Insect Sex Determination Manipulated by Their Endosymbionts: Incidences, Mechanisms and Implications

Abstract

The sex-determining systems of arthropods are surprisingly diverse. Some species have male or female heterogametic sex chromosomes while other species do not have sex chromosomes. Most species are diploids but some species, including wasps, ants, thrips and mites, are haplodiploids (n in males; 2n in females). Many of the sexual aberrations, such as sexual mosaics, sex-specific lethality and conversion of sexuality, can be explained by developmental defects including double fertilization of a binucleate egg, loss of a sex chromosome or perturbation of sex-determining gene expression, which occur accidentally or are induced by certain environmental conditions. However, recent studies have revealed that such sexual aberrations can be caused by various groups of vertically-transmitted endosymbiotic microbes such as bacteria of the genera Wolbachia, Rickettsia, Arsenophonus, Spiroplasma and Cardinium, as well as microsporidian protists. In this review, we first summarize the accumulated data on endosymbiont-induced sexual aberrations, and then discuss how such endosymbionts affect the developmental system of their hosts and what kinds of ecological and evolutionary effects these endosymbionts have on their host populations.

Keywords: Wolbachia; endosymbiont; feminization; insect; male killing; sex determination.

Figure 1

The sex determination cascade in Drosophila melanogaster. PeSxl indicates Sxl transcript from the early promoter. PmSxl indicates Sxl from the late promoter. The gray box shows the conserved part of the cascade. (Adapted from [7].)

Figure 2

Effects of the antibiotic on the sexual phenotype of the butterfly Eurema mandarina infected with two strains of Wolbachia [26]. (a) A normal female and an intersex generated by antibiotic treatment. The intersex has both male and female features in external morphology. (b) Ovarioles of normal females. (c) The reproductive organs of the intersex. Both male-specific organs (testes) and female-specific organs (ovarioles) occur in an individual treated with tetracycline hydrochloride during larval stages. (d) Schematic illustration showing the effect of antibiotic treatment of larvae on adult sexual phenotype. The longer the treatment, the more male-like phenotype appears. NT: non-treated. Tet: tetracycline-treated.

Figure 3

Effects of antibiotics on sexual phenotype of the moth Ostrinia scapulalis infected with Wolbachia [62]. (a) Intersexual individuals generated by tetracycline treatment. Black and white depict male-like color and female-like color, respectively. (b) The proportion of phenotypic females (white), intersexes (gray) and phenotypic males (black) among individuals whose mothers were treated with tetracycline hydrochloride prior to oviposition.

Figure 4

A parsimonious explanation of male killing (MK), feminization (FM) and parthenogenesis induction (PI). Here, MK, FM and PI are all assumed to be associated with the sex-determining process. The hypothetical flows of the male-determining and female-determining information are shown with blue and red arrows, respectively. Horizontal arrows indicate manipulation by endosymbionts. Note that this explanation is a hypothesis and may not necessarily reflect the actual mechanisms.