Abstract

BackgroundAfter decades during which endosymbionts were considered as silent in their hosts, in particular concerning the immune system, recent studies have revealed the contrary. In the present paper, we addressed the effect of Wolbachia, the most prevalent endosymbiont in arthropods, on host immunocompetence. To this end, we chose the A. vulgare-Wolbachia symbiosis as a model system because it leads to compare consequences of two Wolbachia strains (wVulC and wVulM) on hosts from the same population. Moreover, A. vulgare is the only host-species in which Wolbachia have been directly observed within haemocytes which are responsible for both humoral and cellular immune responses.Methodology/Principal FindingsWe sampled gravid females from the same population that were either asymbiotic, infected with wVulC, or infected with wVulM. The offspring from these females were tested and it was revealed that individuals harbouring wVulC exhibited: (i) lower haemocyte densities, (ii) more intense septicaemia in their haemolymph and (iii) a reduced lifespan as compared to individuals habouring wVulM or asymbiotic ones. Therefore, individuals in this population of A. vulgare appeared to suffer more from wVulC than from wVulM. Symbiotic titer and location in the haemocytes did not differ for the two Wolbachia strains showing that these two parameters were not responsible for differences observed in their extended phenotypes in A. vulgare.Conclusion/SignificanceThe two Wolbachia strains infecting A. vulgare in the same population induced variation in immunocompetence and survival of their hosts. Such variation should highly influence the dynamics of this host-symbiont system. We propose in accordance with previous population genetic works, that wVulM is a local strain that has attenuated its virulence through a long term adaptation process towards local A. vulgare genotypes whereas wVulC, which is a widespread and invasive strain, is not locally adapted.

Highlights

  • Investigations on the consequences of endosymbionts on their host’s fitness have revealed that some of them exhibit variable effects, blurring the distinction between mutualism and parasitism

  • We evaluated in A. vulgare individuals infected by wVulC or wVulM: (i) the titer of Wolbachia in ovaries by qPCR (ii) the presence of Wolbachia in haemocytes by electronic microscopy, (iii) the density of haemocytes, (iv) the intensity of natural septicaemia (v) their survival over a 7 month period

  • For Wolbachia, which are the most frequent endosymbiotic bacteria in arthropods, two recent studies suggest that they may interact with the host immune system and modify the host’s ability to overcome infection by other parasites [19,22]

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Summary

Introduction

Investigations on the consequences of endosymbionts on their host’s fitness have revealed that some of them exhibit variable effects, blurring the distinction between mutualism and parasitism. Of the endosymbionts known to exhibit various effects on their host fitness, Wolbachia are the most prevalent in arthropods. As the transmission of Wolbachia is vertical, their fitness is directly linked to the fitness of their hosts Such situations could be seen as favourable to evolve towards obligate symbiosis and mutualism. Such obligate Wolbachia symbioses have only been described in filarial nematodes and in the parasitic wasp Asobara tabida [4,5]. We addressed the effect of Wolbachia, the most prevalent endosymbiont in arthropods, on host immunocompetence. A. vulgare is the only host-species in which Wolbachia have been directly observed within haemocytes which are responsible for both humoral and cellular immune responses

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