A chimeric gene paternally instructs female sex determination in the haplodiploid wasp
            <i>Nasonia</i>

Zou, Yuan; Geuverink, Elzemiek; Beukeboom, Leo W.; Verhulst, Eveline C.; Zande, Louis van de

doi:10.1126/science.abb8949

Cited by 47 publications

(49 citation statements)

References 52 publications

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“…Nasonia vitripennis is a gregarious parasitoid of several pest fly species [22]. The sex determination mechanism in N. vitripennis has been completely elucidated [23][24][25][26], and recently, we illustrated the role of Dsx in regulating sexually dimorphic traits [27]. In parallel, the chemical communication system of N. vitripennis has been intensively studied [28].…”

Section: Introductionmentioning

confidence: 99%

Silencing Doublesex expression triggers three-level pheromonal feminization in Nasonia vitripennis males

et al. 2022

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Doublesex (Dsx) has a conserved function in controlling sexual morphological differences in insects, but our knowledge of its role in regulating sexual behaviour is primarily limited to Drosophila . Here, we show with the parasitoid wasp Nasonia vitripennis that males whose Dsx gene had been silenced ( NvDsx -i) underwent a three-level pheromonal feminization: (i) NvDsx -i males were no longer able to attract females from a distance, owing to drastically reduced titres of the long-range sex pheromone; (ii) NvDsx -i males were courted by wild-type males as though they were females, which correlated with a lower abundance of alkenes in their cuticular hydrocarbon (CHC) profiles. Supplementation with realistic amounts of synthetic ( Z )-9-hentriacontene ( Z 9C31), the most significantly reduced alkene in NvDsx -i males, to NvDsx -i males interrupted courtship by wild-type conspecific males. Supplementation of female CHC profiles with Z 9C31 reduced courtship and mating attempts by wild-type males. These results prove that Z 9C31 is crucial for sex discrimination in N. vitripennis ; and (iii) Nvdsx -i males were hampered in eliciting female receptivity and thus experienced severely reduced mating success, suggesting that they are unable to produce the to-date unidentified oral aphrodisiac pheromone reported in N. vitripennis males. We conclude that Dsx is a multi-level key regulator of pheromone-mediated sexual communication in N. vitripennis .

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Section: Introductionmentioning

confidence: 99%

Silencing Doublesex expression triggers three-level pheromonal feminization in Nasonia vitripennis males

et al. 2022

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“…Aside from forward genetic approaches described above, Nasonia is amenable to reverse genetic approaches, such as RNA interference ( Lynch and Desplan 2006 ; Werren et al 2009 ). The utility of the Nasonia genus model system to identify the genetic basis of a wide variety of biological traits of evolutionary importance has been amply demonstrated in recent years ( Gadau et al 2002 ; Verhulst et al 2010 ; Loehlin and Werren 2012 ; Brucker and Bordenstein 2013 ; Niehuis et al 2013 ; Hoedjes et al 2014 ; Martinson et al 2017 ; Funkhouser-Jones et al 2018 ; Pannebakker et al 2020 ; Zou et al 2020 ).…”

Section: Introductionmentioning

confidence: 99%

Genetic, morphometric, and molecular analyses of interspecies differences in head shape and hybrid developmental defects in the wasp genus Nasonia

Cohen

Jewell

Moody

et al. 2021

G3 Genes|Genomes|Genetics

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Males in the parasitoid wasp genus Nasonia have distinct, species-specific, head shapes. The availability of fertile hybrids among the species, along with obligate haploidy of males, facilitates analysis of complex gene interactions in development and evolution. Previous analyses showed that both the divergence in head shape between N. vitripennis and N. giraulti, and the head-specific developmental defects of F2 haploid hybrid males, are governed by multiple changes in networks of interacting genes. Here we extend our understanding of the gene interactions that affect morphogenesis in male heads. Use of artificial diploid male hybrids shows that alleles mediating developmental defects are recessive, while there are diverse dominance relationships among other head shape traits. At the molecular level, the sex determination locus doublesex plays a major role in male head shape differences, but it is not the only important factor. Introgression of a giraulti region on chromsome 2 reveals a recessive locus that causes completely penetrant head clefting in both males and females in a vitripennis background. Finally, a third species (N. longicornis) was used to investigate the timing of genetic changes related to head morphology, revealing that most changes causing defects arose after the divergence of N. vitripennis from the other species, but prior to the divergence of N. giraulti and N. longicornis from each other. Our results demonstrate that developmental gene networks can be dissected using interspecies crosses in Nasonia, and set the stage for future fine-scale genetic dissection of both head shape and hybrid developmental defects.

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“…The upstream sex determination cascade seems to undergo rapid evolutionary change, as these genes are often replaced, duplicated, and reshuffled, as has been shown in multiple species. For example, in Hymenoptera, the feminizing gene wasp overruler of masculinization ( wom ) in the jewel wasp, Nasonia vitripennis , is a novel gene originating from a p53 gene duplication, but has also been very recently duplicated, with both copies of the gene thought to be functional [ 8 ]. The gene initiating sexual differentiation in the honeybee Apis mellifera , complementary sex determiner ( csd ), originated via a duplication of the feminizer ( fem ) gene, an ortholog of tra [ 9 , 10 ].…”

Section: Introductionmentioning

confidence: 99%

A conserved role of the duplicated Masculinizer gene in sex determination of the Mediterranean flour moth, Ephestia kuehniella

et al. 2021

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Sex determination in the silkworm, Bombyx mori, is based on Feminizer (Fem), a W-linked Fem piRNA that triggers female development in WZ individuals, and the Z-linked Masculinizer (Masc), which initiates male development and dosage compensation in ZZ individuals. While Fem piRNA is missing in a close relative of B. mori, Masc determines sex in several representatives of distant lepidopteran lineages. We studied the molecular mechanisms of sex determination in the Mediterranean flour moth, Ephestia kuehniella (Pyralidae). We identified an E. kuehniella Masc ortholog, EkMasc, and its paralog resulting from a recent duplication, EkMascB. Both genes are located on the Z chromosome and encode a similar Masc protein that contains two conserved domains but has lost the conserved double zinc finger domain. We developed PCR-based genetic sexing and demonstrated a peak in the expression of EkMasc and EkMascB genes only in early male embryos. Simultaneous knock-down experiments of both EkMasc and EkMascB using RNAi during early embryogenesis led to a shift from male- to female-specific splicing of the E. kuehniella doublesex gene (Ekdsx), their downstream effector, in ZZ embryos and resulted in a strong female-biased sex-ratio. Our results thus confirmed the conserved role of EkMasc and/or EkMascB in masculinization. We suggest that the C-terminal proline-rich domain, we have identified in all functionally confirmed Masc proteins, in conjunction with the masculinizing domain, is important for transcriptional regulation of sex determination in Lepidoptera. The function of the Masc double zinc finger domain is still unknown, but appears to have been lost in E. kuehniella.

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A chimeric gene paternally instructs female sex determination in the haplodiploid wasp Nasonia

Cited by 47 publications

References 52 publications

Silencing Doublesex expression triggers three-level pheromonal feminization in Nasonia vitripennis males

Silencing Doublesex expression triggers three-level pheromonal feminization in Nasonia vitripennis males

Genetic, morphometric, and molecular analyses of interspecies differences in head shape and hybrid developmental defects in the wasp genus Nasonia

A conserved role of the duplicated Masculinizer gene in sex determination of the Mediterranean flour moth, Ephestia kuehniella

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