Sex differentiation in crustaceans

In A. vulgare, genetically male embryos (with ZZ sexual chromosomes) that harbor maternally inherited Wolbachia bacteria develop into functional females, which are morphologically and anatomically indistinguishable from genetic females (with ZW sexual chromosomes) This is achieved by preventing androgenic gland differentiation In crustaceans, the androgenic gland synthesizes the androgenic hormone (AH) that is responsible for differentiation of male gonads and secondary characters For example, androgenic gland transplantation into young A. vulgare females results in complete development of male gonads instead of ovaries, leading to complete sex reversal (Katakura, 1960; Juchault and Legrand, 1972). Similar results are obtained by injections of AH extracts, confirming that male differentiation is controlled by this hormone (Martin et al , 1999) AH has been purified and characterized: it is constituted of two chains linked by disulfide bridges (Martin et al ., 1990; 1999; Okuno et al ., 1997) . AH gene expression is highly tissue-specific restricted to androgenic glands (Okuno et al ., 1999; Ohira et al ., 2003; Grève et al ., 2004) . In genetic A. vulgare males, AH mRNA can be detected by PCR as early as at the beginning of male gonad differentiation (unpublished results) AH thus would have an early and local action by inducing male differentiation of embryonic gonads Therefore, feminization of genetic males that have inherited Wolbachia could result from inhibition of androgenic gland differentiation by targeting either the AH gene promoter or AH receptor (Juchault and Legrand, 1985) .

This labile system of sex determination and differentiation suggests that genes necessary for male and female differentiation are carried by chromosomes of both sexes, in which the W and Z chromosomes, poorly morphologically differentiated, only differ by a W-linked factor that inhibits the master gene responsible for male differentiation (Legrand et al ., 1987; Juchault and Mocquard, 1993; Rigaud et al ., 1997) . This factor, as well as Wolba-chia, may target the AH gene or its receptor, or another gene of the sex determination cascade, ultimately leading to inhibition of androgenic gland differentiation This hypothesis suggests a late action of Wolbachia on host target during development, as opposed to very early action of other Wolbachia strains that induce parthenogenesis, cytoplasmic incompatibility or male killing in insects (Bourtzis and Miller, 2003) .

In some cases, Wolbachia action may be incomplete or inefficient. For example, intersex phenotypes, ranging from fertile intersex females (iF) to sterile intersex males (iM), occur in naturally infected populations (Rigaud and Juchault, 1998) This has been interpreted as insufficient bacterial density to inhibit androgenic gland differentiation, but sufficient to target AH receptor in adults, leading to expression of partial feminization. Similar intersexes have been reported in two butterflies hosting Wolbachia (Kageyama and Traut, 2004; Sakamoto et al , 2007) In these species, Wolbachia induce early male killing, but partial feminization can be obtained with lowered bacterial burden after antibiotic treatments Another illustration of incomplete or inefficient feminization in isopods is that naturally symbiotic males are observed in several species, such as P. pruinosus and Oniscus asellus, in which Wolbachia typically induce a feminizing phenotype (Marcade et al ., 1999; Rigaud et al , 1999b) Hence, low Wolbachia density during embryo development results in imperfect feminization or the persistence of bacteria in males, depending on the feminizing power of the strain (Bandi et al , 2001)

Wolbachia-induced feminization has also been demonstrated in two insect species, (Hiroki et al ., 2002; Narita et al ., 2007; Negri et al ., 2006) . However, host genes targeted by feminizing Wolbachia are different in crustaceans and insects In insects, an interaction between bacteria and the master regulator genes that control somatic sex determination in D. melanogaster (Sex-lethal or Doublesex genes) has been hypothesized (Negri et al ., 2006; Narita et al , 2007) Because circulating sexual hormones are lacking in insects, Wolbachia have to infect all host cells and interact with the genetic control of sex determination in each somatic cell Interestingly, such local action has been reported in woodlice infected by a masculinizing virus involved in gynandromorphous mosaics (Juchault et al , 1991)

Feminization should not be considered unique to Wolbachia Other symbionts, such as Cardinium in the mite Brevipalpus phoenicis (Weeks et al ., 2001) and microsporidia and para-mixydia in amphipods (Weedall et al ., 2006; Haine et al ., 2007), are able to induce genetic male individuals to develop as females The mechanism of feminization in the mite (in which haploid symbiotic males reproduce as parthenogenetic females) is not yet known Conversely, microsporidia-induced feminization in amphipods such as Gammarus duebeni or Orchestia spp has been studied more extensively (Terry et al , 1999, 2004) For example, Nosema granulosis induces feminization in G. duebeni by preventing differentiation of the androgenic gland and the production of AH, which also controls male sexual differentiation in this species (Rodgers-Gray et al ., 2004; Haine et al ., 2007) . Hence, similar pathways of sex determination may be targeted by both microsporidia and Wolbachia, in both amphi-pods and isopods

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