Transgenic expression of Nix converts genetic females into males and allows automated sex sorting in Aedes albopictus

Lutrat, Célia; Olmo, Roenick Proveti; Baldet, Thierry; Bouyer, Jérémy; Marois, Eric

doi:10.1038/s42003-022-03165-7

Cited by 20 publications

(28 citation statements)

References 43 publications

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“…The intersex do not produce offspring and pseudo-males, as good as the ones of line AalNix3&4-♂4 do produce some offspring including new pseudo-males, while wild-type males inheriting the gene-drive transgene have the same mating ability as wild-type males, and can mate with wild-type females to transmit the gene drive system resulting in population suppression. Our work confirms and extends a recent contribution by Lutrat et al [21].…”

Section: Introductionsupporting

confidence: 94%

The AalNix3&4 isoform is required and sufficient to convert Aedes albopictus females into males

et al. 2022

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Aedes albopictus is one of the most invasive insect species in the world and an effective vector for many important arboviruses. We reported previously that Ae. albopictus Nix (AalNix) is the male-determining factor of this species. However, whether AalNix alone is sufficient to initiate male development is unknown. Transgenic lines that express each of the three AalNix isoforms from the native promoter were obtained using piggyBac transformation. We verified the stable expression of AalNix isoforms in the transgenic lines and confirm that one isoform, AalNix3&4, is sufficient to convert females into fertile males (pseudo-males) that are indistinguishable from wild-type males. We also established a stable sex-converted female mosquito strain, AalNix3&4-♂4-pseudo-male. The pseudo-male mosquitoes can fly and mate normally with wild-type female, although their mating competitiveness is lower than wild-type. This work further clarifies the role of AalNix in the sex determination pathway and will facilitate the development of Ae. albopictus control strategies that rely on male-only releases such as SIT and sex-ratio distortion.

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Section: Introductionsupporting

confidence: 94%

The AalNix3&4 isoform is required and sufficient to convert Aedes albopictus females into males

et al. 2022

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“…Unlike Lepidoptera, Ae. aegypti mosquitoes have a heterogametic sex determining region [38], which results in maleness being expressed in the heterozygous form [39]. However, feminization converts genetic males into functional females, while the infertility effect converts functional females into non-functional females without male characteristics, suggesting different Wolbachia -related mechanisms [40, 41].…”

Section: Discussionmentioning

confidence: 99%

Wolbachiainhibits ovarian formation and increases blood feeding rate in femaleAedes aegypti

Lau

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Endersby‐Harshman

et al. 2022

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Wolbachia, a gram-negative endosymbiotic bacterium widespread in arthropods, is well-known for changing the reproduction of its host in ways that increase its rate of spread, but there are also costs to hosts that can reduce this. Here we investigated a novel reproductive alteration of Wolbachia wAlbB on its host Aedes aegypti, based on studies of mosquito life history traits, ovarian dissections and gene expression assays. We found that an extended period of the larval stage as well as the egg stage as previously shown can increase the proportion of Wolbachia-infected females that become infertile; the impact of Wolbachia on infertility therefore accumulated before pupation. We found that ovarian formation was blocked in infertile females, even though infected females had relatively lower Wolbachia densities than fertile infected females. Infertile females also showed a higher frequency of blood feeding following a prior blood meal, indicating that they do not enter a complete gonotrophic cycle. Treatments leading to infertility decreased expression of genes related to reproduction. Our results demonstrate effects related to the causes and consequences of infertile wAlbB-infected Ae. aegypti females with implications for Wolbachia releases and have evolutionary implications for Wolbachia infections in novel hosts.

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“…In contrast, complete female-to-male conversion was achieved using the endogenous promoter to express Nix in Ae.aegypti and Ae. albopictus [10,35], indicating that using a promoter region other than the endogenous one can be potentially detrimental for effective male sex determination.…”

Section: Discussionmentioning

confidence: 99%

Partial masculinization of Aedes aegypti females by conditional expression of Nix

et al. 2022

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Background Aedes aegypti, the main vector of dengue, yellow fever, and other arboviruses thrives in tropical and subtropical areas around the globe putting half of the world’s population at risk. Despite aggressive efforts to control the transmission of those viruses, an unacceptable number of cases occur every year, emphasizing the need to develop new control strategies. Proposals for vector control focused on population suppression could offer a feasible alternative method to reduce disease transmission. The induction of extreme male-biased sex ratios has been hypothesized to be able to suppress or collapse a population, with previous experiments showing that stable expression of the male determining factor Nix in A. aegypti is sufficient to convert females into fertile males. Methodology/Principal findings Here, we report on the conditional expression of Nix in transgenic A. aegypti under the control of the tetracycline-dependent (Tet-off) system, with the goal of establishing repressible sex distortion. A masculinization phenotype was observed in three of the seven transgenic lines with females exhibiting male-like long maxillary palps and most importantly, the masculinized females were unable to blood feed. Doxycycline treatment of the transgenic lines only partially restored the normal phenotype from the masculinized transgenic lines, while RT-qPCR analysis of early embryos or adults showed no correlation between the level of masculinization and ectopic Nix expression. Conclusions/Significance While the conditional expression of Nix produced intersex phenotypes, the level of expression was insufficient to program full conversion. Modifications that increase both the level of activation (no tet) and the level of repression (with tet) will be necessary, as such this study represents one step forward in the development of genetic strategies to control vector-borne diseases via sex ratio distortion.

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Transgenic expression of Nix converts genetic females into males and allows automated sex sorting in Aedes albopictus

Cited by 20 publications

References 43 publications

The AalNix3&4 isoform is required and sufficient to convert Aedes albopictus females into males

The AalNix3&4 isoform is required and sufficient to convert Aedes albopictus females into males

Wolbachiainhibits ovarian formation and increases blood feeding rate in femaleAedes aegypti

Partial masculinization of Aedes aegypti females by conditional expression of Nix

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