Wolbachia prevalence patterns: horizontal transmission, recombination, and multiple infections in chestnut gall wasp‐parasitoid communities

Abstract

The Oriental chestnut gall wasp, Dryocosmus kuriphilus Yasumatsu (Hymenoptera: Cynipidae), is a global invasive pest that causes serious damage to almost all chestnut species belonging to the Castanea genus (Fagaceae). Dryocosmus zhuili Liu et Zhu is a recently described sibling species of D. kuriphilus, which induces galls on Castanea henryi (Skan) Rehd. et Wils. There are many indigenous parasitoid species in China which play an important role in the natural regulation of their population dynamics. Wolbachia is a maternally inherited α‐proteobacterium widely found in arthropods. This study screened for the presence of Wolbachia in the two chestnut gall wasps and in six parasitoid species from 12 populations, to investigate the prevalence patterns of Wolbachia in the chestnut gall wasp‐parasitoid communities. We found that D. zhuili and four parasitoid species were infected with Wolbachia; among them, all individuals of the two populations of Megastigmus sp. had multiple Wolbachia infections. By using multilocus sequence types to characterize bacterial strains, three new sequence types were identified. The Wolbachia strains infecting D. zhuili (ST‐507), Torymus sinensis Kamijo (ST‐508), and Sycophila variegata (Curtis) (ST‐508) belonged to supergroup A, whereas the Wolbachia strain infecting Megastigmus nipponicus Kamijo (ST‐503) belonged to supergroup B. Our results also suggested that horizontal transmission of Wolbachia occurs between chestnut gall wasps and their parasitoids. Moreover, multiple Wolbachia infections of Megastigmus sp. may be due to gene recombination and horizontal transmission.

A Case of Intragenic Recombination Dramatically Impacting the Phage WO Genetic Diversity in Gall Wasps

“…On the contrary, other six gall wasp species infected with double or multiple Wolbachia strains harbored diverse types of phage WOs: A. hakonensis with 27 types, Andricus sp2 with 10 types, Latuspina sp1 with nine types, P. masudai and Latuspina sp2 with three types, and Andricus sp3 with four types. The presence of multiple Wolbachia strains has been documented in several insect species ( van Borm et al, 2001 ; Jamnongluk et al, 2002 ; Reuter and Keller, 2003 ; Hou et al, 2020 ). For gall wasps, a high level of multiple Wolbachia infections was found in A. mukaigawae and its associated inquiline Synergus japonicus with five and eight strains, respectively ( Yang et al, 2013 ), and Belonocnema treatae with four strains ( Schuler et al, 2018 ).…”

“…In the closed system of galls, living organisms include gall formers, inquilines, parasitoids, Wolabchia , phage WO, and so forth. Gall inducer-inquiline association ( Yang et al, 2013 ) and host-parasitoid association ( Hou et al, 2020 ) are two known routes of horizontal transmission of Wolbachia in gall wasps. In three inquilines, Synergus sp1 (including individual insects obtained from the galls made by different gall wasps) and Synergus sp3 were infected with the same Wolbachia strain, while Synergus sp2 was infected with another Wolbachia strain ( Supplementary Figure 6 ); however, they all carried the same phage WO type.…”

“…The phage WO type was also detected in A. hakonensis . D. zhuili , and A. mairei infected with different Wolbachia strains ( Hou et al, 2020 ), but they carried phage WO with identical orf7 sequence. Therefore, it was highly likely that phage WOs were transferred in gall wasp species through gall inducer-inquiline association (and host-parasitoid association) with or without Wolbachia .…”

“…In addition to true gall formers, the Cynipidae also include phytophagous inquilines, which live inside the galls of other species. Several studies have revealed Wolbachia infection in diverse cynipid species with high infection rates ( Plantard et al, 1998 ; Abe and Miura, 2002 ; Rokas et al, 2002 ; Zhu et al, 2007 ; Yang et al, 2013 ; Hou et al, 2020 ; Zhao et al, 2021 ), and some gall wasp species show multiple Wolbachia infections ( Yang et al, 2013 ; Hou et al, 2020 ). The results of Yang et al (2013) suggested a potential possibility of plant tissue-mediated Wolbachia horizontal transmission between gall inducers and their associated inquilines.…”

Wolbachiahost shifts: routes, mechanisms, constraints and evolutionary consequences

“…All of these features may increase the probability of parasitism‐mediated host shifts. Not surprisingly therefore, these pervasive ecological interactions have been found to facilitate horizontal transfer, notably in the case of Wolbachia and host–parasitoid interactions (Cook & Butcher, 1999; Heath et al ., 1999; Vavre et al ., 1999; Hunter, Perlman, & Kelly, 2003; Kittayapong et al ., 2003; Huigens et al ., 2004 b ; Raychoudhury et al ., 2009; Kageyama et al ., 2010; Morrow et al ., 2014; Ahmed et al ., 2015; Klopfstein et al ., 2018; Hou et al ., 2020).…”