Evolution of single and double Wolbachia symbioses during speciation in the Drosophila simulans complex.

Abstract

Maternally inherited bacteria of the genus Wolbachia are responsible for the early death of embryos in crosses between uninfected females and infected males in several insect species. This phenomenon, known as cytoplasmic incompatibility, also occurs between strains infected by different symbionts in some species, including Drosophila simulans. Wolbachia was found in two species closely related to D. simulans, Drosophila mauritiana, and Drosophila sechellia, and shown to cause incompatibility in the latter species but not in D. mauritiana. Comparison of bacterial and mtDNA history clarifies the origins of bacterial and incompatibility polymorphisms in D. simulans. Infection in D. mauritiana is probably the result of introgression of an infected D. simulans cytoplasm. Some D. simulans and D. sechellia cytoplasmic lineages harbor two bacteria as a consequence of a double infection which probably occurred in a common ancestor. The descendant symbionts in each species are associated with similar incompatibility relationships, which suggests that little variation of incompatibility types has occurred within maternal lineages beyond that related to the density of symbionts in their hosts. Wolbachia symbionts are responsible for different modifications of sexual reproduction in insects and isopods, including parthenogenesis (1-3), feminization (2, 4), and cytoplasmic incompatibility (2, 5-11). The latter phenornenon is characterized by anomalies in the first mitoses of the zygote (12-15), generally a loss of paternal chromosomes, which results in death of offspring from crosses between uninfected females and infected males or all male progenies in haplodiploid species. The death of offspring of uninfected females favors the spread and maintenance of the infection in natural populations. Incompatibility also occurs in certain crosses between infected individuals harboring different bacterial strains (16)(17)(18)(19). In this case, different incompatibility types are distinguished on the basis of incompatibility relationships.Two cases of incompatibility-type polymorphism have been the subject of detailed studies: the large polymorphism observed in the mosquito Culex pipiens (20)(21)(22) and the more limited one described in Drosophila simulans (15, 19, 23, 24). In the latter species, uninfected flies (type W) and three infected types (R, S, and M) have been distinguished from a large geographical survey. These types are associated with different mitochondrial types, as expected if both mtDNA and symbionts are maternally transmitted. However, there was heritable variation of incompatibility properties of S strains (23). Incompatibility-type polymorphism can have many causes, including variation of symbionts themselves or variation of symbiont density in their hosts (11, 23, 25, 26). In Drosophila, a simple method to assess density effects in males is to measure the frequency of infected sperm cysts duringThe publication costs of this article were defrayed in part by page charge payment. This article must therefor...

Characterization of non-cytoplasmic incompatibility inducing Wolbachia in two continental African populations of Drosophila simulans

“…This is expected because Wolbachia and mitochondria are transmitted together through the egg cytoplasm so that they should remain associated over time (provided that horizontal and/or paternal transmission of Wolbachia and/or mitochondria are not too frequent). Thus, the wRi and wAu variants are associated with the siII haplotype (Hale and Hoffmann, 1990;James and Ballard, 2000), the wHa and wNo variants are associated with the siI haplotype (Montchamp-Moreau et al, 1991;Rousset and Solignac, 1995), and the wMa variant is associated with the siIII haplotype (Rousset et al, 1992). As shown here, wKi is also associated with siIII.…”

“…Three variants have been shown to induce CI when present in males and to rescue from their own effect when present in females: wRi (Hoffmann et al, 1986), wHa (O'Neill and Karr, 1990) and wNo (Merçot et al, 1995). Three other variants have been described that do not seem to induce CI when present in males: wMa (Rousset and Solignac, 1995), wAu (Hoffmann et al, 1996) and wKi (Merçot and Poinsot, 1998a;Poinsot and Merçot, 1999). Furthermore, wKi has been demonstrated to possess a functional resc: eggs infected by wKi are rescued in crosses with wNo-infected males (Merçot and Poinsot, 1998a;Poinsot and Merçot, 1999).…”

Genome comparisons indicate recent transfer ofwRi‐likeWolbachiabetween sister speciesDrosophila suzukiiandD. subpulchrella

“…Given that on the order of half of Drosophila speciation events show evidence for reinforcement (i.e., accelerated rates of evolution for premating isolation associated with overlapping ranges) (Coyne & Orr, 1989, 1997; Turelli, Lipkowitz, & Brandvain, 2014), hybridization is apparently common among sister species of Drosophila . Introgression has been invoked to explain the closely related Wolbachia found within the simulans and yakuba clades in the D. melanogaster subgroup (Lachaise et al., 2000; Rousset & Solignac, 1995). In both cases, the introgression hypothesis is favored over horizontal transmission because the hosts also share essentially identical mitochondrial DNA.…”

Cloning and sequencing of wsp encoding gene fragments reveals a diversity of co-infecting Wolbachia strains in Acromyrmex leafcutter ants

“…Sequences generated in this study are indicated in bold. The bar represents a distance of 0.050 (about 25 MY if a wsp evolutionary rate of 0.2% per MY is assumed, Wenseleers et al, 2001). and Solignac, 1995;Wenseleers et al, 1998;Werren et al, 1995a, b;Werren and Windsor, 2000) or more rarely, triple infections (Kondo et al, 2002;Vavre et al, 1999). A stable triple Wolbachia infection has also been created artificially by microinjection of an additional strain in double infected Drosophila (Rousset et al, 1999).…”