Wolbachia-induced incompatibility precedes other hybrid incompatibilities in Nasonia

Abstract

Wolbachia are cytoplasmically inherited bacteria that cause a number of reproductive alterations in insects, including cytoplasmic incompatibility, an incompatibility between sperm and egg that results in loss of sperm chromosomes following fertilization. Wolbachia are estimated to infect 15-20% of all insect species, and also are common in arachnids, isopods and nematodes. Therefore, Wolbachia-induced cytoplasmic incompatibility could be an important factor promoting rapid speciation in invertebrates, although this contention is controversial. Here we show that high levels of bidirectional cytoplasmic incompatibility between two closely related species of insects (the parasitic wasps Nasonia giraulti and Nasonia longicornis) preceded the evolution of other postmating reproductive barriers. The presence of Wolbachia severely reduces the frequency of hybrid offspring in interspecies crosses. However, antibiotic curing of the insects results in production of hybrids. Furthermore, F1 and F2 hybrids are completely viable and fertile, indicating the absence of F1 and F2 hybrid breakdown. Partial interspecific sexual isolation occurs, yet it is asymmetric and incomplete. Our results indicate that Wolbachia-induced reproductive isolation occurred in the early stages of speciation in this system, before the evolution of other postmating isolating mechanisms (for example, hybrid inviability and hybrid sterility).

Host genotype changes bidirectional to unidirectional cytoplasmic incompatibility in Nasonia longicornis

“…As Nasonia has a haplodiploid mode of sex determination the zygotic death manifests itself in the diploid daughters, but not in the haploid sons. CI results in the loss of paternal chromatin, whereby most of the diploid zygotes are killed but some get transformed into males, which increases the number of sons in the progeny family size of an incompatible cross (Bordenstein et al, 2001). Thus, incompatible crosses in N. longicornis can be distinguished from a compatible cross by a reduction in the number of daughters and a slight increase in the number of sons.…”

“…Statistical analysis CI in N. longicornis is expressed primarily as a reduction in the number of daughters and a slight increase in the number of sons in an incompatible cross (Bordenstein et al, 2001). As Nasonia has a haplodiploid mode of sex determination the zygotic death manifests itself in the diploid daughters, but not in the haploid sons.…”

“…Presence of more than one incompatibility type has been found in a number of different insects including mosquitoes, fruit flies, beetles and wasps (Laven, 1959;Breeuwer and Werren, 1990;O'Neill and Karr, 1990;Montchamp-Moreau et al, 1991;PerrotMinnot et al, 1996;Bordenstein et al, 2001). Bidirectional CI (bi-CI) has attracted particular attention because of its potential role in preventing gene flow between two different incompatibility types and thus contributing to reproductive isolation and speciation (Breeuwer and Werren, 1990;Werren, 1998;Bordenstein et al, 2001;Bordenstein, 2003;Telschow et al, 2002Telschow et al, , 2005a.…”

“…Some of the mechanisms by which Wolbachia achieve this are killing of infected males, induction of parthenogenesis in infected females, feminization of genetic males and cytoplasmic incompatibility (CI) (reviewed in Werren et al, 2008). As a result, Wolbachia-induced host-reproductive manipulation has profound implications for many fundamental biological processes, such as sex determination (Rigaud et al, 1997;Werren and Beukeboom, 1998), sexual selection (Jiggins et al, 2000;Koukou et al, 2006), speciation (Laven, 1959;Breeuwer and Werren, 1990;Bordenstein et al, 2001;Jaenike et al, 2006) and organization of host genome structure (Kondo et al, 2002b, Dunning-Hotopp et al, 2007.…”

Influence of Antibiotic Treatment and Wolbachia Curing on Sexual Isolation Among Drosophila Melanogaster Cage Populations

“…Indirect evidence for a possible role of Wolbachia in speciation includes studies showing bidirectional CI (bi-CI) (Bordenstein et al 2001) and unidirectional CI (uni-CI) (Shoemaker et al 2000) contributing to reproductive incompatibility between closely related species. Theoretical studies show that both uni-and bi-CI can promote divergence between populations (Telschow et al 2002a,b) and probably reinforce premating isolation (Telschow et al 2005a,b) in the face of substantial gene flow.…”