Females infected with symbiotic bacteria have proliferation advantage over uninfected: Clarification of a pest control strategy of "predatory insects"

A research group led by Researcher Yuta Owashi, and Deputy Leader Daisuke Kageyama of the Institute of Agrobiological Sciences at the National Agriculture and Food Research Organization (NARO), and Associate Professor Tetsuya Adachi of the Department of Agricultural and Environmental Sciences, Faculty of Agriculture at the University of Miyazaki, has reported that the Rickettsia symbionts, which widely infect Nesidiocoris tenuis, a natural predator for agricultural insect pests such as whiteflies and thrips, manipulate N. tenuis reproduction to increase offspring of infected females. The finding indicates that the status of infection by symbiotic bacteria such as Rickettsia is important for the efficient propagation of N. tenuis. The biological pest control technology using predatory insects is expected to be more effective by optimizing the N. tenuis propagation efficiency through the use of symbiotic bacteria.

Many insects are infected by symbiotic bacteria. Symbiotic bacteria are transmitted from mother to child but usually not from an infected individual to another. Some symbiotic bacteria have also been found to provide nutrients to insects or manipulate insect reproduction in several ways, such as sterilization and sex-ratio distortion. However, their actual functions are rarely known, and the functions of many symbiotic bacteria remain unknown. Clarifying their function is expected to facilitate functional enhancement and application of predatory insects as pest control agents.

N. tenuis, which preys on whiteflies, thrips, and other insect pests, are becoming increasingly popular as a biopesticide or indigenous predator in various geographical regions. Symbionts found in N. tenuis include bacteria of the genera Rickettsia and Wolbachia. N. tenuis individuals collected in various parts of Japan carried Rickettsia symbionts at rates ranging from 21% to 96% depending on the region, and the function of Rickettsia remained unknown.

The research group crossed N. tenuis females and males of a Rickettsia-infected line and an uninfected line, in which Rickettsia symbionts were eradicated with an antibiotic, in a total of four combination patterns and compared the combination patterns in terms of the number of laid eggs and egg hatch rate. The number of laid eggs was similar around 20 eggs per 6 days for all combinations. However, the egg hatch rate was 0% only for the combination of infected males and uninfected females, whereas approximately 60%−80% of eggs hatched in the other combinations. The phenomenon in which uninfected females mating only with symbiont-infected males produce eggs that do not hatch is called cytoplasmic incompatibility.

Several different symbiotic bacteria, such as Wolbachia and Cardinium, have been known to cause cytoplasmic incompatibility. Although the Rickettsia symbionts have been found in a variety of insects, including whiteflies and aphids, this is the first study to show that Rickettsia infection cause cytoplasmic incompatibility. While Rickettsia symbionts are classified into several groups based on phylogenetic analysis, the Rickettsia strain found in N. tenuis was closely related to the Bellii clade, which contains many Rickettsia isolates found only in insects such as stink bugs and aphids. The Bellii clade is distinct from the Spotted fever and Typhus clades, which contain pathogenic Rickettsia transmitted by mites and lice. The key to the sustained effectiveness of predatory insects as biopesticides is to maintain sufficient populations after female and male predators are released in the field or greenhouse.

The results of this study showed that the predatory insect N. tenuis symbiotically infected by Rickettsia is advantageous for efficient propagation in laboratory experiments. Moving forward, studies to demonstrate the efficient propagation of and effective pest control by Rickettsia-infected N. tenuis in agricultural settings such as fields and greenhouses are expected to lead to the implementation of the biological pest control technology using predatory insects with improved performance. By clarifying the frequency of cytoplasmic incompatibility in wild N. tenuis populations and other practical aspects in the field environment, the technology is expected to find application under various conditions suitable to specific geographical regions.

Rickettsia symbionts have been widely found in stink bugs, whiteflies, aphids, and other agricultural pests. Moving forward, studies to clarify the responsible genes and the details of molecular mechanisms for Rickettsia-induced cytoplasmic incompatibility are expected to lead to the development of the pest control technology targeting population control of various insect pests.

Journal Information
Publication: Proceedings of the Royal Society B
Title: Rickettsia induces strong cytoplasmic incompatibility in a predatory insect
DOI: 10.1098/rspb.2024.0680