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Seminal fluid gene expression and reproductive fitness in Drosophila melanogaster

BACKGROUND: The rapid evolution of seminal fluid proteins (SFPs) has been suggested to be driven by adaptations to postcopulatory sexual selection (e.g. sperm competition). However, we have recently shown that most SFPs evolve rapidly under relaxed selective pressures. Given the role of SFPs in comp...

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Autores principales: Patlar, Bahar, Civetta, Alberto
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8867848/
https://www.ncbi.nlm.nih.gov/pubmed/35196983
http://dx.doi.org/10.1186/s12862-022-01975-1
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author Patlar, Bahar
Civetta, Alberto
author_facet Patlar, Bahar
Civetta, Alberto
author_sort Patlar, Bahar
collection PubMed
description BACKGROUND: The rapid evolution of seminal fluid proteins (SFPs) has been suggested to be driven by adaptations to postcopulatory sexual selection (e.g. sperm competition). However, we have recently shown that most SFPs evolve rapidly under relaxed selective pressures. Given the role of SFPs in competition for fertilization phenotypes, like the ability to transfer and store sperm and the modulation of female receptivity and ovulation, the prevalence of selectively relaxed SFPs appears as a conundrum. One possible explanation is that selection on SFPs might be relaxed in terms of protein amino acid content, but adjustments of expression are essential for post-mating function. Interestingly, there is a general lack of systematic implementation of gene expression perturbation assays to monitor their effect on phenotypes related to sperm competition. RESULTS: We successfully manipulated the expression of 16 SFP encoding genes using tissue-specific knockdowns (KDs) and determined the effect of these genes’ perturbation on three important post-mating phenotypes: female refractoriness to remating, defensive (P1), and offensive (P2) sperm competitive abilities in Drosophila melanogaster. Our analyses show that KDs of tested SFP genes do not affect female refractoriness to remating and P2, however, most gene KDs significantly decreased P1. Moreover, KDs of SFP genes that are selectively constrained in terms of protein-coding sequence evolution have lower P1 than KDs of genes evolving under relaxed selection. CONCLUSIONS: Our results suggest a more predominant role, than previously acknowledged, of variation in gene expression than coding sequence changes on sperm competitive ability in D. melanogaster. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12862-022-01975-1.
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spelling pubmed-88678482022-02-25 Seminal fluid gene expression and reproductive fitness in Drosophila melanogaster Patlar, Bahar Civetta, Alberto BMC Ecol Evol Research BACKGROUND: The rapid evolution of seminal fluid proteins (SFPs) has been suggested to be driven by adaptations to postcopulatory sexual selection (e.g. sperm competition). However, we have recently shown that most SFPs evolve rapidly under relaxed selective pressures. Given the role of SFPs in competition for fertilization phenotypes, like the ability to transfer and store sperm and the modulation of female receptivity and ovulation, the prevalence of selectively relaxed SFPs appears as a conundrum. One possible explanation is that selection on SFPs might be relaxed in terms of protein amino acid content, but adjustments of expression are essential for post-mating function. Interestingly, there is a general lack of systematic implementation of gene expression perturbation assays to monitor their effect on phenotypes related to sperm competition. RESULTS: We successfully manipulated the expression of 16 SFP encoding genes using tissue-specific knockdowns (KDs) and determined the effect of these genes’ perturbation on three important post-mating phenotypes: female refractoriness to remating, defensive (P1), and offensive (P2) sperm competitive abilities in Drosophila melanogaster. Our analyses show that KDs of tested SFP genes do not affect female refractoriness to remating and P2, however, most gene KDs significantly decreased P1. Moreover, KDs of SFP genes that are selectively constrained in terms of protein-coding sequence evolution have lower P1 than KDs of genes evolving under relaxed selection. CONCLUSIONS: Our results suggest a more predominant role, than previously acknowledged, of variation in gene expression than coding sequence changes on sperm competitive ability in D. melanogaster. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12862-022-01975-1. BioMed Central 2022-02-23 /pmc/articles/PMC8867848/ /pubmed/35196983 http://dx.doi.org/10.1186/s12862-022-01975-1 Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Patlar, Bahar
Civetta, Alberto
Seminal fluid gene expression and reproductive fitness in Drosophila melanogaster
title Seminal fluid gene expression and reproductive fitness in Drosophila melanogaster
title_full Seminal fluid gene expression and reproductive fitness in Drosophila melanogaster
title_fullStr Seminal fluid gene expression and reproductive fitness in Drosophila melanogaster
title_full_unstemmed Seminal fluid gene expression and reproductive fitness in Drosophila melanogaster
title_short Seminal fluid gene expression and reproductive fitness in Drosophila melanogaster
title_sort seminal fluid gene expression and reproductive fitness in drosophila melanogaster
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8867848/
https://www.ncbi.nlm.nih.gov/pubmed/35196983
http://dx.doi.org/10.1186/s12862-022-01975-1
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