scholarly journals Maleness-on-the-Y (MoY) orchestrates male sex determination in major agricultural fruit fly pests

2019 ◽  
Author(s):  
Angela Meccariello ◽  
Marco Salvemini ◽  
Pasquale Primo ◽  
Brantley Hall ◽  
Panagiota Koskinioti ◽  
...  

AbstractIn insects, rapidly evolving primary sex-determining signals are transduced by a conserved regulatory module producing sex-specific proteins that direct sex determination and sexual differentiation1-4. In the agricultural pest Ceratitis capitata (medfly), a Y-linked maleness factor (M) is thought to repress the autoregulatory splicing of transformer (Cctra), which is required in XX individuals to establish and maintain female sex determination5,6. Despite previous attempts of isolating Y-linked genes using the medfly whole genome, the M factor has remained elusive7. Here, we report the identification of a Y-linked gene, Maleness-on the-Y (MoY), and show that it encodes a small novel protein which is both necessary and sufficient for medfly male sex determination. Transient silencing of MoY in XY individuals leads to the development of fertile females while transient expression of MoY in XX individuals results in fertile males. Notably, a cross between these sex reverted individuals gives rise to both fertile males and females indicating that a functional MoY can be maternally transmitted. In contrast to the diversity of M factors found in dipteran species8-11, we discovered MoY orthologues in seven other Tephritid species spanning ∼111 millions of years of evolution (Mya). We confirmed their male determining function in the olive fly (Bactrocera oleae) and the oriental fruit fly (Bactrocera dorsalis). This unexpected conservation of the primary MoY signal in a large number of important agricultural pests12 will facilitate the development of transferable genetic control strategies in these species, for example sterile male releases or sex-ratio-distorting gene drives.

Science ◽  
2019 ◽  
Vol 365 (6460) ◽  
pp. 1457-1460 ◽  
Author(s):  
Angela Meccariello ◽  
Marco Salvemini ◽  
Pasquale Primo ◽  
Brantley Hall ◽  
Panagiota Koskinioti ◽  
...  

In insects, rapidly evolving primary sex-determining signals are transduced by a conserved regulatory module controlling sexual differentiation. In the agricultural pest Ceratitis capitata (Mediterranean fruit fly, or Medfly), we identified a Y-linked gene, Maleness-on-the-Y (MoY), encoding a small protein that is necessary and sufficient for male development. Silencing or disruption of MoY in XY embryos causes feminization, whereas overexpression of MoY in XX embryos induces masculinization. Crosses between transformed XY females and XX males give rise to males and females, indicating that a Y chromosome can be transmitted by XY females. MoY is Y-linked and functionally conserved in other species of the Tephritidae family, highlighting its potential to serve as a tool for developing more effective control strategies against these major agricultural insect pests.


2019 ◽  
Vol 19 (S1) ◽  
Author(s):  
Elias D. Asimakis ◽  
Vangelis Doudoumis ◽  
Ashok B. Hadapad ◽  
Ramesh S. Hire ◽  
Costas Batargias ◽  
...  

Abstract Background Various endosymbiotic bacteria, including Wolbachia of the Alphaproteobacteria, infect a wide range of insects and are capable of inducing reproductive abnormalities to their hosts such as cytoplasmic incompatibility (CI), parthenogenesis, feminization and male-killing. These extended phenotypes can be potentially exploited in enhancing environmentally friendly methods, such as the sterile insect technique (SIT), for controlling natural populations of agricultural pests. The goal of the present study is to investigate the presence of Wolbachia, Spiroplasma,Arsenophonus and Cardinium among Bactrocera,Dacus and Zeugodacus flies of Southeast Asian populations, and to genotype any detected Wolbachia strains. Results A specific 16S rRNA PCR assay was used to investigate the presence of reproductive parasites in natural populations of nine different tephritid species originating from three Asian countries, Bangladesh, China and India. Wolbachia infections were identified in Bactrocera dorsalis, B. correcta, B. scutellaris andB. zonata, with 12.2–42.9% occurrence, Entomoplasmatales in B. dorsalis, B. correcta, B. scutellaris, B. zonata,Zeugodacus cucurbitae and Z. tau (0.8–14.3%) and Cardinium in B. dorsalis andZ. tau (0.9–5.8%), while none of the species tested, harbored infections with Arsenophonus. Infected populations showed a medium (between 10 and 90%) or low (< 10%) prevalence, ranging from 3 to 80% for Wolbachia, 2 to 33% for Entomoplasmatales and 5 to 45% for Cardinium. Wolbachia and Entomoplasmatales infections were found both in tropical and subtropical populations, the former mostly in India and the latter in various regions of India and Bangladesh. Cardinium infections were identified in both countries but only in subtropical populations. Phylogenetic analysis revealed the presence ofWolbachia with some strains belonging either to supergroup B or supergroup A. Sequence analysis revealed deletions of variable length and nucleotide variation in three Wolbachia genes. Spiroplasma strains were characterized as citri–chrysopicola–mirum and ixodetis strains while the remaining Entomoplasmatales to the Mycoides–Entomoplasmataceae clade.Cardinium strains were characterized as group A, similar to strains infecting Encarsia pergandiella. Conclusions Our results indicated that in the Southeast natural populations examined, supergroup A Wolbachia strain infections were the most common, followed by Entomoplasmatales and Cardinium. In terms of diversity, most strains of each bacterial genus detected clustered in a common group. Interestingly, the deletions detected in three Wolbachia genes were either new or similar to those of previously identified pseudogenes that were integrated in the host genome indicating putative horizontal gene transfer events in B. dorsalis, B. correcta and B. zonata.


2018 ◽  
Author(s):  
Mariana Mateos ◽  
Humberto Martinez ◽  
Silvia B. Lanzavecchia ◽  
Claudia Conte ◽  
Karina Guillén ◽  
...  

AbstractMembers of the true fruit flies (family Tephritidae) are among the most serious agricultural pests worldwide, whose control and management demands large and costly international efforts. The need for cost-effective and environmentally-friendly integrated pest management (IPM) has led to the development and implementation of autocidal control strategies. Autocidal approaches include the widely used sterile insect technique (SIT) and the incompatible insect technique (IIT). IIT relies on maternally transmitted bacteria (namely Wolbachia), to cause a conditional sterility in crosses between released mass-reared Wolbachia-infected males and wild females, which are either uninfected or infected with a different Wolbachia strain (i.e., cytoplasmic incompatibility; CI). Herein, we review the current state of knowledge on Wolbachia-tephritid interactions including infection prevalence in wild populations, phenotypic consequences, and their impact on life history traits. Numerous pest tephritid species are reported to harbor Wolbachia infections, with a subset exhibiting high prevalence. The phenotypic effects of Wolbachia have been assessed in very few tephritid species, due in part to the difficulty of manipulating Wolbachia infection (removal or transinfection). Based on recent methodological advances (high-throughput DNA sequencing) and a breakthrough concerning the mechanistic basis of CI, we suggest research avenues that could accelerate generation of necessary knowledge for the potential use of Wolbachia-based IIT in area-wide integrated pest management (AW-IPM) strategies for the population control of tephritid pests.


BMC Genetics ◽  
2020 ◽  
Vol 21 (S2) ◽  
Author(s):  
Pasquale Primo ◽  
Angela Meccariello ◽  
Maria Grazia Inghilterra ◽  
Andrea Gravina ◽  
Giuseppe Del Corsano ◽  
...  

Abstract Background Females of the Mediterranean fruit fly Ceratitis capitata (Medfly) are major agricultural pests, as they lay eggs into the fruit crops of hundreds of plant species. In Medfly, female sex determination is based on the activation of Cctransformer (Cctra). A maternal contribution of Cctra is required to activate Cctra itself in the XX embryos and to start and epigenetically maintain a Cctra positive feedback loop, by female-specific alternative splicing, leading to female development. In XY embryos, the male determining Maleness-on-the-Y gene (MoY) blocks this activation and Cctra produces male-specific transcripts encoding truncated CcTRA isoforms and male differentiation occurs. Results With the aim of inducing frameshift mutations in the first coding exon to disrupt both female-specific and shorter male-specific CcTRA open reading frames (ORF), we injected Cas9 ribonucleoproteins (Cas9 and single guide RNA, sgRNA) in embryos. As this approach leads to mostly monoallelic mutations, masculinization was expected only in G1 XX individuals carrying biallelic mutations, following crosses of G0 injected individuals. Surprisingly, these injections into XX-only embryos led to G0 adults that included not only XX females but also 50% of reverted fertile XX males. The G0 XX males expressed male-specific Cctra transcripts, suggesting full masculinization. Interestingly, out of six G0 XX males, four displayed the Cctra wild type sequence. This finding suggests that masculinization by Cas9-sgRNA injections was independent from its mutagenic activity. In line with this observation, embryonic targeting of Cctra in XX embryos by a dead Cas9 (enzymatically inactive, dCas9) also favoured a male-specific splicing of Cctra, in both embryos and adults. Conclusions Our data suggest that the establishment of Cctra female-specific autoregulation during the early embryogenesis has been repressed in XX embryos by the transient binding of the Cas9-sgRNA on the first exon of the Cctra gene. This hypothesis is supported by the observation that the shift of Cctra splicing from female to male mode is induced also by dCas9. Collectively, the present findings corroborate the idea that a transient embryonic inactivation of Cctra is sufficient for male sex determination.


Genetica ◽  
2015 ◽  
Vol 143 (6) ◽  
pp. 717-727 ◽  
Author(s):  
Wei Peng ◽  
Wenping Zheng ◽  
Alfred M. Handler ◽  
Hongyu Zhang

2019 ◽  
Author(s):  
Valeria Petrella ◽  
Serena Aceto ◽  
Vincenza Colonna ◽  
Giuseppe Saccone ◽  
Remo Sanges ◽  
...  

AbstractBackgroundPhlebotomine sand flies (Diptera, Nematocera) are important vectors of several pathogens, including Leishmania parasites, causing serious diseases of humans and dogs. Despite their importance as disease vectors, most aspects of sand fly biology remain unknown including the molecular bases of their reproduction and sex determination, aspects also relevant for the development of novel vector control strategies.ResultsUsing a comparative genomics/transcriptomics approach, we identified the sex determining genes in phlebotomine sand flies and proposed the first model for the sex determination cascade of these insects. For all the genes identified, we produced manually curated gene models, developmental gene expression profile and performed evolutionary molecular analysis. We identified and characterized, for the first time in a Nematocera species, the transformer (tra) homolog which exhibits both conserved and novel features. The analysis of the tra locus in sand flies and its expression pattern suggest that this gene is able to autoregulate its own splicing, as observed in the fruit fly Ceratitis capitata and several other insect species.ConclusionsOur results permit to fill the gap about sex determination in sand flies, contribute to a better understanding of this developmental pathway in Nematocera and open the way for the identification of sex determining orthologs in other species of this important Diptera sub-order. Furthermore, the sex determination genes identified in our work also provide the opportunity of future biotech applications to control natural population of sand flies, reducing their impact on public health.


2020 ◽  
Vol 113 (5) ◽  
pp. 343-354 ◽  
Author(s):  
Issaka Zida ◽  
Souleymane Nacro ◽  
Rémy Dabiré ◽  
Irénée Somda

Abstract Fruit flies are significant insect pests, worldwide. Tephritid species diversity and their seasonal abundance were investigated over 2 yr (May 2017 to May 2019) in Western Burkina Faso. A mass trapping experiment consisting of 288 Tephri Trap types, operating with four types of parapheromones comprising methyl eugenol, terpinyl acetate, trimedlure, and cue lure and an insecticide (Dichlorvos), was used for attracting and killing insects. Plant formations including natural fallows, mango orchards, and agroforestry parks in each of the six study sites were selected for data collection. Twenty-nine tephritid species belonging to 10 genera were identified. Fourteen fruit fly species were identified for the first time in Burkina Faso. The genera Ceratitis MacLeay (Diptera : Tephritidae) and Dacus Fabricius (Diptera: Tephritidae) with, respectively, 14 and 7 species recorded were the most represented. The dominant species caught was the invasive Bactrocera dorsalis Hendel (Diptera: Tephritidae) followed by Ceratitis cosyra Walker (Diptera: Tephritidae) and Ceratitis silvestrii Bezzi (Diptera: Tephritidae). The fruit fly population density was very high during the rainy season, with peaks occurring in June or July. The fruit fly species were generally more abundant during the hot and rainy seasons than during the cold and dry seasons. The highest diversity was recorded in natural fallows, as compared with the mango orchards and agroforestry parks. Tephritid species found refuge in the mango orchards during the dry and cold periods. The results of that investigation may be used for developing a sustainable pest management strategy for commercial orchards.


2011 ◽  
Vol 102 (1) ◽  
pp. 103-111 ◽  
Author(s):  
M.K. Schutze ◽  
A. Jessup ◽  
A.R. Clarke

AbstractFour morphologically cryptic species of the Bactrocera dorsalis fruit fly complex (B. dorsalis s.s., B. papayae, B. carambolae and B. philippinensis) are serious agricultural pests. As they are difficult to diagnose using traditional taxonomic techniques, we examined the potential for geometric morphometric analysis of wing size and shape to discriminate between them. Fifteen wing landmarks generated size and shape data for 245 specimens for subsequent comparisons among three geographically distinct samples of each species. Intraspecific wing size was significantly different within samples of B. carambolae and B. dorsalis s.s. but not within samples of B. papayae or B. philippinensis. Although B. papayae had the smallest wings (average centroid size=6.002 mm±0.061 SE) and B. dorsalis s.s. the largest (6.349 mm±0.066 SE), interspecific wing size comparisons were generally non-informative and incapable of discriminating species. Contrary to the wing size data, canonical variate analysis based on wing shape data discriminated all species with a relatively high degree of accuracy; individuals were correctly reassigned to their respective species on average 93.27% of the time. A single sample group of B. carambolae from locality ‘TN Malaysia’ was the only sample to be considerably different from its conspecific groups with regards to both wing size and wing shape. This sample was subsequently deemed to have been originally misidentified and likely represents an undescribed species. We demonstrate that geometric morphometric techniques analysing wing shape represent a promising approach for discriminating between morphologically cryptic taxa of the B. dorsalis species complex.


2020 ◽  
Vol 10 (1) ◽  
Author(s):  
Jun-Feng Cheng ◽  
Ting Yu ◽  
Zhong-Jian Chen ◽  
Shicheng Chen ◽  
Yu-Peng Chen ◽  
...  

Abstract The citrus fruit fly Bactrocera (Tetradacus) minax is a major and devastating agricultural pest in Asian subtropical countries. Previous studies have shown that B. minax interacts with plant hosts via the efficient chemosensory system. However, the molecular components of the B. minax chemosensory system have not been well characterized. Herein, we identified a total of 25 putative odorant-binding receptors (OBPs), 4 single-copy chemosensory proteins (CSPs) and 53 candidate odorant receptors (ORs) using a newly generated whole-genome dataset for B. minax. This study significantly extended the chemosensation-related gene profiles (particularly, OBPs and ORs) in six other tephritid species. Comparative transcriptome analysis of adult B. minax and Bactrocera dorsalis showed that there were 14 highly expressed OBPs (FPKM > 100) in B. dorsalis and 7 highly expressed ones in B. minax. The expression level of CSP3 gene and CSP4 gene was higher in B. dorsalis than that in B. minax. Comparative genomic and transcriptomic analyses of chemosensory genes in the citrus fruit fly B. minax provided new insights for preventive control of this agriculture important pest and closely related species.


2020 ◽  
Vol 27 (1) ◽  
pp. 109-129
Author(s):  
Laura Moquet ◽  
Jim Payet ◽  
Serge Glenac ◽  
Hélène Delatte

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