Wolbachia in scale insects: a distinct pattern of infection frequencies and potential transfer routes via ant associates

Abstract

Wolbachia is one of the most successful endosymbiotic bacteria of arthropods. Known as the master of manipulation, Wolbachia can induce a wide range of phenotypes in its host that can have far-reaching ecological and evolutionary consequences and may be exploited for disease and pest control. However, our knowledge of Wolbachia's distribution and infection rate is unevenly distributed across arthropod groups such as scale insects. We fitted a distribution of within-species prevalence of Wolbachia to our data and compared it to distributions fitted to an up-to-date dataset compiled from surveys across all arthropods. The estimated distribution parameters indicate a Wolbachia infection frequency of 43.6% (at a 10% prevalence threshold) in scale insects. Prevalence of Wolbachia in scale insects follows a distribution similar to exponential decline (most species are predicted to have low prevalence infections), in contrast to the U-shaped distribution estimated for other taxa (most species have a very low or very high prevalence). We observed no significant associations between Wolbachia infection and scale insect traits. Finally, we screened for Wolbachia in scale insect's ecological associates. We found a positive correlation between Wolbachia infection in scale insects and their ant associates, pointing to a possible route of horizontal transfer of Wolbachia.

Host phylogeny and ecological associations best explain Wolbachia host shifts in scale insects Running title: Wolbachia host shifts

“…Intimacy of direct physical interaction between ants and scale insects may provide a route of microbial exchange, as seen in other hemipteran groups (Ivens et al, 2018;Pringle & Moreau, 2017). In a previous study, a positive correlation between Wolbachia infection in scale insects and their associates indicated that ants may play a role in host-shifting (Sanaei, Lin, et al, 2021). Here, we found that only one out of five case of infected ant-scale insect pairs shares the same Wolbachiastrain.…”

“…While we do not have enough statistical power to test which route of transfer is the most common and in which directions these transfers take place, our data support the hypothesis that the associates tested in the current study play a role in host shifting. Although positive correlations were not previously observed between infection of scale insects and their associates (Sanaei, Lin, et al, 2021), here we observed sharing similar Wolbachia strains between pairs of scale insect and not only ants but also wasps, beetles and flies (File S3). In addition, infection by the super-spreader stain "w Sph1" of several species of scale insects, ants, and wasps is another source of evidence for a substantial contribution of associate species in Wolbachia host-shifting in scale insects.…”

“…Despite several similarities with other hemipterans, found that most species are predicted to have low to intermediateWolbachia prevalence, in contrast to a u-shaped distribution (most species have a very low or very high prevalence) predicted for other groups (Hilgenboecker et al, 2008). Also, a positive correlation between Wolbachia infection in scale insects and their associate ants indirectly points to a plausible route of transfer (Sanaei, Lin, et al, 2021). These preliminary results provided a broad view of theWolbachia infection dynamic in scale insects and thus inspired us to investigate Wolbachia strain diversity and consequently hostshifting in scale insects.…”

“…We selected 59 specimens from 29 scale insect species that had tested positive for Wolbachia in a previous Wolbachia screening project (Sanaei, Lin, et al, 2021) (File S2). 16 of these scale insects were collected together with a directly associated insect (including ants, wasps, flies, beetles, moths), and these were also included.…”

Host phylogeny and ecological associations best explain Wolbachia host shifts in scale insects

“…In particular, many are usually observed in close interactions with ants through trophallaxis (where the honeydew produced by the scale insects is consumed by ants) (Buckley & Gullan, 1991;Gullan et al, 1993;Hölldobler et al, 1990). Despite several similarities with other hemipterans, Sanaei, Lin, et al (2021) found that most species are predicted to have low to intermediate Wolbachia prevalence, in contrast to a u-shaped distribution (most species have a very low or very high prevalence) predicted for other groups (Hilgenboecker et al, 2008). Also, a positive correlation between Wolbachia infection in scale insects and their associate ants indirectly points to a plausible route of transfer (Sanaei, Lin, et al, 2021).…”