Article

Wolbachia density and virulence attenuation after transfer into a novel host

Yale University, New Haven, Connecticut, United States
Proceedings of the National Academy of Sciences (Impact Factor: 9.67). 04/2002; 99(5):2918-23. DOI: 10.1073/pnas.052466499
Source: PubMed

ABSTRACT

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.

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    • "Yet it is not understood how well-known symbioses such as between leafcutter ants and fungi (Mueller et al. 2005; Schultz and Brady 2008), fig wasps and trees (Machado et al. 2001; Herre et al. 2008) or humans and their microbiota (Human Microbiome Project Consortium 2012) originated. Insights are traditionally inferred from comparative studies on closely related species groups such as Wolbachia, which shows the full spectrum of symbiosis, including parasitism, where one partner receives fitness benefits at the expense of the other, commensalism, which brings asymmetrical advantage to one partner at no cost to the other, and mutualism, which favors both (McGraw et al. 2002; Fry et al. 2004). Nevertheless, empirical evidence for the origin of symbiosis remains equivocal because confounding factors in the history of these associations cannot be excluded and, therefore, cause and effect relationships cannot easily be teased apart. "
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    • "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). "
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    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.
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    • "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]. "
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