A rapidly spreading deleterious aphid endosymbiont that uses horizontal as well as vertical transmission

Abstract

Endosymbiotic bacteria that live inside the cells of insects are typically only transmitted maternally and can spread by increasing host fitness and/or modifying reproduction in sexual hosts. Transinfections of Wolbachia endosymbionts are now being used to introduce useful phenotypes into sexual host populations, but there has been limited progress on applications using other endosymbionts and in asexual populations. Here, we develop a unique pathway to application in aphids by transferring the endosymbiont Rickettsiella viridis to the major crop pest Myzus persicae . Rickettsiella infection greatly reduced aphid fecundity, decreased heat tolerance, and modified aphid body color, from light to dark green. Despite inducing host fitness costs, Rickettsiella spread rapidly through caged aphid populations via plant-mediated horizontal transmission. The phenotypic effects of Rickettsiella were sensitive to temperature, with spread only occurring at 19 °C and not 25 °C. Body color modification was also lost at high temperatures despite Rickettsiella maintaining a high density. Rickettsiella shows the potential to spread through natural M. persicae populations by horizontal transmission and subsequent vertical transmission. Establishment of Rickettsiella in natural populations could reduce crop damage by modifying population age structure, reducing population growth and providing context-dependent effects on host fitness. Our results highlight the importance of plant-mediated horizontal transmission and interactions with temperature as drivers of endosymbiont spread in asexual insect populations.

Warm temperature inhibits cytoplasmic incompatibility induced by endosymbiotic Rickettsiella in a spider host

“…Warmer rearing temperatures strongly decreased CI induction by Rickettsiella in male M. fradeorum spiders, but only mildly decreased CI rescue in female spiders. Thermal sensitivity for Rickettsiella-induced phenotypes is consistent with results for a different strain of Rickettsiella in an aphid host, which exhibits a different set of host phenotypic effects that don't include CI (Gu et al 2023). In the present study, CI strength overall was notably weaker than in prior studies by our group (Rosenwald et al 2020), which were conducted at room temperature, but in a laboratory that was cool throughout the duration of the experiments (J.…”

“…There is growing evidence that symbiont-induced host phenotypes, such as CI, can be thermally sensitive but potentially idiosyncratic (Corbin et al 2017, Doremus et al 2019, Shropshire et al 2020, Chrostek et al 2021, Corbin et al 2021, Hague et al 2022, Jones et al 2023, Martins et al 2023). The effect of temperature on Rickettsiella -induced CI has not previously been investigated, but in a non-CI-inducing Rickettsiella strain in aphids, temperature affects Rickettsiella titer, host phenotype, and spread in the host population (Gu et al PNAS 2023).…”

A diversity of endosymbionts across Australian aphids and their persistence in aphid cultures

“…Such an approach has recently been used in other pests and disease vectors, such as the transfer of disease blocking Wolbachia into planthoppers, Nilaparvata lugens (Gong et al, 2020) and the widespread use of transinfected Wolbachia in mosquitoes, Aedes aegypti and Aedes albopictus, to suppress arbovirus transmission (Caragata et al, 2021). In these cases the spread of the endosymbionts is assisted by their ability to generate cytoplasmic incompatibility (Hoffmann et al, 2011) which requires sexual reproduction, although in aphids there are other plant-based pathways through which endosymbionts can spread (Gu et al, 2023).…”

A new guest to the blood feast: a novel symbiotic lineage associated with a haematophagous leech from the genusHaementeria

“…Obligate symbiosis is a widespread phenomenon across a variety of animals, particularly within those with a nutrient-limited diet (e.g. plant sap or blood; Bennett and Moran 2013;Gu et al 2023;Husnik and McCutcheon 2016;Manzano-Marín et al 2023a;Matsuura et al 2018). Once these obligate associates establish a stable vertical transmission, their genomes undergo radical changes, which include loss of dispensable genes/pathways, an invasion by and subsequent loss of mobile elements, and a shift in nucleotide composition (i.e.…”

“…Obligate symbiosis is a widespread phenomenon across a variety of animals, particularly within those with a nutrient-limited diet (e.g. plant sap or blood; Bennett and Moran 2013; Gu et al . 2023; Husnik and McCutcheon 2016; Manzano-Marín et al .…”