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 <i>Wolbachia</i> 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 <i>Rickettsiella viridis</i> to the major crop pest <i>Myzus persicae</i>. <i>Rickettsiella</i> infection greatly reduced aphid fecundity, decreased heat tolerance, and modified aphid body color, from light to dark green. Despite inducing host fitness costs, <i>Rickettsiella</i> spread rapidly through caged aphid populations via plant-mediated horizontal transmission. The phenotypic effects of <i>Rickettsiella</i> 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 <i>Rickettsiella</i> maintaining a high density. <i>Rickettsiella</i> shows the potential to spread through natural <i>M. persicae</i> populations by horizontal transmission and subsequent vertical transmission. Establishment of <i>Rickettsiella</i> 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.