Title: Drosophila melanogaster sex peptide regulates mated female midgut morphology and physiology
Drosophila melanogaster females 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. more »« less
McDonough-Goldstein, Caitlin E.; Pitnick, Scott; Dorus, Steve
(, Scientific Reports)
null
(Ed.)
Abstract Oocyte composition can directly influence offspring fitness, particularly in oviparous species such as most insects, where it is the primary form of parental investment. Oocyte production is also energetically costly, dependent on female condition and responsive to external cues. Here, we investigated whether mating influences mature oocyte composition in Drosophila melanogaster using a quantitative proteomic approach. Our analyses robustly identified 4,485 oocyte proteins and revealed that stage-14 oocytes from mated females differed significantly in protein composition relative to oocytes from unmated females. Proteins forming a highly interconnected network enriched for translational machinery and transmembrane proteins were increased in oocytes from mated females, including calcium binding and transport proteins. This mating-induced modulation of oocyte maturation was also significantly associated with proteome changes that are known to be triggered by egg activation. We propose that these compositional changes are likely to have fitness consequences and adaptive implications given the importance of oocyte protein composition, rather than active gene expression, to the maternal-to-zygotic transition and early embryogenesis.
Abstract BackgroundMorphologic sex differences between males and females typically emerge after the primordial germ cell migration and gonad formation, although sex is determined at fertilization based on chromosome composition. A key debated sexual difference is the embryonic developmental rate, within vitroproduced male embryos often developing faster. However, the molecular mechanisms driving early embryonic sex differences remain unclear. ResultsTo investigate the transcriptional sex difference during early development,in vitroproduced bovine blastocysts were collected and sexed by PCR. A significant male-biased development was observed in expanded blastocysts. Ultra-low input RNA-seq analysis identified 837 DEGs, with 231 upregulated and 606 downregulated in males. Functional enrichment analysis revealed male-biased DEGs were associated with metabolic regulation, whereas female-biased DEGs were related to female gonad development, sex differentiation, inflammatory pathways, and TGF-beta signaling. Comparing X chromosome and autosome expression ratio, we found that female-biased DEGs contributed to the higher X-linked gene dosage, a phenomenon not observed in male embryos. Moreover, we identified the sex-biased transcription factors and RNA-bind proteins, including pluripotent factors such asSOX21andPRDM14, and splicing factorsFMR1andHNRNPH2. Additionally, we revealed 1,555 significantly sex-biased differential alternative splicing (AS), predominantly skipped exons, mapped to 906 genes, with 59 overlapping with DEGs enriched in metabolic and autophagy pathways. By incorporating novel isoforms from long reads sequencing, we identified 1,151 sex-biased differentially expressed isoforms (DEIs) associated with 1,017 genes. Functional analysis showed that female-biased DEIs were involved in the negative regulation of transcriptional activity, while male-biased DEIs were related to energy metabolism. Furthermore, we identified sex-biased differential exon usage inDENND1B, DIS3L2, DOCK11, IL1RAPL2,andZRSR2Y,indicating their sex-specific regulation in early embryo development. ConclusionThis study provided a comprehensive analysis of transcriptome differences between male and female bovine blastocysts, integrating sex-biased gene expression, alternative splicing, and isoform dynamics. Our findings indicate that enriched metabolism processes in male embryos may contribute to the faster developmental pace, providing insights into sex-specific regulatory mechanisms during early embryogenesis. Plain English summaryMale and female early embryos develop at different speeds, with male embryos often developing faster than female embryos. However, the reasons behind these early differences remain unclear. In this study, we examined gene activity in bovine embryos to uncover the biological factors regulating these early sex differences. We collected in vitro-produced bovine blastocysts, examined their sex, and confirmed that male embryos develop faster. By analyzing global gene activity, including alternative splicing, which allows one gene to code for multiple RNA isoforms and proteins, we found distinct gene expression profiles between male and female embryos. Male embryos showed higher activity in genes related to metabolism and cellular functions, while female embryos had increased activity in genes associated with female-specific gonad development and gene expression regulation. We also examined differences in how genes on the X chromosome were expressed. Female embryos had higher X-linked gene expression, which may contribute to sex-specific developmental regulation. Additionally, we identified sex-specific transcription factors and RNA-binding proteins that regulate early embryo development, some of which are known to control pluripotency and gene splicing. Overall, our study provides new insights into how gene activity shapes early sex differences, suggesting that enhanced metabolism in male embryos may be a key driver of their faster developmental rate. HighlightsMale embryos develop faster due to increased gene expression in metabolism pathwaysFemale embryos exhibit higher X-linked gene expression, suggesting X-dosage compensation plays a role in early developmentSex-biased alternative splicing events contribute to embryonic metabolism, autophagy, and transcriptional regulation in embryosSex-biased isoform diversity contributes to distinct developmental regulation in male and female embryosKey pluripotency factors (SOX21, PRDM14) and splicing regulators (FMR1, HNRNPH2) drive sex-specific gene expression
Lewis, Rebecca J.; Bueno, Gabrielle L.; Di Fiore, Anthony
(, Frontiers in Ecology and Evolution)
Female mammals employ reproductive strategies (e.g., internal gestation) that result in power asymmetries specific to intersexual dyads. Because the number of eggs available for fertilization at any given time for most mammals is quite limited, having a fertilizable egg is potentially an important source of economic power for females. Control over mating opportunities is a source of intersexual leverage for female Verreaux’s sifaka ( Propithecus verreauxi ). We examined economic factors thought to influence the value of mating opportunities, and, thus, the extent of female leverage: kinship and market effects. Using a longitudinal dataset of agonistic interactions collected during focal animal sampling of all adult individuals in 10 social groups from 2008 to 2019, we tested the effects of relatedness, female parity, reproductive season, and adult sex ratio (population and group) on (1) the direction of submissive signaling and (2) which sex won a contested resource. While 96% of the acts of submission were directed from males toward females, females only won a third of their conflicts with males. Thus, our study has implications for evolutionary explanations of female-biased power. If female power evolved due to their greater need for food and other resources, then intersexual conflicts would be expected to result in males more consistently relinquishing control of resources. As expected, males were more likely to chatter submissively toward successful mothers, during the mating season, and when the sex ratio was male-biased. Although females generally had less power to win a conflict when their fertilizable egg was less valuable (when they were nulliparous or unsuccessful mothers or when interacting with male kin) and with an increasing female-bias in the sex ratio, this ability to win additionally was influenced by which sex initiated the conflict. Our study demonstrates that female leverage can be influenced by the supply and demand for mating opportunities, but evoking submission does not translate into winning a resource. Indeed, intersexual power is dynamic, contextual, and dependent on the individuals in the dyad.
Bath, Eleanor; Gleason, Jennifer M
(, Proceedings of the Royal Society B: Biological Sciences)
Aggression is a key determinant of fitness in many species, mediating access to mates, food and breeding sites. Variation in intrasexual aggression across species is likely to be driven by variation in resource availability and distribution. While males primarily compete over access to mates, females are likely to compete over resources to maximize offspring quantity and/or quality, such as food or breeding sites. To date, however, most studies have focused on male aggression, and we know little about drivers of female aggression across species. To investigate potential reproductive drivers of female aggression, we tested the relationship between three reproductive traits and aggression in eightDrosophilaspecies. Using machine learning classifiers developed forDrosophila melanogaster, we quantified aggressive behaviours displayed in the presence of yeast for mated and unmated females. We found that female aggression was correlated with ovariole number across species, suggesting that females who lay more eggs are more aggressive. A need for resources for egg production or oviposition sites may therefore be drivers of female aggression, though other potential hypotheses are discussed.
Saveer, Ahmed M.; DeVries, Zachary C.; Santangelo, Richard G.; Schal, Coby
(, Scientific Reports)
null
(Ed.)
Abstract Reproductive fitness and survival are enhanced by adaptive behaviors that are modulated by internal physiological states and external social contexts. The common bed bug, Cimex lectularius , is an obligate hematophagous ectoparasite that requires host blood for growth, development, and reproduction. We investigated how mating, starvation and social interactions affect host-seeking, blood feeding, oviposition, and survival of female bed bugs. The percentage of females that fed and the amount of blood they ingested were greater in mated females (90–100%) than in unmated females (48–60%). Mating state also modulated the female’s orientation towards human skin odor in an olfactometer; more mated (69%) than unmated (23%) females responded to human odors. The response rate of unmated females (60%) to skin odor increased with longer starvation period, while the opposite pattern was observed in mated females (20%). Although fecundity after a single blood meal was unaffected by long or short residence and interaction with males, females subjected to frequent copulation attempts had lower survivorship and lifespan than females housed with males for only 24 h. Taken together, these results indicate that by adaptively and coordinately expressing behaviors based on the internal physiological state, females maximize their survival and reproductive fitness.
White, Melissa A., Bonfini, Alessandro, Wolfner, Mariana F., and Buchon, Nicolas. Drosophila melanogaster sex peptide regulates mated female midgut morphology and physiology. Retrieved from https://par.nsf.gov/biblio/10222591. Proceedings of the National Academy of Sciences 118.1 Web. doi:10.1073/pnas.2018112118.
White, Melissa A., Bonfini, Alessandro, Wolfner, Mariana F., & Buchon, Nicolas. Drosophila melanogaster sex peptide regulates mated female midgut morphology and physiology. Proceedings of the National Academy of Sciences, 118 (1). Retrieved from https://par.nsf.gov/biblio/10222591. https://doi.org/10.1073/pnas.2018112118
White, Melissa A., Bonfini, Alessandro, Wolfner, Mariana F., and Buchon, Nicolas.
"Drosophila melanogaster sex peptide regulates mated female midgut morphology and physiology". Proceedings of the National Academy of Sciences 118 (1). Country unknown/Code not available. https://doi.org/10.1073/pnas.2018112118.https://par.nsf.gov/biblio/10222591.
@article{osti_10222591,
place = {Country unknown/Code not available},
title = {Drosophila melanogaster sex peptide regulates mated female midgut morphology and physiology},
url = {https://par.nsf.gov/biblio/10222591},
DOI = {10.1073/pnas.2018112118},
abstractNote = {Drosophila melanogaster females 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.},
journal = {Proceedings of the National Academy of Sciences},
volume = {118},
number = {1},
author = {White, Melissa A. and Bonfini, Alessandro and Wolfner, Mariana F. and Buchon, Nicolas},
editor = {null}
}
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