Endosymbiotic Wolbachia infect a number of arthropod species in which they can affect the reproductive system. While maternally transmitted, unlike mitochondria their molecular phylogeny does not parallel that of their hosts. This strongly suggests horizontal transmission among species, the mechanisms of which remain unknown. Such transfers require intimate between-species relationships, and thus host-parasite associations are outstandingly appropriate for study. Here, we demonstrate that hymenopteran parasitoids of frugivorous Drosophila species are especially susceptible to Wolbachia infection. Of the five common European species, four proved to be infected; furthermore, multiple infections are common, with one species being doubly infected and two triply infected (first report). Phylogenetic statuses of the Wolbachia infecting the different species of the community have been studied using the gene wsp, a highly variable gene recently described. This study reveals exciting similarities between the Wolbachia variants found in parasitoids and their hosts. These arguments strongly support the hypothesis of frequent natural Wolbachia transfers into other species and open a new field for genetic exchanges among species, especially in host-parasitoid associations.

Transposable elements (TEs) make up around 10%-15% of the Drosophila melanogaster genome, but its sibling species Drosophila simulans carries only one third as many such repeat sequences. We do not, however, have an overall view of copy numbers of the various classes of TEs (long terminal repeat [LTR] retrotransposons, non-LTR retrotransposons, and transposons) in genomes of natural populations of both species. We analyzed 34 elements in individuals from various natural populations of these species. We show that D. melanogaster has higher average chromosomal insertion site numbers per genome than D. simulans for all TEs except five. The LTR retrotransposons gypsy, ZAM, and 1731 and the transposon bari-1 present similar low copy numbers in both species. The transposon hobo has a large number of insertion sites, with significantly more sites in D. simulans. High variation between populations in number of insertion sites of some elements of D. simulans suggests that these elements can invade the genome of the entire species starting from a local population. We propose that TEs in the D. simulans genome are being awakened and amplified as they had been a long time ago in D. melanogaster.

We present a detailed case history of the origin and evolution of a new essential gene and, in so doing, provide the first molecular identification of a Drosophila paternal effect gene, ms(3)K81 (K81).

Genome size varies considerably between species, and transposable elements (TEs) are known to play an important role in this variability. However, it is far from clear whether TEs are involved in genome size differences between populations within a given species. We show here that in Drosophila melanogaster and Drosophila simulans the size of the genome varies among populations and is correlated with the TE copy number on the chromosome arms. The TEs embedded within the heterochromatin do not seem to be involved directly in this phenomenon, although they may contribute to differences in genome size. Furthermore, genome size and TE content variations parallel the worldwide colonization of D. melanogaster species. No such relationship exists for the more recently dispersed D. simulans species, which indicates that a quantitative increase in the TEs in local populations and fly migration are sufficient to account for the increase in genome size, with no need for an adaptation hypothesis.

Some species of parasitic wasps have domesticated viral machineries to deliver immunosuppressive factors to their hosts. Up to now, all described cases fall into the Ichneumonoidea superfamily, which only represents around 10% of hymenoptera diversity, raising the question of whether such domestication occurred outside this clade. Furthermore, the biology of the ancestral donor viruses is completely unknown. Since the 1980’s, we know that Drosophila parasitoids belonging to the Leptopilina genus, which diverged from the Ichneumonoidea superfamily 225My ago, do produce immuno-suppressive virus-like structure in their reproductive apparatus. However, the viral origin of these structures has been the subject of debate. In this paper, we provide genomic and experimental evidence that those structures do derive from an ancestral virus endogenization event. Interestingly, its close relatives induce a behaviour manipulation in present-day wasps. Thus, we conclude that virus domestication is more prevalent than previously thought and that behaviour manipulation may have been instrumental in the birth of such associations.

For insects, the prevalence of numerous vertically transmitted viruses can be high in their host populations. These viruses often have few, if any, pathological effects on their hosts, and consequently, many of them can remain unnoticed for long periods, despite their potential role in the evolution of the host phenotype. Some females of Leptopilina boulardi, a solitary parasitoid of Drosophila larvae, are infected by an inherited virus (LbFV) that manipulates the behavior of the wasp by increasing its tendency to lay eggs in a host that is already parasitized (superparasitism). This behavioral alteration allows horizontal transmission of the virus within superparasitized Drosophila larvae. Using suppressive subtractive hybridization with infected and uninfected lines, we identified one putative viral sequence. Based on this sequence, we developed a simple PCR test. We tested the correlation between the superparasitism phenotype and PCR amplification of the putative viral marker using several experimental conditions (including horizontal transfers) and several parasitoid genotypes. All of the results revealed that there was a perfect match between the superparasitism phenotype and the amplification profile, which validated use of the molecular marker as a tool to track the presence of the virus and provided the first genomic data for this fascinating virus. The results also show that there was very efficient horizontal and vertical transmission of LbFV, which probably explains its high prevalence in the French populations that we sampled (67 and 70% of infected females). This manipulative virus is likely to play a major role in the ecology and evolution of its parasitoid host.

Parasites are sometimes able to manipulate the behavior of their hosts. However, the molecular cues underlying this phenomenon are poorly documented. We previously reported that the parasitoid wasp Leptopilina boulardi which develops from Drosophila larvae is often infected by an inherited DNA virus. In addition to being maternally transmitted, the virus benefits from horizontal transmission in superparasitized larvae (Drosophila that have been parasitized several times). Interestingly, the virus forces infected females to lay eggs in already parasitized larvae, thus increasing the chance of being horizontally transmitted. In a first step towards the identification of virus genes responsible for the behavioral manipulation, we present here the genome sequence of the virus, called LbFV. The sequencing revealed that its genome contains an homologous repeat sequence (hrs) found in eight regions in the genome. The presence of this hrs may explain the genomic plasticity that we observed for this genome. The genome of LbFV encodes 108 ORFs, most of them having no homologs in public databases. The virus is however related to Hytrosaviridae, although distantly. LbFV may thus represent a member of a new virus family. Several genes of LbFV were captured from eukaryotes, including two anti-apoptotic genes. More surprisingly, we found that LbFV captured from an ancestral wasp a protein with a Jumonji domain. This gene was afterwards duplicated in the virus genome. We hypothesized that this gene may be involved in manipulating the expression of wasp genes, and possibly in manipulating its behavior.

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