<i>Rickettsia</i> symbionts spread via mixed mode transmission, increasing female fecundity and sex ratio shift by host hormone modulating.

Abstract

Heritable symbionts are common among animals in nature, but the molecular mechanisms underpinning symbiont invasions of host populations have been elusive. In this study, we demonstrate the spread of <i>Rickettsia</i> in an invasive agricultural pest, the whitefly <i>Bemisia tabaci</i> Mediterranean (MED), across northeastern China from 2018 to 2023. Here, we show that the beneficial symbiont <i>Rickettsia</i> spreads by manipulating host hormone signals. Our analyses suggest that <i>Rickettsia</i> have been horizontally acquired by <i>B. tabaci</i> MED from another invasive whitefly <i>B. tabaci</i> Middle East-Asia Minor 1 during periods of coexistence. <i>Rickettsia</i> is transmitted maternally and horizontally from female <i>B. tabaci</i> MED individuals. <i>Rickettsia</i> infection enhances fecundity and results in female bias among whiteflies. Our findings reveal that <i>Rickettsia</i> infection stimulates juvenile hormone (JH) synthesis, in turn enhancing fecundity, copulation events, and the female ratio of the offspring. Consequently, <i>Rickettsia</i> infection results in increased whitefly fecundity and female bias by modulating the JH pathway. More female progeny facilitates the transmission of <i>Rickettsia</i>. This study illustrates that the spread of <i>Rickettsia</i> among invasive whiteflies in northeastern China is propelled by host hormone regulation. Such symbiont invasions lead to rapid physiological and molecular evolution in the host, influencing the biology and ecology of an invasive species.