Regional specialization, polyploidy, and seminal fluid transcripts in the Drosophila female reproductive tract DOI Creative Commons
Rachel C. Thayer, Elizabeth S. Polston,

Jixiang Xu

et al.

Proceedings of the National Academy of Sciences, Journal Year: 2024, Volume and Issue: 121(44)

Published: Oct. 25, 2024

Sexual reproduction requires the choreographed interaction of female cells and molecules with sperm seminal fluid. In internally fertilizing animals, these interactions are managed by specialized tissues within reproductive tract (FRT), such as a uterus, glands, storage organs. However, somatic remain understudied, hindering insight into molecular that support fertility. Here, we report identification, characterization, analysis cell types throughout FRT in premier

Language: Английский

The roles of sexual selection and sexual conflict in shaping patterns of genome and transcriptome variation DOI
Nicole M. Tosto, Emily R. Beasley, Bob B. M. Wong

et al.

Nature Ecology & Evolution, Journal Year: 2023, Volume and Issue: 7(7), P. 981 - 993

Published: March 23, 2023

Language: Английский

Citations

35

Functional Diversity and Evolution of the Drosophila Sperm Proteome DOI Creative Commons
Martin D. Garlovsky,

Jessica Sandler,

Timothy L. Karr

et al.

Molecular & Cellular Proteomics, Journal Year: 2022, Volume and Issue: 21(10), P. 100281 - 100281

Published: Aug. 17, 2022

Spermatozoa are central to fertilization and the evolutionary fitness of sexually reproducing organisms. As such, a deeper understanding sperm proteomes (and associated reproductive tissues) has proven critical advancement fields sexual selection biology. Due their extraordinary complexity, proteome depth-of-coverage is dependent on advancements in technology related bioinformatics, both which have made significant decade since last Drosophila was published. Here, we provide an updated version melanogaster (DmSP3) using improved separation detection methods genome annotation. Combined with previous versions proteome, DmSP3 contains total 3176 proteins, first label-free quantitation for 2125 proteins. The top 20 most abundant proteins included structural elements α- β-tubulins leucyl-aminopeptidases. Both gene content protein abundance were significantly reduced X chromosome, consistent prior genomic studies chromosome evolution. We identified 9 16 Y-linked including known testis-specific male fertility factors. also almost one-half ribosomal DmSP3. role this subset unknown. Surprisingly, our expanded 122 seminal fluid (Sfps), originally accessory glands. show that fraction 'sperm-associated Sfps' recalcitrant concentrated salt detergent treatments, suggesting subclass Sfps expressed testes may additional functions sperm, per se. Overall, results add growing landscape biology particular provides quantitative evidence at level findings supporting meiotic sex-chromosome inactivation model male-specific

Language: Английский

Citations

20

Seminal fluid gene expression and reproductive fitness in Drosophila melanogaster DOI Creative Commons
Bahar Patlar, Alberto Civetta

BMC Ecology and Evolution, Journal Year: 2022, Volume and Issue: 22(1)

Published: Feb. 23, 2022

Abstract Background The rapid evolution of seminal fluid proteins (SFPs) has been suggested to be driven by adaptations postcopulatory sexual selection (e.g. sperm competition). However, we have recently shown that most SFPs evolve rapidly under relaxed selective pressures. Given the role in competition for fertilization phenotypes, like ability transfer and store modulation female receptivity ovulation, prevalence selectively appears as a conundrum. One possible explanation is on might terms protein amino acid content, but adjustments expression are essential post-mating function. Interestingly, there general lack systematic implementation gene perturbation assays monitor their effect phenotypes related competition. Results We successfully manipulated 16 SFP encoding genes using tissue-specific knockdowns (KDs) determined these genes’ three important phenotypes: refractoriness remating, defensive (P1), offensive (P2) competitive abilities Drosophila melanogaster . Our analyses show KDs tested do not affect remating P2, however, significantly decreased P1. Moreover, constrained protein-coding sequence lower P1 than evolving selection. Conclusions results suggest more predominant role, previously acknowledged, variation coding changes D.

Language: Английский

Citations

19

The seminal odorant binding protein Obp56g is required for mating plug formation and male fertility in Drosophila melanogaster DOI Creative Commons
Nora C. Brown, Benjamin Gordon, Caitlin E. McDonough-Goldstein

et al.

eLife, Journal Year: 2023, Volume and Issue: 12

Published: Dec. 21, 2023

In Drosophila melanogaster and other insects, the seminal fluid proteins (SFPs) male sex pheromones that enter female with sperm during mating are essential for fertility induce profound post-mating effects on physiology. The SFPs in D. taxa include several members of large gene family known as odorant binding (Obps). Work has shown some Obp genes highly expressed antennae can mediate behavioral responses to odorants, potentially by carrying these molecules receptors. These observations have led hypothesis Obps might act molecular carriers or compounds important fertility, though functional evidence any species is lacking. Here, we used genetics test role seven response (PMR). We found Obp56g required induction PMR, whereas six dispensable. males lacking fail form a plug mated female's reproductive tract, leading ejaculate loss reduced storage, likely due its expression ejaculatory bulb. also examined evolutionary history genes, studies documented rapid evolution turnover SFP across taxa. extensive lability copy number positive selection acting two Obp22a Obp51a. Comparative RNAseq data from tract multiple revealed shows high subset taxa, conserved head phylogeny. Together, suggest may been co-opted function over time.

Language: Английский

Citations

11

Synthesis and Scope of the Role of Postmating Prezygotic Isolation in Speciation DOI
Martin D. Garlovsky, Emma Whittington, Tomáš Albrecht

et al.

Cold Spring Harbor Perspectives in Biology, Journal Year: 2023, Volume and Issue: 16(10), P. a041429 - a041429

Published: Dec. 27, 2023

How barriers to gene flow arise and are maintained key questions in evolutionary biology. Speciation research has mainly focused on that occur either before mating or after zygote formation. In comparison, postmating prezygotic (PMPZ) isolation-a barrier acts gamete release but formation-is less frequently investigated may hold a unique role generating biodiversity. Here we discuss the distinctive features of PMPZ isolation, including primary drivers molecular mechanisms underpinning isolation. We then present first comprehensive survey isolation research, revealing it is widespread form across eukaryotes. The also exposes obstacles studying part attributable challenges involved directly measuring uncovering its causal mechanisms. Finally, identify outstanding knowledge gaps provide recommendations for improving future This will allow us better understand nature this often-neglected reproductive contribution speciation.

Language: Английский

Citations

11

An orphan gene is essential for efficient sperm entry into eggs in Drosophila melanogaster DOI

Sara Y. Guay,

Prajal H. Patel,

Jonathon M. Thomalla

et al.

Genetics, Journal Year: 2025, Volume and Issue: unknown

Published: Feb. 4, 2025

Abstract While spermatogenesis has been extensively characterized in the Drosophila melanogaster model system, very little is known about genes required for fly sperm entry into eggs. We identified a lineage-specific gene, which we named katherine johnson (kj), that efficient fertilization. Males do not express kj produce and transfer are stored normally females, but from these males enter eggs with severely reduced efficiency. Using tagged transgenic rescue construct, observed KJ protein localizes around edge of nucleus at various stages undetectable mature sperm. These data suggest exerts an effect on development, loss results fertilization ability. Interestingly, lacks detectable sequence similarity to any other protein, suggesting could be orphan gene. previous bioinformatic analyses indicated was restricted group Drosophila, putative orthologs conserved synteny, male-biased expression, predicted features across genus, as well likely instances gene some lineages. Thus, present common ancestor. It unclear whether its role fertility had already evolved time or developed later lineage leading D. melanogaster. Our demonstrate new aspect male reproduction shaped by provide molecular foothold further investigating mechanism Drosophila.

Language: Английский

Citations

0

Gene expression differentiation in the reproductive tissues of Drosophila willistoni subspecies and their hybrids DOI Creative Commons
José M. Ranz,

Alwyn C. Go,

Pablo M. González

et al.

Molecular Ecology, Journal Year: 2023, Volume and Issue: 32(13), P. 3605 - 3623

Published: March 31, 2023

Early lineage diversification is central to understand what mutational events drive species divergence. Particularly, gene misregulation in interspecific hybrids can inform about genes and pathways underlie hybrid dysfunction. In Drosophila hybrids, how regulatory evolution impacts different reproductive tissues remains understudied. Here, we generate a new genome assembly annotation willistoni analyse the patterns of transcriptome divergence between two allopatrically evolved D. subspecies, their male sterile female fertile progeny across testis, accessory gland, ovary. Patterns modes were tissue-specific. Despite no indication for cell-type differences this tissue exhibited largest magnitude expression differentiation subspecies parentals hybrids. No evidence anomalous dosage compensation was detected nor differential role neo- ancestral arms X chromosome. Compared autosomes, chromosome appeared enriched transgressively expressed testis despite being least differentiated subspecies. Evidence fine clustering suggests chromatin structure on misregulation. Lastly, GO terms not typically associated with sperm function, instead hinting at development tissue. Our thorough tissue-level portrait recently diverged provides more nuanced view early changes during speciation.

Language: Английский

Citations

8

Single-nucleus transcriptomes reveal evolutionary and functional properties of cell types in theDrosophilaaccessory gland DOI Open Access

Alex C Majane,

Julie M. Cridland,

David J. Begun

et al.

Genetics, Journal Year: 2021, Volume and Issue: 220(2)

Published: Nov. 25, 2021

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

Language: Английский

Citations

18

Socially transferred materials: why and how to study them DOI Creative Commons
Sanja Maria Hakala, Haruna Fujioka, Katharina Gapp

et al.

Trends in Ecology & Evolution, Journal Year: 2022, Volume and Issue: 38(5), P. 446 - 458

Published: Dec. 19, 2022

When biological material is transferred from one individual's body to another, as in ejaculate, eggs, and milk, secondary donor-produced molecules are often along with the main cargo, influence physiology fitness of receiver. Both social solitary animals exhibit such transfers at certain life stages. The secondary, bioactive, transfer-supporting components socially materials have evolved convergently point where they used applications across taxa type transfer. composition these typically highly dynamic context dependent, their drive physiological behavioral evolution many taxa. Our establishment concept unifies this multidisciplinary topic will benefit both theory applications.

Language: Английский

Citations

13

Evolution and genetics of accessory gland transcriptome divergence between Drosophila melanogaster and D. simulans DOI

Alex C Majane,

Julie M. Cridland,

Logan Blair

et al.

Genetics, Journal Year: 2024, Volume and Issue: 227(2)

Published: March 22, 2024

Abstract Studies of allele-specific expression in interspecific hybrids have provided important insights into gene-regulatory divergence and hybrid incompatibilities. Many such investigations Drosophila used transcriptome data from complex mixtures many tissues or gonads, however, regulatory may vary widely among species, sexes, tissues. Thus, we lack sufficiently broad sampling to be confident about the general biological principles divergence. Here, seek fill some these gaps literature by characterizing evolution misexpression a somatic male sex organ, accessory gland, F1 between melanogaster D. simulans. The gland produces seminal fluid proteins, which play an role female fertility subject adaptive due male–male male–female interactions. We find that trans differences are relatively more abundant than cis, contrast most literature, though large effect-size rare. Seminal protein genes significantly elevated levels tend regulated through both cis limited (over- underexpression relative parents) this organ compared other studies. As previous studies, male-biased overrepresented misexpressed much likely underexpressed. ATAC-Seq show chromatin accessibility is correlated with species expression. This work identifies unique properties suggests importance tissue-specific

Language: Английский

Citations

2