Wolbachia and host intrinsic reproductive barriers contribute additively to postmating isolation in spider mites

Abstract

Wolbachia are widespread maternally-inherited bacteria suggested to play a role in arthropod host speciation through induction of cytoplasmic incompatibility, but this hypothesis remains controversial. Most studies addressing Wolbachia-induced incompatibilities concern closely-related populations, which are intrinsically compatible. Here, we used three populations of two genetically differentiated colour forms of the haplodiploid spider mite Tetranychus urticae to dissect the interaction between Wolbachia-induced and host-associated incompatibilities, and to assess their relative contribution to post-mating isolation. We found that these two sources of incompatibility act through different mechanisms in an additive fashion. Host-associated incompatibility contributes 1.5 times more than Wolbachia-induced incompatibility in reducing hybrid production, the former through an overproduction of haploid sons at the expense of diploid daugters (ca. 75% decrease) and the latter by increasing the embryonic mortality of daughters (by ca. 49%). Furthermore, regardless of cross direction, we observed nearcomplete F1 hybrid sterility and complete F2 hybrid breakdown between populations of the two forms, but that Wolbachia did not contribute to this outcome. This study identifies the mechanistic independence and additive nature of host-intrinsic and Wolbachia-induced sources of isolation. It suggests that Wolbachia could drive reproductive isolation in this system, thereby potentially affecting host differentiation and distribution in the field.

Interacting host modifier systems control Wolbachia-induced cytoplasmic incompatibility in a haplodiploid mite

“…Morphological classification showed that the Bch line is distinct from T. urticae (electronic supplementary material) and compatible control crosses of T. urticae males of all near-isogenic lines and uninfected Bch females produced hybrid F1 females. Virgin F1 females did not oviposit across our cross types (n= five females per cross type, if present), a post-zygotic reproductive barrier that is commonly observed in interspecific crosses with Tetranychus mites [38,39].…”

“…Introgressive transfer of Wolbachia into the Bch nuclear background failed since F1 females did not oviposit. Hybrid sterility is a pervasive post-zygotic reproductive barrier between tetranychid species [38,39]. We morphologically classified the Bch line (electronic supplementary material).…”

“…where MDobs and MDc are the estimated MD values in the incompatible and respective compatible crosses, respectively [25, 39,43]. The corrected FM-CI phenotype (FMcorr) was calculated using the estimated FM values;…”

“…where FMobs and FMc are the estimated FM values in the incompatible and respective compatible crosses, respectively (based on [25, 39,43]).…”

Interacting host modifier systems controlWolbachia-induced cytoplasmic incompatibility in a haplodiploid mite

“…where MD obs and MD c are the estimated MD values in the incompatible and respective compatible crosses (Poinsot et al 1998;Zélé et al 2020;Cruz et al 2021). The corrected FM-CI phenotype (FM corr ) was calculated using the estimated FM values;…”