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

Abstract

Wolbachia are among the most prevalent and widespread endosymbiotic bacteria on Earth. Wolbachia's success in infecting an enormous number of arthropod species is attributed to two features: the range of phenotypes they induce in their hosts, and their ability to switch between host species. Whilst much progress has been made in elucidating their induced phenotypes, our understanding of Wolbachia host‐shifting is still very limited: we lack answers to even fundamental questions concerning Wolbachia's routes of transfer and the importance of factors influencing host shifts. Here, we investigate the diversity and host‐shift patterns of Wolbachia in scale insects, a group of arthropods with intimate associations with other insects that make them well suited to studying host shifts. Using Illumina multitarget amplicon sequencing of Wolbachia‐infected scale insects and their direct associates we determined the identity of all Wolbachia strains. We then fitted a generalized additive mixed model to our data to estimate the influence of host phylogeny and the geographical distribution on Wolbachia strain sharing among scale insect species. The model predicts no significant contribution of host geography but strong effects of host phylogeny, with high rates of Wolbachia sharing among closely related species and a sudden drop‐off in sharing with increasing phylogenetic distance. We also detected the same Wolbachia strain in scale insects and several intimately associated species (ants, wasps and flies). This indicates putative host shifts and potential routes of transfers via these associates and highlights the importance of ecological connectivity in Wolbachia host‐shifting.

Varying phylogenetic signal in susceptibility to four bacterial pathogens across species of Drosophilidae

“…Artificial transfers of Wolbachia are most successful between closely related hosts [22,23]. This tallies with field data on Wolbachia distributions that found strong effects of the host phylogeny, with high rates of Wolbachia sharing between closely related species, and a decline in co-occurrence in different hosts with increasing phylogenetic distance between these hosts [8]. Viruses show similar trends, with phylogenetic distance and clade effects explaining large amounts of variation in susceptibility to several viruses [24,25].…”

“…Despite a major focus on viral pathogens, there is an increasing awareness that bacterial pathogens also commonly undergo host shifts [6][7][8], which has been linked to their recent emergence as causative agents of disease in several host systems, including humans, livestock, wildlife, and plants [6][7][8].…”

Cryptic community structure and metabolic interactions among the heritable facultative symbionts of the pea aphid

“…Though we envision growth of symbiont study through multiplexed, multi‐locus, next‐generation sequencing of protein‐coding genes (e.g. Sanaei et al, 2023), the PCR screening and Sanger sequencing approach used here provided flexible scaling, genotyping strategy adjustments, and detailed insights into symbiont community structure not possible through other approaches.…”

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

“…As part of a separate study, the amplicons generated by this study, including 16S, gatB, coxA and fbpA from 75 Wolbachia positive samples, were sent for Illumina pooled amplicon sequencing with 10–30 K coverage (Sanaei et al ., 2021a). The output of this high‐throughput sequencing approach yielded Wolbachia strains belonging to supergroups A, B and F for all samples (Sanaei et al ., 2021a), which is an indication of the specificity of our screening methodology. Therefore, by using our suggested screening methodology, the probability of false‐positive samples seems to be very low.…”

“…As a positive control, we used extracted DNA of Drosophila melanogaster with a confirmed Wolbachia infection by w Mel strain (Monsanto‐Hearne and Johnson, 2018) for all PCRs. As part of a separate study, the amplicons generated by this study, including 16S, gatB, coxA and fbpA from 75 Wolbachia positive samples, were sent for Illumina pooled amplicon sequencing with 10–30 K coverage (Sanaei et al ., 2021a). The output of this high‐throughput sequencing approach yielded Wolbachia strains belonging to supergroups A, B and F for all samples (Sanaei et al ., 2021a), which is an indication of the specificity of our screening methodology.…”