scholarly journals A neuropeptide signaling system that rapidly enforces paternity in the Aedes aegypti mosquito

2017 ◽  
Author(s):  
Laura B. Duvall ◽  
Nipun S. Basrur ◽  
Henrik Molina ◽  
Conor J. McMeniman ◽  
Leslie B. Vosshall
Keyword(s):  
Aedes Aegypti ◽  
Egg Production ◽  
Seminal Fluid ◽  
Ejaculatory Duct ◽  
Accessory Gland ◽  
Biologically Active ◽  
Wild Type ◽  
Peptide Receptor ◽  
Sex Peptide ◽  
Asian Tiger

AbstractFemale Dengue and Zika vector mosquitoes (Aedes aegypti) generally mate once, with sperm from this male fertilizing all eggs produced in her lifetime. Here we implicate HP-I, an Aedes- and male-specific neuropeptide transferred to females, and its cognate receptor in the female, NPYLR1, in rapid enforcement of paternity. HP-I mutant males were ineffective in enforcing paternity when a second male was given access to the female within 1 hour. NPYLR1 mutant females produced mixed paternity offspring at high frequency. Synthetic HP-I injected into wild-type virgins reduced successful matings, but had no effect on NPYLR1 mutant females. Asian tiger mosquito (Ae. albopictus) HP-I potently activated Ae. aegypti NPYLR1. Invasive Ae. albopictus males are known to copulate with and sterilize Ae. aegypti females, and cross-species transfer of HP-I may contribute to this phenomenon. This neuropeptide system promotes rapid paternity enforcement within Ae. aegypti, but may promote local extinction in areas where they compete with Ae. albopictus.One Sentence SummaryAedes-specific peptide rapidly enforces paternityTextAe. aegypti females typically mate only once with one male in their lifetime, a behavior known as “monandry” (1). This single mating event provisions the female with sufficient sperm to fertilize the >500 eggs she will produce during her ∼4-6 week lifespan in the laboratory (2). Successful mating is capable of inducing lifetime refractoriness to subsequent insemination by other males, enforcing the paternity of the first male (3-5). In other species, males use diverse strategies to assure the paternity of their offspring, for instance physical barriers such as mating plugs found in mice (6) and Anopheline mosquitoes (7), and anti-aphrodisiac pheromones used by Drosophila melanogaster males to tag female flies as non-virgin (8). Another widely used strategy in insects is the transfer of biologically active male seminal proteins, produced by the male accessory gland and secreted into the ejaculatory duct along with sperm during insemination, to affect the sexual receptivity of the female (3, 9-13). Perhaps the best-characterized male seminal fluid protein in insects is the Drosophila fly sex peptide (11), which acts on the sex peptide receptor in the female to suppress receptivity and trigger egg production (12). Drosophila sex peptide receptor mutant females will readily remate with multiple males, and wild-type females that mate with sex peptide mutant males remain sexually receptive.

scholarly journals Changes in Female Drosophila Sleep following Mating Are Mediated by SPSN-SAG Neurons

2016 ◽  
Vol 31 (6) ◽  
pp. 551-567 ◽  
Author(s):  
David S Garbe ◽  
Abigail S Vigderman ◽  
Emilia Moscato ◽  
Abigail E. Dove ◽  
Christopher G. Vecsey ◽  
...  
Keyword(s):  
Drosophila Melanogaster ◽  
Egg Production ◽  
Behavioral Responses ◽  
Mating Status ◽  
Peptide Receptor ◽  
Dietary Preference ◽  
Sex Peptide ◽  
Central Brain ◽  
Sleep Sex ◽  
Sensorimotor Processes

Female Drosophila melanogaster, like many other organisms, exhibit different behavioral repertoires after mating with a male. These postmating responses (PMRs) include increased egg production and laying, increased rejection behavior (avoiding further male advances), decreased longevity, altered gustation and decreased sleep. Sex Peptide (SP), a protein transferred from the male during copulation, is largely responsible for many of these behavioral responses, and acts through a specific circuit to induce rejection behavior and alter dietary preference. However, less is known about the mechanisms and neurons that influence sleep in mated females. In this study, we investigated postmating changes in female sleep across strains and ages and on different media, and report that these changes are robust and relatively consistent under a variety of conditions. We find that female sleep is reduced by male-derived SP acting through the canonical sex peptide receptor (SPR) within the same neurons responsible for altering other PMRs. This circuit includes the SPSN-SAG neurons, whose silencing by DREADD induces postmating behaviors including sleep. Our data are consistent with the idea that mating status is communicated to the central brain through a common circuit that diverges in higher brain centers to modify a collection of postmating sensorimotor processes.

scholarly journals Drosophila melanogastersex peptide regulates mated female midgut morphology and physiology

2020 ◽  
Vol 118 (1) ◽  
pp. e2018112118
Author(s):  
Melissa A. White ◽  
Alessandro Bonfini ◽  
Mariana F. Wolfner ◽  
Nicolas Buchon
Keyword(s):  
Egg Production ◽  
Energy Homeostasis ◽  
Seminal Fluid ◽  
Large Shift ◽  
Sex Peptide ◽  
Regulation Of Carbohydrate Metabolism ◽  
Lipid Metabolism Genes ◽  
Necessary And Sufficient ◽  
Transcriptomic Changes ◽  
Seminal Fluid Protein

Drosophila melanogasterfemales experience a large shift in energy homeostasis after mating to compensate for nutrient investment in egg production. To cope with this change in metabolism, mated females undergo widespread physiological and behavioral changes, including increased food intake and altered digestive processes. The mechanisms by which the female digestive system responds to mating remain poorly characterized. Here, we demonstrate that the seminal fluid protein Sex Peptide (SP) is a key modulator of female post-mating midgut growth and gene expression. SP is both necessary and sufficient to trigger post-mating midgut growth in females under normal nutrient conditions, and likely acting via its receptor, Sex Peptide Receptor (SPR). Moreover, SP is responsible for almost the totality of midgut transcriptomic changes following mating, including up-regulation of protein and lipid metabolism genes and down-regulation of carbohydrate metabolism genes. These changes in metabolism may help supply the female with the nutrients required to sustain egg production. Thus, we report a role for SP in altering female physiology to enhance reproductive output: Namely, SP triggers the switch from virgin to mated midgut state.

Single-nucleus transcriptomes reveal evolutionary and functional properties of cell types in the Drosophila accessory gland

Genetics ◽  
2021 ◽  
Author(s):  
Alex C Majane ◽  
Julie M Cridland ◽  
David J Begun
Keyword(s):  
Seminal Fluid ◽  
Ejaculatory Duct ◽  
Evolutionary Process ◽  
Cell Types ◽  
Accessory Gland ◽  
Male Reproduction ◽  
Seminal Fluid Proteins ◽  
Cell Diversity ◽  
Single Nucleus ◽  
First Time

Abstract Many traits responsible for male reproduction evolve quickly, including gene expression phenotypes in germline and somatic male reproductive tissues. Rapid male evolution in polyandrous species is thought to be driven by competition among males for fertilizations and conflicts between male and female fitness interests that manifest in post-copulatory phenotypes. In Drosophila, seminal fluid proteins secreted by three major cell types of the male accessory gland and ejaculatory duct are required for female sperm storage and use, and influence female post-copulatory traits. Recent work has shown that these cell types have overlapping but distinct effects on female post-copulatory biology, yet relatively little is known about their evolutionary properties. Here we use single-nucleus RNA-Seq of the accessory gland and ejaculatory duct from Drosophila melanogaster and two closely related species to comprehensively describe the cell diversity of these tissues and their transcriptome evolution for the first time. We find that seminal fluid transcripts are strongly partitioned across the major cell types, and expression of many other genes additionally define each cell type. We also report previously undocumented diversity in main cells. Transcriptome divergence was found to be heterogeneous across cell types and lineages, revealing a complex evolutionary process. Furthermore, protein adaptation varied across cell types, with potential consequences for our understanding of selection on male post-copulatory traits.

scholarly journals Evolutionary History of the Sex-Peptide (Acp70A) Gene Region in Drosophila melanogaster

Genetics ◽  
1997 ◽  
Vol 147 (1) ◽  
pp. 189-197 ◽  
Author(s):  
Susanna Cirera ◽  
Montserrat Aguadé
Keyword(s):  
Evolutionary History ◽  
Seminal Fluid ◽  
Accessory Gland ◽  
Nucleotide Variation ◽  
Coding Region ◽  
Sex Peptide ◽  
Historical Factors ◽  
History Of ◽  
Recent Origin ◽  
Flanking Region

Abstract In Drosophila the products of the seminal fluid stimulate oviposition and suppress remating in the female. Of all the accessory gland peptides (Acp's) involved in these two responses, the sex-peptide (coded by the Acp70A gene) is among the best characterized at the functional level. A 1.2-kb fragment encompassing the Acp70A gene of nine lines from a natural population of D. melanogaster and one allele of D. sechellia was sequenced to study the forces shaping nucleotide variation within and between species. The coding region of D. simulans and D. mauritiana was also sequenced. A Ser to Ala replacement polymorphism at the last position of the signal peptide was detected in D. melanogaster. The Ser and Ala alleles are at intermediate frequencies. The level of nucleotide variation is lower for the derived Ala allele, which is compatible with a recent origin and an increase in frequency due to positive selection. Variation at the 5′ flanking region is structured in two major highly differentiated haplotypes, whose distribution does not conform to neutral expectations. Selective and/or historical factors could contribute to the observed overall patterning of nucleotide variation at the Acp70A region.

scholarly journals Seminal influences: Drosophila Acps and the molecular interplay between males and females during reproduction

2007 ◽  
Vol 47 (3) ◽  
pp. 427-445 ◽  
Author(s):  
K. Ravi Ram ◽  
Mariana F. Wolfner
Keyword(s):  
Egg Production ◽  
Seminal Fluid ◽  
Insect Pests ◽  
Accessory Gland ◽  
Accessory Gland Proteins ◽  
Communication Tools ◽  
Physiological Processes ◽  
Males And Females ◽  
And Behavior ◽  
Female Responses

Abstract Successful reproduction requires contributions from both the male and the female. In Drosophila, contributions from the male include accessory gland proteins (Acps) that are components of the seminal fluid. Upon their transfer to the female, Acps affect the female's physiology and behavior. Although primary sequences of Acp genes exhibit variation among species and genera, the conservation of protein biochemical classes in the seminal fluid suggests a conservation of functions. Bioinformatics coupled with molecular and genetic tools available for Drosophila melanogaster has expanded the functional analysis of Acps in recent years to the genomic/proteomic scale. Molecular interplay between Acps and the female enhances her egg production, reduces her receptivity to remating, alters her immune response and feeding behavior, facilitates storage and utilization of sperm in the female and affects her longevity. Here, we provide an overview of the D. melanogaster Acps and integrate the results from several studies that bring the current number of known D. melanogaster Acps to 112. We then discuss several examples of how the female's physiological processes and behaviors are mediated by interactions between Acps and the female. Understanding how Acps elicit particular female responses will provide insights into reproductive biology and chemical communication, tools for analyzing models of sexual cooperation and/or sexual conflict, and information potentially useful for strategies for managing insect pests.

scholarly journals Single-nucleus transcriptomes reveal functional and evolutionary properties of cell types in the Drosophila accessory gland

2021 ◽  
Author(s):  
Alex C. Majane ◽  
Julie M. Cridland ◽  
David J. Begun
Keyword(s):  
Seminal Fluid ◽  
Ejaculatory Duct ◽  
Evolutionary Process ◽  
Cell Types ◽  
Accessory Gland ◽  
Male Reproduction ◽  
Seminal Fluid Proteins ◽  
Cell Diversity ◽  
Single Nucleus ◽  
First Time

Many traits responsible for male reproduction evolve quickly, including gene expression phenotypes in germline and somatic male reproductive tissues. Rapid male evolution in polyandrous species is thought to be driven by competition among males for fertilizations and conflicts between male and female fitness interests that manifest in post-copulatory phenotypes. In Drosophila, seminal fluid proteins secreted by three major cell types of the male accessory gland and ejaculatory duct are required for female sperm storage and use, and influence female post-copulatory traits. Recent work has shown that these cell types have overlapping but distinct effects on female post-copulatory biology, yet relatively little is known about their evolutionary properties. Here we use single-nucleus RNA-Seq of the accessory gland and ejaculatory duct from Drosophila melanogaster and two closely related species to comprehensively describe the cell diversity of these tissues and their transcriptome evolution for the first time. We find that seminal fluid transcripts are strongly partitioned across the major cell types, and expression of many other genes additionally define each cell type. We also report previously undocumented diversity in main cells. Transcriptome divergence was found to be heterogeneous across cell types and lineages, revealing a complex evolutionary process. Furthermore, protein adaptation varied across cell types, with potential consequences for our understanding of selection on male post-copulatory traits.

scholarly journals Cross-generational fitness benefits of mating and male seminal fluid

2007 ◽  
Vol 4 (1) ◽  
pp. 6-8 ◽  
Author(s):  
Nicholas K Priest ◽  
Deborah A Roach ◽  
Laura F Galloway
Keyword(s):  
Egg Production ◽  
Seminal Fluid ◽  
Accessory Gland ◽  
Sexual Partners ◽  
Good Genes ◽  
Parental Effects ◽  
Accessory Gland Proteins ◽  
Offspring Production ◽  
Female Survival ◽  
Fitness Benefits

In many species, the physical act of mating and exposure to accessory gland proteins (Acps) in male seminal fluid reduces female survival and offspring production. It is not clear what males gain from harming their sexual partners or why females mate frequently despite being harmed. Using sterile strains of Drosophila melanogaster that differ in their production of Acps, we found that both the physical act of mating and exposure to male seminal fluid in mothers increase the fitness of daughters. We show that the changes in daughter fitness are mediated by parental effects, not by sexual selection involving good genes or owing to variation in maternal egg production. These results support the idea that male harm of females might partly evolve through cross-generational fitness benefits.

scholarly journals The Effect of Sex Peptide and Calorie Intake on Fecundity in FemaleDrosophila melanogaster

2009 ◽  
Vol 9 ◽  
pp. 1178-1189 ◽  
Author(s):  
Blanka Rogina
Keyword(s):  
Egg Production ◽  
Accessory Gland ◽  
Calorie Intake ◽  
Accessory Gland Proteins ◽  
Female Response ◽  
Sex Peptide ◽  
Calorie Diet ◽  
And Control ◽  
High Calorie Diet ◽  
High Calorie

The accessory gland proteins (Acps) of the male Drosophila cause changes in the behavior and physiology of female flies. Sex peptide (SP) is one of the Acps that initiates many changes, including an increase in egg production. The data presented here show that SP overexpression in transgenic (G-10) female flies increases egg production when females are kept on a standard and high-calorie diet, relative to controls that do not express SP. Particularly, a high increase in egg production observed in G-10 females on a high-calorie diet suggests that SP overexpression magnifies the female response to caloric uptake. However, on a calorie-restricted diet, the fecundity of G-10 females overexpressing SP is lower than control females. On a high-calorie diet, mating increases early egg production in G-10 and control females, but lifelong total egg production is only increased in control females, most likely due to the physiological changes set off by substantial initial egg production in G-10 females.

scholarly journals Sperm modulate uterine immune parameters relevant to embryo implantation and reproductive success in mice

2021 ◽  
Vol 4 (1) ◽  
Author(s):  
John E. Schjenken ◽  
David J. Sharkey ◽  
Ella S. Green ◽  
Hon Yeung Chan ◽  
Ricky A. Matias ◽  
...  
Keyword(s):  
Reproductive Success ◽  
Seminal Fluid ◽  
Embryo Implantation ◽  
Reproductive Investment ◽  
Global Gene Expression ◽  
Wild Type ◽  
Mouse Uterus ◽  
Immune Parameters ◽  
Oocyte Fertilization

AbstractSeminal fluid factors modulate the female immune response at conception to facilitate embryo implantation and reproductive success. Whether sperm affect this response has not been clear. We evaluated global gene expression by microarray in the mouse uterus after mating with intact or vasectomized males. Intact males induced greater changes in gene transcription, prominently affecting pro-inflammatory cytokine and immune regulatory genes, with TLR4 signaling identified as a top-ranked upstream driver. Recruitment of neutrophils and expansion of peripheral regulatory T cells were elevated by seminal fluid of intact males. In vitro, epididymal sperm induced IL6, CXCL2, and CSF3 in uterine epithelial cells of wild-type, but not Tlr4 null females. Collectively these experiments show that sperm assist in promoting female immune tolerance by eliciting uterine cytokine expression through TLR4-dependent signaling. The findings indicate a biological role for sperm beyond oocyte fertilization, in modulating immune mechanisms involved in female control of reproductive investment.

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