Asymmetric Phenotypes of Sterile Hybrid Males From Reciprocal Crosses Between Species of the Anopheles gambiae Complex

Liang, Jiangtao; Hodge, James M.; Sharakhov, Igor V.

doi:10.3389/fevo.2021.660207

Cited by 4 publications

(2 citation statements)

References 47 publications

(79 reference statements)

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“…MAG proteins are an essential component of seminal fluid deposited into the An. gambiae female reproductive tract during copulation and they play important roles in inducing female post-mating responses, including oviposition and monogamy [ 80 , 81 , 82 , 83 ]. An over-representation of MAG-biased genes on the X chromosome [ 26 ] suggests that components of male reproductive biology in malaria mosquitoes can be antagonistic.…”

Section: Discussionmentioning

confidence: 99%

Retrogene Duplication and Expression Patterns Shaped by the Evolution of Sex Chromosomes in Malaria Mosquitoes

Miller

Chen

Liang

et al. 2022

Genes

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Genes that originate during evolution are an important source of novel biological functions. Retrogenes are functional copies of genes produced by retroduplication and as such are located in different genomic positions. To investigate retroposition patterns and retrogene expression, we computationally identified interchromosomal retroduplication events in nine portions of the phylogenetic history of malaria mosquitoes, making use of species that do or do not have classical sex chromosomes to test the roles of sex-linkage. We found 40 interchromosomal events and a significant excess of retroduplications from the X chromosome to autosomes among a set of young retrogenes. These young retroposition events occurred within the last 100 million years in lineages where all species possessed differentiated sex chromosomes. An analysis of available microarray and RNA-seq expression data for Anopheles gambiae showed that many of the young retrogenes evolved male-biased expression in the reproductive organs. Young autosomal retrogenes with increased meiotic or postmeiotic expression in the testes tend to be male biased. In contrast, older retrogenes, i.e., in lineages with undifferentiated sex chromosomes, do not show this particular chromosomal bias and are enriched for female-biased expression in reproductive organs. Our reverse-transcription PCR data indicates that most of the youngest retrogenes, which originated within the last 47.6 million years in the subgenus Cellia, evolved non-uniform expression patterns across body parts in the males and females of An. coluzzii. Finally, gene annotation revealed that mitochondrial function is a prominent feature of the young autosomal retrogenes. We conclude that mRNA-mediated gene duplication has produced a set of genes that contribute to mosquito reproductive functions and that different biases are revealed after the sex chromosomes evolve. Overall, these results suggest potential roles for the evolution of meiotic sex chromosome inactivation in males and of sexually antagonistic conflict related to mitochondrial energy function as the main selective pressures for X-to-autosome gene reduplication and testis-biased expression in these mosquito lineages.

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Section: Discussionmentioning

confidence: 99%

Retrogene Duplication and Expression Patterns Shaped by the Evolution of Sex Chromosomes in Malaria Mosquitoes

Miller

Chen

Liang

et al. 2022

Genes

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“…gambiae species complex contains the most important malaria vectors in sub-Saharan Africa ( O’Loughlin, 2020 ). Although some studies have shown that lab colonies of different species can cross-mate and produce viable eggs ( Liang et al, 2021 ), five species do not overlap geographically, whilst there are pre-mating barriers between other species ( Diabaté et al, 2009 ). Notably though, hybridisation has been observed between wild An.…”

Section: Endogenous Gene Targets For More Efficient Crispr-based Homi...mentioning

confidence: 99%

Driving down malaria transmission with engineered gene drives

et al. 2022

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The last century has witnessed the introduction, establishment and expansion of mosquito-borne diseases into diverse new geographic ranges. Malaria is transmitted by female Anopheles mosquitoes. Despite making great strides over the past few decades in reducing the burden of malaria, transmission is now on the rise again, in part owing to the emergence of mosquito resistance to insecticides, antimalarial drug resistance and, more recently, the challenges of the COVID-19 pandemic, which resulted in the reduced implementation efficiency of various control programs. The utility of genetically engineered gene drive mosquitoes as tools to decrease the burden of malaria by controlling the disease-transmitting mosquitoes is being evaluated. To date, there has been remarkable progress in the development of CRISPR/Cas9-based homing endonuclease designs in malaria mosquitoes due to successful proof-of-principle and multigenerational experiments. In this review, we examine the lessons learnt from the development of current CRISPR/Cas9-based homing endonuclease gene drives, providing a framework for the development of gene drive systems for the targeted control of wild malaria-transmitting mosquito populations that overcome challenges such as with evolving drive-resistance. We also discuss the additional substantial works required to progress the development of gene drive systems from scientific discovery to further study and subsequent field application in endemic settings.

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Hybridization between Aedes aegypti and Aedes mascarensis mosquitoes leads to disruption of male sex determination

Liang,

Kang,

Michalak

et al. 2024

Commun Biol

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Understanding the sex determination pathway and its disruptions in mosquitoes is critical for the effective control of disease vectors through genetic manipulations based on sex separation. When male hybrids of Aedes aegypti females and Ae. mascarensis males are backcrossed to Ae. aegypti females, a portion of the backcross progeny manifests as males with abnormal sexual differentiation. We discovered a significant correlation between pupal abnormalities and the feminization of subsequent adults exemplified by the relative abundance of ovarian and testicular tissues. All intersex individuals were genetic males as they expressed a male determining factor, Nix. Further, our analysis of the sex-specific splicing of doublesex and fruitless transcripts demonstrated the presence of both male and female splice variants indicating that sex determination is disrupted. A comparative transcriptomic analysis revealed similar expression levels of most female-associated genes in reproductive organs and carcasses between intersexual males and normal females. Moreover, intersexes had largely normal gene expression in testes but significant gene downregulation in male accessory glands when compared with normal males. We conclude that evolving hybrid incompatibilities between Ae. aegypti and Ae. mascarensis involve disruption of sex determination and are accompanied by changes in gene expression associated with sexual differentiation.

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Asymmetric Phenotypes of Sterile Hybrid Males From Reciprocal Crosses Between Species of the Anopheles gambiae Complex

Cited by 4 publications

References 47 publications

Retrogene Duplication and Expression Patterns Shaped by the Evolution of Sex Chromosomes in Malaria Mosquitoes

Retrogene Duplication and Expression Patterns Shaped by the Evolution of Sex Chromosomes in Malaria Mosquitoes

Driving down malaria transmission with engineered gene drives

Hybridization between Aedes aegypti and Aedes mascarensis mosquitoes leads to disruption of male sex determination

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