Influences of two coexisting endosymbionts, CI-inducing Wolbachia and male-killing Spiroplasma, on the performance of their host Laodelphax striatellus (Hemiptera: Delphacidae).

Kazuki Yoshida,Shou‐Horng Huang,Makoto Tokuda,Sachiyo Sanada‐Morimura

doi:10.1002/ece3.5392

Abstract

The small brown planthopper Laodelphax striatellus (Hemiptera: Delphacidae) is reported to have the endosymbiont Wolbachia, which shows a strong cytoplasmic incompatibility (CI) between infected males and uninfected females. In the 2000s, female‐biased L. striatellus populations were found in Taiwan, and this sex ratio distortion was the result of male‐killing induced by the infection of another endosymbiont, Spiroplasma. Spiroplasma infection is considered to negatively affect both L. striatellus and Wolbachia because the male‐killing halves the offspring of L. striatellus and hinders the spread of Wolbachia infection via CI. Spiroplasma could have traits that increase the fitness of infected L. striatellus and/or coexisting organisms because the coinfection rates of Wolbachia and Spiroplasma were rather high in some areas. In this study, we investigated the influences of the infection of these two endosymbionts on the development, reproduction, and insecticide resistance of L. striatellus in the laboratory. Our results show that the single‐infection state of Spiroplasma had a negative influence on the fertility of L. striatellus, while the double‐infection state had no significant influence. At late nymphal and adult stages, the abundance of Spiroplasma was lower in the double‐infection state than in the single‐infection state. In the double‐infection state, the reduction of Spiroplasma density may be caused by competition between the two endosymbionts, and the negative influence of Spiroplasma on the fertility of host may be relieved. The resistance of L. striatellus to four insecticides was compared among different infection states of endosymbionts, but Spiroplasma infection did not contribute to increase insecticide resistance. Because positive influences of Spiroplasma infection were not found in terms of the development, reproduction, and insecticide resistance of L. striatellus, other factors improving the fitness of Spiroplasma‐infected L. striatellus may be related to the high frequency of double infection in some L. striatellus populations.

Highlights

Heritable bacterial endosymbionts are commonly found in diverse arthropods including insects (Bourtzis & Miller, 2006; Riegler & O'Neill, 2007)
Male‐killings are caused by various bacterial symbionts (Hurst, Jiggins, & Majerus, 2003), for example, Wolbachia in butterflies (Dyson, Kamath, & Hurst, 2002; Hurst, Jiggins, et al, 1999; Jiggins, Hurst, Schulenburg, & Majerus, 2001; Mitsuhashi, Fukuda, Nicho, & Murakami, 2004) and coleopterans (Fialho & Stevens, 2000; Hurst, Jiggins, et al, 1999), Rickettsia in coleopter‐ ans (Hurst, Majerus, & Walker, 1993; Lawson, Mousseau, Klaper, Hunter, & Werren, 2001; Werren et al, 1994), and Arsenophonus in a parasitoid wasp (Gherna et al, 1991; Werren, Skinner, & Huger, 1986)
To reveal the interactions among L. striatellus, Wolbachia, and Spiroplasma, we investigated the influences of two symbionts on the developmental and reproductive performance of L. striatellus

Summary

| INTRODUCTION

Heritable bacterial endosymbionts are commonly found in diverse arthropods including insects (Bourtzis & Miller, 2006; Riegler & O'Neill, 2007). The manipulation strategies increase the number of infected females in the population because the bacteria are fundamentally maintained by vertical transmission through egg cytoplasm (Ferree et al, 2005; Moran & Wernegreen, 2000) Such reproductive manipulations have evolved in phyloge‐ netically diverse groups of bacteria, including Wolbachia, Rickettsia, Arsenophonus, Spiroplasma, and Cardinium (Moran, McCutcheon, & Nakabachi, 2008). Because the female‐biased populations in Taiwan were in‐ fected with Wolbachia, this is a rare example of two endosymbionts possessing different manipulation strategies coexisting in the same insect population. In this system, male‐killing caused by Spiroplasma may virtually invalidate the CI strategy of Wolbachia. To reveal the interactions among L. striatellus, Wolbachia, and Spiroplasma, we investigated the influences of two symbionts on the developmental and reproductive performance of L. striatellus

| MATERIALS AND METHODS

| DISCUSSION

Findings

CONFLICT OF INTEREST