Mating-Induced Transcriptome Changes in the Reproductive Tract of Female Aedes aegypti

Alfonso-Parra, Catalina; Ahmed-Braimah, Yasir H.; Degner, Ethan C.; Avila, Frank W.; Villarreal, Susan M.; Pleiss, Jeffrey A.; Wolfner, Mariana F.; Harrington, Laura C.

doi:10.1371/journal.pntd.0004451

Cited by 82 publications

(134 citation statements)

References 80 publications

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“…2006; Innocenti and Morrow 2009; Gomulski et al. 2012; Alfonso-Parra et al. 2016), we found that mating increases the expression of genes involved in metabolism of carbohydrates and lipids, and reduction of oxidative stress in the female abdomen (supplementary table S6 a , Supplementary Material online).…”

Section: Discussionmentioning

confidence: 99%

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Mating Changes Sexually Dimorphic Gene Expression in the Seed Beetle Callosobruchus maculatus

Immonen

Sayadi

Bayram

et al. 2017

Genome Biology and Evolution

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Sexually dimorphic phenotypes arise largely from sex-specific gene expression, which has mainly been characterized in sexually naïve adults. However, we expect sexual dimorphism in transcription to be dynamic and dependent on factors such as reproductive status. Mating induces many behavioral and physiological changes distinct to each sex and is therefore expected to activate regulatory changes in many sex-biased genes. Here, we first characterized sexual dimorphism in gene expression in Callosobruchus maculatus seed beetles. We then examined how females and males respond to mating and how it affects sex-biased expression, both in sex-limited (abdomen) and sex-shared (head and thorax) tissues. Mating responses were largely sex-specific and, as expected, females showed more genes responding compared with males (∼2,000 vs. ∼300 genes in the abdomen, ∼500 vs. ∼400 in the head and thorax, respectively). Of the sex-biased genes present in virgins, 16% (1,041 genes) in the abdomen and 17% (243 genes) in the head and thorax altered their relative expression between the sexes as a result of mating. Sex-bias status changed in 2% of the genes in the abdomen and 4% in the head and thorax following mating. Mating responses involved de-feminization of females and, to a lesser extent, de-masculinization of males relative to their virgin state: mating decreased rather than increased dimorphic expression of sex-biased genes. The fact that regulatory changes of both types of sex-biased genes occurred in both sexes suggests that male- and female-specific selection is not restricted to male- and female-biased genes, respectively, as is sometimes assumed.

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Section: Discussionmentioning

confidence: 99%

“…2008; Rogers et al. 2008; Alfonso-Parra et al. 2016) and Ceratitis capitata fruit flies (Gomulski et al.…”

Section: Introductionmentioning

confidence: 99%

Mating Changes Sexually Dimorphic Gene Expression in the Seed Beetle Callosobruchus maculatus

Immonen

Sayadi

Bayram

et al. 2017

Genome Biology and Evolution

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“…For example, the sequenced genomes of A. aegypti (Nene et al, ), A. albopictus (Chen et al, ), C. quinquefasciatus (Arensburger et al, ), and 16 Anopheles species (Neafsey et al, ) provides a resource to mine for sperm‐relevant genes that are homologous to D. melanogaster or other organisms. Transcriptomics of reproductive tissues in A. aegypti (Akbari et al, ; Alfonso‐Parra et al, ) and A. gambiae (Rogers et al, ; Baker et al, ) and proteomics of semen and sperm in A. aegypti (Sirot et al, ) and A. albopictus (Boes et al, ) provide databases from which specific genes of interest can be investigated. Finally, targeted mutagenesis has been accomplished in mosquitoes using rapidly advancing genome editing techniques, such as transcription activator‐like effector nuclease (TALENs) (Aryan et al, ; Smidler et al, ), zinc‐finger nucleases (DeGennaro et al, ; McMeniman et al, ), and, most recently, the CRISPR‐Cas9 system (Dong et al, ; Kistler et al, ).…”

Section: Discussionmentioning

confidence: 99%

A mosquito sperm's journey from male ejaculate to egg: Mechanisms, molecules, and methods for exploration

Degner

Harrington

2016

Molecular Reproduction Devel

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SUMMARYThe fate of mosquito sperm in the female reproductive tract has been addressed sporadically and incompletely, resulting in significant gaps in our understanding of sperm‐female interactions that ultimately lead to fertilization. As with other Diptera, mosquito sperm have a complex journey to their ultimate destination, the egg. After copulation, sperm spend a short time at the site of insemination where they are hyperactivated and quickly congregate near the entrance of the spermathecal ducts. Within minutes, they travel up the narrow ducts to the spermathecae, likely through the combined efforts of female transport and sperm locomotion. The female nourishes sperm and maintains them in these permanent storage organs for her entire life. When she is ready, the female coordinates the release of sperm with ovulation, and the descending egg is fertilized. Although this process has been well studied via microscopy, many questions remain regarding the molecular processes that coordinate sperm motility, movement through the reproductive tract, maintenance, and usage. In this review, we describe the current understanding of a mosquito sperm's journey to the egg, highlighting gaps in our knowledge of mosquito reproductive biology. Where insufficient information is available in mosquitoes, we describe analogous processes in other organisms, such as Drosophila melanogaster, as a basis for comparison, and we suggest future areas of research that will illuminate how sperm successfully traverse the female reproductive tract. Such studies may yield molecular targets that could be manipulated to control populations of vector species. Mol. Reprod. Dev. 83: 897–911, 2016. © 2016 The Authors. Molecular Reproduction and Development Published by Wiley Periodicals, Inc.

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“…By contrast, reproduction in other dipteran species has been examined extensively [18][19][20][21][22][23][24][25][26][27][28][29][30] . In most Diptera, insemination does not involve injection of a spermatophore; rather, male seminal fluid is usually transferred directly into the female reproductive tract, often with the addition of a mating plug to reduce male-male competition as is seen in mosquitoes and Drosophila [31][32][33][34] .…”

Section: Introductionmentioning

confidence: 99%

Multi-level analysis of reproduction in the Antarctic midge,Belgica antarctica, identifies female and male accessory gland products that are altered by larval stress and impact progeny viability

Finch

Perrieta

Davis

et al. 2019

Preprint

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Background -The Antarctic midge, Belgica antarctica, is a wingless, non-biting midge endemic to Antarctica. Larval development requires at least two years, but adult life lasts only two weeks. The nonfeeding adults mate in swarms and females die shortly after oviposition. Eggs are suspended in a gel of unknown composition that is expressed from the female accessory gland. This project characterizes molecular mechanisms underlying reproduction in this midge by examining differential gene expression in whole males, females, and larvae, as well as in male and female accessory glands. Functional studies were used to assess the role of the gel encasing the eggs, as well as the impact of stress on reproductive biology.Results -RNA-seq analyses revealed sex-and development-specific gene sets along with those associated with the accessory glands. Proteomic analyses were used to define the composition of the egg-containing gel, which is generated during multiple developmental stages and derived from both the accessory gland and other female organs. Functional studies indicate the gel provides a larval food source and thermal and dehydration buffer, all of which are critical for viability. Larval dehydration stress directly reduces production of storage proteins and key accessory gland components, a feature that impacts adult reproductive success. Modeling reveals that bouts of dehydration may significantly impact population growth. Conclusions -This work lays a foundation for further examination of reproduction in midges andprovides new information related to general reproduction in dipterans. A key aspect is that reproduction and stress dynamics, currently understudied in polar organisms, are likely to prove critical for determining how climate change will alter survivability.

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Mating-Induced Transcriptome Changes in the Reproductive Tract of Female Aedes aegypti

Cited by 82 publications

References 80 publications

Mating Changes Sexually Dimorphic Gene Expression in the Seed Beetle Callosobruchus maculatus

Mating Changes Sexually Dimorphic Gene Expression in the Seed Beetle Callosobruchus maculatus

A mosquito sperm's journey from male ejaculate to egg: Mechanisms, molecules, and methods for exploration

Multi-level analysis of reproduction in the Antarctic midge,Belgica antarctica, identifies female and male accessory gland products that are altered by larval stress and impact progeny viability

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