Extensive genetic differentiation between homomorphic sex chromosomes in the mosquito vector, Aedes aegypti

AbstractMechanisms and evolutionary dynamics of sex-determination systems are of particular interest in insect vectors of human pathogens like mosquitoes because novel control strategies aim to convert pathogen-transmitting females into non-biting males, or rely on accurate sexing for the release of sterile males. In Aedes aegypti, the main vector of dengue and Zika viruses, sex determination is governed by a dominant male-determining locus, previously thought to reside within a small, non-recombining, sex-determining region (SDR) of an otherwise homomorphic sex chromosome. Here, we provide evidence that sex chromosomes in Ae. aegypti are genetically differentiated between males and females over a region much larger than the SDR. Our linkage mapping intercrosses failed to detect recombination between X and Y chromosomes over a 123-Mbp region (40% of their physical length) containing the SDR. This region of reduced male recombination overlapped with a smaller 63-Mbp region (20% of the physical length of the sex chromosomes) displaying high male-female genetic differentiation in unrelated wild population from Brazil and Australia and in a reference laboratory strain originating from Africa. In addition, the sex-differentiated genomic region was associated with a significant excess of male-to-female heterozygosity and contained a small cluster of loci consistent with Y-specific null alleles. We demonstrate that genetic differentiation between sex chromosomes is sufficient to assign individuals to their correct sex with high accuracy. We also show how data on allele frequency differences between sexes can be used to estimate linkage disequilibrium between loci and the sex-determining locus. Our discovery of large-scale genetic differentiation between sex chromosomes in Ae. aegypti lays a new foundation for mapping and population genomic studies, as well as for mosquito control strategies targeting the sex-determination pathway.

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Extensive Genetic Differentiation between Homomorphic Sex Chromosomes in the Mosquito Vector, Aedes aegypti

Genome Biology and Evolution ◽

10.1093/gbe/evx171 ◽

2017 ◽

Vol 9 (9) ◽

pp. 2322-2335 ◽

Cited By ~ 17

Author(s):

Albin Fontaine ◽

Igor Filipović ◽

Thanyalak Fansiri ◽

Ary A. Hoffmann ◽

Changde Cheng ◽

...

Keyword(s):

Genetic Differentiation ◽

Aedes Aegypti ◽

Sex Chromosomes ◽

Mosquito Vector

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Development and Characterization of Novel Microsatellite Markers for a Dominant Parasitoid (Stethynium Empoasca) in Tea Plantations Using High-throughput Sequencing

10.21203/rs.3.rs-65383/v1 ◽

2020 ◽

Author(s):

Jinyu Li ◽

Longqing Shi ◽

Jie Chen ◽

Minsheng You ◽

Shijun You

Keyword(s):

Biological Control ◽

Gene Flow ◽

Genetic Differentiation ◽

Microsatellite Markers ◽

High Throughput ◽

High Throughput Sequencing ◽

Control Strategies ◽

Null Alleles ◽

Individual Gene ◽

Tea Plantations

Abstract Background: Stethynium empoasca is an egg parasitoid of the predominant tea pest, and is regarded as the most promising candidate for both augmentative and conservative biological control in tea plantations. However, little is presently known about its biology, ecology, and genetics. Methods: Novel microsatellite markers were developed for S. empoasca from transcriptome sequences generated using high-throughput sequencing. The identified markers were then validated and characterized using 98 individuals from five geographically distinct populations through the tests of Hardy–Weinberg equilibrium and linkage disequilibrium as well as the analyses of genetic diversity, genetic differentiation, and gene flow.Results: A total of 54,520 microsatellites were identified from 117Mb clean sequences. By assessing with five geographical populations, a total of 18 loci were demonstrated to be polymorphic, stable, and repetitive. The genetic variation over the 18 loci varied with allele number ranging from 2 to 7, polymorphism information content from 0.234 to 0.634; and observed and expected heterozygosity from 0.166 to 0.686 and 0.276 to 0.753, respectively. Meanwhile, the 18 loci showed a low frequency of null alleles (0 – 0.107), and the inbreeding coefficient revealed a range from −0.143 to 0.173, with the exception of loci Ste36 (0.4076). Based on analysis of these 18 loci, the assessed populations showed low to moderate levels of genetic differentiation, in which individuals clearly grouped into two clusters. And the recent dispersal rates between the geographically distinct populations were identified to be much lower (0.011 – 0.250) than the individual gene exchange rates within a population (0.683 – 0.939).Conclusion: The identified 18 microsatellite markers could reveal a pattern of spatial structure and gene flow in S. empoasca populations according to geographic variability. This work provides an important basis for future studies on how these markers can be used in studies of the biology, genetics, and ecology of this important parasitoid. The findings can further provide important information for the development of biological control strategies in tea plantations. Additionally, our study reaffirms the importance and efficiency of high-throughput sequencing in microsatellite marker development for non-model species lacking reference genome information.

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A functional requirement for sex-determination M/m locus region lncRNA genes in Aedes aegypti female larvae

Scientific Reports ◽

10.1038/s41598-021-90194-7 ◽

2021 ◽

Vol 11 (1) ◽

Author(s):

Keshava Mysore ◽

Limb K. Hapairai ◽

Ping Li ◽

Joseph B. Roethele ◽

Longhua Sun ◽

...

Keyword(s):

Aedes Aegypti ◽

Sex Determination ◽

Population Control ◽

Control Strategies ◽

Adult Males ◽

Non Coding Rna ◽

Female Specific ◽

Interfering Rna ◽

Long Non Coding Rna ◽

Male Mosquitoes

AbstractAlthough many putative long non-coding RNA (lncRNA) genes have been identified in insect genomes, few of these genes have been functionally validated. A screen for female-specific larvicides that facilitate Aedes aegypti male sex separation uncovered multiple interfering RNAs with target sites in lncRNA genes located in the M/m locus region, including loci within or tightly linked to the sex determination locus. Larval consumption of a Saccharomyces cerevisiae (yeast) strain engineered to express interfering RNA corresponding to lncRNA transcripts resulted in significant female death, yet had no impact on male survival or fitness. Incorporation of the yeast larvicides into mass culturing protocols facilitated scaled production and separation of fit adult males, indicating that yeast larvicides could benefit mosquito population control strategies that rely on mass releases of male mosquitoes. These studies functionally verified a female-specific developmental requirement for M/m locus region lncRNA genes, suggesting that sexually antagonistic lncRNA genes found within this highly repetitive pericentromeric DNA sequence may be contributing to the evolution of A. aegypti sex chromosomes.

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Antiviral Effectors and Gene Drive Strategies for Mosquito Population Suppression or Replacement to Mitigate Arbovirus Transmission by Aedes aegypti

Insects ◽

10.3390/insects11010052 ◽

2020 ◽

Vol 11 (1) ◽

pp. 52 ◽

Cited By ~ 6

Author(s):

Adeline Williams ◽

Alexander Franz ◽

William Reid ◽

Ken Olson

Keyword(s):

Aedes Aegypti ◽

Disease Transmission ◽

Mosquito Control ◽

Control Strategies ◽

Mosquito Vector ◽

Close Monitoring ◽

Gene Drive ◽

Population Replacement ◽

Effector Genes ◽

Population Suppression

The mosquito vector Aedes aegypti transmits arthropod-borne viruses (arboviruses) of medical importance, including Zika, dengue, and yellow fever viruses. Controlling mosquito populations remains the method of choice to prevent disease transmission. Novel mosquito control strategies based on genetically manipulating mosquitoes are being developed as additional tools to combat arbovirus transmission. Genetic control of mosquitoes includes two basic strategies: population suppression and population replacement. The former aims to eliminate mosquito populations while the latter aims to replace wild populations with engineered, pathogen-resistant mosquitoes. In this review, we outline suppression strategies being applied in the field, as well as current antiviral effector genes that have been characterized and expressed in transgenic Ae. aegypti for population replacement. We discuss cutting-edge gene drive technologies that can be used to enhance the inheritance of effector genes, while highlighting the challenges and opportunities associated with gene drives. Finally, we present currently available models that can estimate mosquito release numbers and time to transgene fixation for several gene drive systems. Based on the recent advances in genetic engineering, we anticipate that antiviral transgenic Ae. aegypti exhibiting gene drive will soon emerge; however, close monitoring in simulated field conditions will be required to demonstrate the efficacy and utility of such transgenic mosquitoes.

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Activation of the autophagy pathway decreases dengue virus infection in Aedes aegypti cells

Parasites & Vectors ◽

10.1186/s13071-021-05066-w ◽

2021 ◽

Vol 14 (1) ◽

Author(s):

Tse-Yu Chen ◽

Chelsea T. Smartt

Keyword(s):

Aedes Aegypti ◽

Dengue Virus ◽

Small Molecules ◽

Control Strategies ◽

Virus Titer ◽

Denv Infection ◽

Mosquito Vector ◽

Transcript Levels ◽

Rapamycin Treatment ◽

Autophagy Pathway

Abstract Background Mosquito-borne dengue virus (DENV) causes major disease worldwide, impacting 50–100 million people every year, and is spread by the major mosquito vector Aedes aegypti. Understanding mosquito physiology, including antiviral mechanisms, and developing new control strategies have become an important step towards the elimination of DENV disease. In the study reported here, we focused on autophagy, a pathway suggested as having a positive influence on virus replication in humans, as a potential antiviral target in the mosquito. Methods To understand the role played by autophagy in Ae. aegypti, we examined the activation of this pathway in Aag-2 cells, an Ae. aegypti-derived cell line, infected with DENV. Rapamycin and 3-methyladenine, two small molecules that have been shown to affect the function of the autophagy pathway, were used to activate or suppress, respectively, the autophagy pathway. Results At 1-day post-DENV infection in Aag-2 cells, transcript levels of both the microtubule-associated protein light chain 3-phosphatidylethanolamine conjugate (LC3-II) and autophagy-related protein 1 (ATG1) increased. Rapamycin treatment activated the autophagy pathway as early as 1-h post-treatment, and the virus titer had decreased in the Aag-2 cells at 2 days post-infection; in contrast, the 3-methyladenine treatment did not significantly affect the DENV titer. Treatment with these small molecules also impacted the ATG12 transcript levels in DENV-infected cells. Conclusions Our studies revealed that activation of the autophagy pathway through rapamycin treatment altered DENV infection in the mosquito cells, suggesting that this pathway could be a possible antiviral mechanism in the mosquito system. Here we provide fundamental information needed to proceed with future experiments and to improve our understanding of the mosquito’s immune response against DENV. Graphical Abstract

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A Simple PCR Assay for Discrimination of Dengue Vectors from Nsukka LGA, Nigeria

International Annals of Science ◽

10.21467/ias.10.1.67-77 ◽

2020 ◽

Vol 10 (1) ◽

pp. 67-77

Author(s):

Amos Watentena ◽

Ikem Chris Okoye ◽

Ikechukwu Eugene Onah ◽

Onwude Cosmas Ogbonnaya ◽

Emmanuel Ogudu

Keyword(s):

Aedes Aegypti ◽

Aedes Albopictus ◽

Mosquito Species ◽

Public Health Problem ◽

Major Public Health Problem ◽

Mosquito Vector ◽

Aedes Mosquitoes ◽

Allele Specific ◽

Arboviral Diseases ◽

Dengue Vectors

Mosquitoes of Aedes species are vectors of several arboviral diseases which continue to be a major public health problem in Nigeria. This study among other things, morphologically identified Aedes mosquitoes collected from Nsukka LGA and used an allele specific PCR amplification for discrimination of dengue vectors. Larval sampling, BG-sentinel traps and modified human landing catches were used for mosquito sampling in two selected autonomous communities of Nsukka LGA (Nsukka and Obimo). A total of 124 Aedes mosquitoes consisting of five (5) different species were collected from April to June, 2019 in a cross-sectional study that covered 126 households, under 76 distinct geographical coordinates. Larvae was mainly collected from plastic containers 73% (n=224), metallic containers 14% (n=43), earthen pots 9% (n=29) and used car tyres 3% (n=9), reared to adult stage 69.35% (n=86), and all mosquitoes were identified using standard morphological keys. Five (5) Aedes mosquito species were captured; Aedes aegypti 83(66.94%), Aedes albopictus 33(26.61%), Aedes simpsoni (4.48%), Aedes luteocephalus (≤1%) and Aedes vittatus (≤1%). Nsukka autonomous community had higher species diversity than Obimo. Allele specific amplification confirmed dengue vectors, Aedes aegypti and Aedes albopictus species on a 2% agarose gel. Since the most recent re-emergence of arboviral diseases is closely associated with Aedes species, findings of this study, therefore, give further evidence about the presence of potential arboviral vectors in Nigeria and describe the role of a simple PCR in discriminating some. Further entomological studies should integrate PCR assays in mosquito vector surveillance.

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The Diversity and Evolution of Sex Chromosomes in Frogs

Genes ◽

10.3390/genes12040483 ◽

2021 ◽

Vol 12 (4) ◽

pp. 483

Author(s):

Wen-Juan Ma ◽

Paris Veltsos

Keyword(s):

Sex Determination ◽

Sex Chromosomes ◽

Chromosome Evolution ◽

Sex Chromosome ◽

Comparative Genomic ◽

Ancestral State ◽

Heteromorphic Sex Chromosomes ◽

Genomic Studies ◽

Evolutionary Trajectories ◽

Heterogametic Sex

Frogs are ideal organisms for studying sex chromosome evolution because of their diversity in sex chromosome differentiation and sex-determination systems. We review 222 anuran frogs, spanning ~220 Myr of divergence, with characterized sex chromosomes, and discuss their evolution, phylogenetic distribution and transitions between homomorphic and heteromorphic states, as well as between sex-determination systems. Most (~75%) anurans have homomorphic sex chromosomes, with XY systems being three times more common than ZW systems. Most remaining anurans (~25%) have heteromorphic sex chromosomes, with XY and ZW systems almost equally represented. There are Y-autosome fusions in 11 species, and no W-/Z-/X-autosome fusions are known. The phylogeny represents at least 19 transitions between sex-determination systems and at least 16 cases of independent evolution of heteromorphic sex chromosomes from homomorphy, the likely ancestral state. Five lineages mostly have heteromorphic sex chromosomes, which might have evolved due to demographic and sexual selection attributes of those lineages. Males do not recombine over most of their genome, regardless of which is the heterogametic sex. Nevertheless, telomere-restricted recombination between ZW chromosomes has evolved at least once. More comparative genomic studies are needed to understand the evolutionary trajectories of sex chromosomes among frog lineages, especially in the ZW systems.

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Cytogenetic Analysis of the Asian Box Turtles of the Genus Cuora (Testudines, Geoemydidae)

Genes ◽

10.3390/genes12020156 ◽

2021 ◽

Vol 12 (2) ◽

pp. 156

Author(s):

Lorenzo Clemente ◽

Sofia Mazzoleni ◽

Eleonora Pensabene ◽

Tomáš Protiva ◽

Philipp Wagner ◽

...

Keyword(s):

Sex Determination ◽

Sex Chromosomes ◽

Wide Distribution ◽

Iucn Red List ◽

Telomeric Repeats ◽

Rdna Loci ◽

Box Turtles ◽

Genotypic Sex Determination ◽

Poorly Differentiated ◽

Almost All

The Asian box turtle genus Cuora currently comprises 13 species with a wide distribution in Southeast Asia, including China and the islands of Indonesia and Philippines. The populations of these species are rapidly declining due to human pressure, including pollution, habitat loss, and harvesting for food consumption. Notably, the IUCN Red List identifies almost all species of the genus Cuora as Endangered (EN) or Critically Endangered (CR). In this study, we explore the karyotypes of 10 Cuora species with conventional (Giemsa staining, C-banding, karyogram reconstruction) and molecular cytogenetic methods (in situ hybridization with probes for rDNA loci and telomeric repeats). Our study reveals a diploid chromosome number of 2n = 52 chromosomes in all studied species, with karyotypes of similar chromosomal morphology. In all examined species, rDNA loci are detected at a single medium-sized chromosome pair and the telomeric repeats are restricted to the expected terminal position across all chromosomes. In contrast to a previous report, sex chromosomes are neither detected in Cuoragalbinifrons nor in any other species. Therefore, we assume that these turtles have either environmental sex determination or genotypic sex determination with poorly differentiated sex chromosomes. The conservation of genome organization could explain the numerous observed cases of interspecific hybridization both within the genus Cuora and across geoemydid turtles.

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The maintenance of polygenic sex determination depends on the dominance of fitness effects which are predictive of the role of sexual antagonism

G3 Genes|Genome|Genetics ◽

10.1093/g3journal/jkab149 ◽

2021 ◽

Author(s):

Richard P Meisel

Keyword(s):

Sex Determination ◽

Sex Chromosomes ◽

House Fly ◽

Sexual Antagonism ◽

Antagonistic Effects ◽

Fitness Effects ◽

Y Chromosomes ◽

Sexually Antagonistic Selection ◽

The Individual ◽

Polygenic Sex Determination

Abstract In species with polygenic sex determination, multiple male- and female-determining loci on different proto-sex chromosomes segregate as polymorphisms within populations. The extent to which these polymorphisms are at stable equilibria is not yet resolved. Previous work demonstrated that polygenic sex determination is most likely to be maintained as a stable polymorphism when the proto-sex chromosomes have opposite (sexually antagonistic) fitness effects in males and females. However, these models usually consider polygenic sex determination systems with only two proto-sex chromosomes, or they do not broadly consider the dominance of the alleles under selection. To address these shortcomings, I used forward population genetic simulations to identify selection pressures that can maintain polygenic sex determination under different dominance scenarios in a system with more than two proto-sex chromosomes (modeled after the house fly). I found that overdominant fitness effects of male-determining proto-Y chromosomes are more likely to maintain polygenic sex determination than dominant, recessive, or additive fitness effects. The overdominant fitness effects that maintain polygenic sex determination tend to have proto-Y chromosomes with sexually antagonistic effects (male-beneficial and female-detrimental). In contrast, dominant fitness effects that maintain polygenic sex determination tend to have sexually antagonistic multi-chromosomal genotypes, but the individual proto-sex chromosomes do not have sexually antagonistic effects. These results demonstrate that sexual antagonism can be an emergent property of the multi-chromosome genotype without individual sexually antagonistic chromosomes. My results further illustrate how the dominance of fitness effects has consequences for both the likelihood that polygenic sex determination will be maintained as well as the role sexually antagonistic selection is expected to play in maintaining the polymorphism.

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Predicting Aedes aegypti infestation using landscape and thermal features

Scientific Reports ◽

10.1038/s41598-020-78755-8 ◽

2020 ◽

Vol 10 (1) ◽

Author(s):

Camila Lorenz ◽

Marcia C. Castro ◽

Patricia M. P. Trindade ◽

Maurício L. Nogueira ◽

Mariana de Oliveira Lage ◽

...

Keyword(s):

Remote Sensing ◽

Aedes Aegypti ◽

Vector Control ◽

Land Surface ◽

Urban Areas ◽

Negative Binomial ◽

Control Strategies ◽

Winter Season ◽

Landsat 8 ◽

Thermal Features

AbstractIdentifying Aedes aegypti breeding hotspots in urban areas is crucial for the design of effective vector control strategies. Remote sensing techniques offer valuable tools for mapping habitat suitability. In this study, we evaluated the association between urban landscape, thermal features, and mosquito infestations. Entomological surveys were conducted between 2016 and 2019 in Vila Toninho, a neighborhood of São José do Rio Preto, São Paulo, Brazil, in which the numbers of adult female Ae. aegypti were recorded monthly and grouped by season for three years. We used data from 2016 to 2018 to build the model and data from summer of 2019 to validate it. WorldView-3 satellite images were used to extract land cover classes, and land surface temperature data were obtained using the Landsat-8 Thermal Infrared Sensor (TIRS). A multilevel negative binomial model was fitted to the data, which showed that the winter season has the greatest influence on decreases in mosquito abundance. Green areas and pavements were negatively associated, and a higher cover of asbestos roofs and exposed soil was positively associated with the presence of adult females. These features are related to socio-economic factors but also provide favorable breeding conditions for mosquitos. The application of remote sensing technologies has significant potential for optimizing vector control strategies, future mosquito suppression, and outbreak prediction.

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