Cryptic diversity, reproductive isolation and cytoplasmic incompatibility in a classic biological control success story

Abstract

Molecular genetics and symbiont diagnostics have revolutionized our understanding of insect species diversity, and the transformative effects of bacterial symbionts on host life history. Encarsia inaron is a parasitoid wasp that has been shown to harbour two bacterial endosymbionts, Wolbachia and Cardinium. Known then as E. partenopea, it was introduced to the USA in the late 1980s from populations collected in Italy and Israel for the biological control of an ornamental tree pest, the ash whitefly, Siphoninus phillyreae. We studied natural populations from sites in the USA, the Mediterranean and the Middle East as well as from a Cardinium‐infected laboratory culture established from Italy, with the aims of characterizing these populations genetically, testing reproductive isolation, determining symbiont infection status in their native and introduced range, and determining symbiont role. The results showed that the two Encarsia populations introduced to the USA are genetically distinct, reproductively isolated, have different symbionts and different host–symbiont interactions, and can be considered different biological species. One (‘E. inaron’) is doubly infected by Wolbachia and Cardinium, while only Cardinium is present in the other (‘E. partenopea’). The Cardinium strains in the two species are distinct, although closely related, and crossing tests indicate that the Cardinium infecting ‘E. partenopea’ induces cytoplasmic incompatibility. The frequency of symbiont infection found in the native and introduced range of these wasps was similar, unlike the pattern seen in some other systems. These results also lead to a retelling of a successful biological control story, with several more characters than had been initially described.

A revision of the Encarsia pergandiella species complex (Hymenoptera: Aphelinidae) shows cryptic diversity in parasitoids of whitefly pests

“…This result is consistent with previous studies showing that the region 28S‐D2 is conserved, if not invariant, among closely related species of chalcidoids that are well differentiated biologically and for the COI sequence (Heraty et al., ; Gebiola et al., ). As an example, a single 28S‐D2 polymorphism has been found to discriminate cryptic species characterized by consistent variation in COI sequences in Eulophidae (Gebiola et al., ; Nugnes et al., ), as well as in the genus Encarsia (Gebiola et al ., ). As for COI, the level of divergence found between the three lineages (3.4–5%) is similar to or even higher than that found between cryptic species of other parasitoid wasps (Heraty et al., ; Gebiola et al ., ; Nugnes et al., ).…”

“…Wolbachia in Encarsia formosa Gahan ( van Meer et al, 1999;Zchori-Fein et al, 2001) and Cardinium in all other examined species (Zchori-Fein et al, 2001Giorgini et al, 2009). Further, in some species, these bacterial symbionts cause cytoplasmic incompatibility, a form of reproductive incompatibility occurring when uninfected females mate with infected males, while the other three possible crosses between symbiont-infected and uninfected males and females produce normal numbers of offspring (Hunter et al, 2003;Perlman et al, 2006;Gebiola et al, 2016).…”

“…The taxonomy and systematics of Encarsia have greatly benefited from the use of molecular markers, such as the expansion region D2 of the ribosomal gene 28S (Babcock & Heraty, 2000;Babcock et al, 2001;Manzari et al, 2002) and the mitochondrial gene cytochrome c oxidase subunit I (COI) (de León et al, 2010). However, the problem of genetically identifying cryptic species of Encarsia has been tackled only twice, using COI alone (Monti et al, 2005) or in combination with 28S-D2 (Gebiola et al, 2016). The application of multivariate morphometrics to revise species groups of Encarsia has also been useful (Heraty & Polaszek, 2000;Pedata & Polaszek, 2003;Polaszek et al, 2004), and has enabled the discovery of cryptic species (Manzari et al, 2002;Giorgini & Baldanza, 2004).…”

Reproductive isolation due to prezygotic isolation and postzygotic cytoplasmic incompatibility in parasitoid wasps

“…Prezygotic ecological isolation and sexual isolation seem to be common (Bredlau & Kester, 2015;Danci et al, 2006;Gounou, Chabi-Olaye, Poehling, & Schulthess, 2008;Heimpel, Antolin, Franqui, & Strand, 1997;Joyce et al, 2010;Kaiser et al, 2015;Sundaralingam, Hower, & Kim, 2001), also in populations which must have been separated only very recently (Desneux et al, 2009). CI due to the endosymbionts Wolbachia or Cardinium has been reported in several parasitoid systems (Wolbachia: e.g., Bordenstein et al, 2001;Bordenstein & Werren, 2007;Branca, Ru, Vavre, Silvain, & Dupas, 2011;Gebiola, White, et al, 2016;Cardinium: Gotoh, Noda, & Ito, 2007;Perlman, Kelly, & Hunter, 2008;Zhang, Zhao, & Hong, 2012;. Apart from CI, only very few studies exist on intrinsic postzygotic barriers, especially for those barriers affecting males.…”

Independent cytoplasmic incompatibility induced byCardiniumandWolbachiamaintains endosymbiont coinfections in haplodiploid thrips populations

“…All these factors define the infection threshold beyond which infection frequencies in host populations will either increase (toward a stable equilibrium or fixation of infection) or decrease (toward loss of infection). The strength of Wolbachia CI can depend on the bacterial genotype (Charlat et al 2004), the host genotype (Bordenstein et al 2003), temperature (Hoffmann et al 1986;Clancy and Hoffmann 1998) and bacterial density (Breeuwer and Werren 1993;Bourtzis et al 1996;Mouton et al 2003), but less is known for Cardinium except for the reports of host developmental factors (Perlman et al 2014) and genotypic effects (Ros and Breeuwer 2009;Gebiola et al 2016b). The strength of Wolbachia CI can depend on the bacterial genotype (Charlat et al 2004), the host genotype (Bordenstein et al 2003), temperature (Hoffmann et al 1986;Clancy and Hoffmann 1998) and bacterial density (Breeuwer and Werren 1993;Bourtzis et al 1996;Mouton et al 2003), but less is known for Cardinium except for the reports of host developmental factors (Perlman et al 2014) and genotypic effects (Ros and Breeuwer 2009;Gebiola et al 2016b).…”