study reveals a strong host involvement in Wolbachia replication rates, the independence of density control responses in different tissues, and the strength of natural selection acting on reproductive fitness.

Download full-text


Available from: David J Merritt,
13 Reads
  • Source
    • "A second, and not mutually exclusive hypothesis, is that rapid adaptation of symbionts to novel host environments permits long-term persistence of symbionts whose initial performance in a host is poor. Indeed, several studies have shown attenuated direct costs to the fitness of the host over time in the virulent 'popcorn' strain of Wolbachia (McGraw et al., 2002; Carrington et al., 2010), as well as evolution towards mutualism of strains in nature (Weeks et al., 2007). The genus Spiroplasma is one of the most common maternally inherited endosymbiont groups, with a wide range of hosts including insects, crustaceans, arachnids and plants (Gasparich et al., 2004). "
    [Show abstract] [Hide abstract]
    ABSTRACT: Maternally inherited symbionts are common in arthropods and many have important roles in host adaptation. The observation that specific symbiont lineages infect distantly related host species implies new interactions are commonly established by lateral transfer events. However, studies have shown that symbionts often perform poorly in novel hosts. We hypothesized selection on the symbiont may be sufficiently rapid that poor performance in a novel host environment is rapidly ameliorated, permitting symbiont maintenance. Here, we test this prediction for a Spiroplasma strain transinfected into the novel host Drosophila melanogaster. In the generations immediately following transinfection, the symbiont had low transmission efficiency to offspring and imposed severe fitness costs on its host. We observed that effects on host fitness evolved rapidly, being undetectable after 17 generations in the novel host, whereas vertical transmission efficiency was poorly responsive over this period. Our results suggest that long-term symbiosis may more readily be established in cases where symbionts perform poorly in just one aspect of symbiosis.Heredity advance online publication, 4 February 2015; doi:10.1038/hdy.2014.112.
    Heredity 02/2015; 114(6). DOI:10.1038/hdy.2014.112 · 3.81 Impact Factor
  • Source
    • "The exponential growth of the symbiont may be the cause of the life-shortening, either by direct tissue damage or by constituting a significant metabolic burden compromising the insect's health. This is reminiscent of host life-shortening by the exponentially growing wMelPop strain [15], [17], [44]. "
    [Show abstract] [Hide abstract]
    ABSTRACT: Wolbachia, endosymbionts that reside naturally in up to 40-70% of all insect species, are some of the most prevalent intracellular bacteria. Both Wolbachia wAu, naturally associated with Drosophila simulans, and wMel, native to Drosophila melanogaster, have been previously described to protect their hosts against viral infections. wMel transferred to D. simulans was also shown to have a strong antiviral effect. Here we directly compare one of the most protective wMel variants and wAu in D. melanogaster in the same host genetic background. We conclude that wAu protects better against viral infections, it grows exponentially and significantly shortens the lifespan of D. melanogaster. However, there is no difference between wMel and wAu in the expression of selected antimicrobial peptides. Therefore, neither the difference in anti-viral effect nor the life-shortening could be attributed to the immune stimulation by exogenous Wolbachia. Overall, we prove that stable transinfection with a highly protective Wolbachia is not necessarily associated with general immune activation.
    PLoS ONE 06/2014; 9(6):e99025. DOI:10.1371/journal.pone.0099025 · 3.23 Impact Factor
  • Source
    • "(Serbus et al., 2008). Along with reproductive organs, Wolbachia are also revealed in different tissues of larvae and adult hosts (Dobson et al., 1999; McGraw et al., 2002; Clark et al., 2005; Zhukova et al., 2008). The influence of Wolbachia var ies from mutualistic to parasitic, depending on the host species and bacteria strain (Serbus et al., 2008). "
    [Show abstract] [Hide abstract]
    ABSTRACT: The pathogenic Wolbachia strain wMelPop is detected in the central nervous system, muscles, and retina of Drosophila melanogaster. It reduces the host lifespan by a factor of two. This fact makes it promising for the control of insect pests and vectors of human diseases. Any symbiotic association is exposed to various stress factors: starvation, heat, cold and etc., which affect the symbiont interaction significantly. This study considers the influence of low (16°C) and high (29°C) temperature on the survival and lifespan of D. melanogaster females infected with the Wolbachia strain wMelPop. The ultrastructure of brain cells and distribution of the bacteria in this cells were studied. On day 7 of exposure to high temperature, electron-dense bodies occur in brain cells of the flies, resembling degrading bacteria. The amount of these bodies increases dramatically by day 13 of incubation at 29°C. On the basis of population and EM analysis, we identified the critical period (7–13 days) of high temperature influence, which dramatically decreases the survival of D. melanogaster.
    Russian Journal of Genetics: Applied Research 11/2013; 3(6). DOI:10.1134/S2079059713060099
Show more