Abstract
Many intracellular microbial symbionts of arthropods are strictly vertically transmitted and manipulate their host's reproduction in ways that enhance their own transmission. Rare horizontal transmission events are nonetheless necessary for symbiont spread to novel host lineages. Horizontal transmission has been mostly inferred from phylogenetic studies but the mechanisms of spread are still largely a mystery. Here, we investigated transmission of two distantly related bacterial symbionts – Rickettsia and Hamiltonella – from their host, the sweet potato whitefly, Bemisia tabaci, to three species of whitefly parasitoids: Eretmocerus emiratus, Eretmocerus eremicus and Encarsia pergandiella. We also examined the potential for vertical transmission of these whitefly symbionts between parasitoid generations. Using florescence in situ hybridization (FISH) and transmission electron microscopy we found that Rickettsia invades Eretmocerus larvae during development in a Rickettsia-infected host, persists in adults and in females, reaches the ovaries. However, Rickettsia does not appear to penetrate the oocytes, but instead is localized in the follicular epithelial cells only. Consequently, Rickettsia is not vertically transmitted in Eretmocerus wasps, a result supported by diagnostic polymerase chain reaction (PCR). In contrast, Rickettsia proved to be merely transient in the digestive tract of Encarsia and was excreted with the meconia before wasp pupation. Adults of all three parasitoid species frequently acquired Rickettsia via contact with infected whiteflies, most likely by feeding on the host hemolymph (host feeding), but the rate of infection declined sharply within a few days of wasps being removed from infected whiteflies. In contrast with Rickettsia, Hamiltonella did not establish in any of the parasitoids tested, and none of the parasitoids acquired Hamiltonella by host feeding. This study demonstrates potential routes and barriers to horizontal transmission of symbionts across trophic levels. The possible mechanisms that lead to the differences in transmission of species of symbionts among species of hosts are discussed.
Highlights
The occurrence of arthropods serving as hosts for bacterial symbionts is very common
In preliminary screening we found that two species of Eretmocerus, Er. eremicus (Rose & Zolnerowich) and Er. sp. nr. emiratus (Zolnerowich & Rose), were both highly infected with a Rickettsia that had the same 16S rDNA and citrate synthase gene sequences as the Rickettsia in their host, B. tabaci
Symbiont identity The sequences obtained from the Rickettsia and Hamiltonella primers were 99% similar to the sequences of ‘‘Rickettsia endosymbiont of Bemisia tabaci’’ (DQ077707.1) and ‘‘secondary endosymbiont of Bemisia tabaci 16S ribosomal RNA gene’’ (AY429618.1) respectively
Summary
The occurrence of arthropods serving as hosts for bacterial symbionts is very common. This, and the fact that the same secondary symbionts are sometimes found in distantly related hosts, is attributed to rare horizontal transmission events of the symbionts between species [1,10,11]. The routes of horizontal transmission are not very well known, transmission via common host plants and/or common natural enemies has been hypothesized, and phylogenetic evidence for the latter has been provided [12,13,14]. Rare examples of experimentally demonstrated natural intra-specific horizontal transmission include Arsenophonus [15], Wolbachia [16] and a virus [17] in parasitoids, as well as transmission between mates of the same aphid species [18]. While elegant work has shown how Wolbachia colonizes the germ line of a Drosophila host following injection of cured individuals [26], why symbionts fail to become established is not understood
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