scholarly journals Sexual selection rewires reproductive protein networks

2018 ◽  
Author(s):  
Timothy L. Karr ◽  
Helen Southern ◽  
Matthew Rosenow ◽  
Toni I. Gossmann ◽  
Rhonda R. Snook
Keyword(s):  
Sexual Selection ◽  
Seminal Fluid ◽  
Sodium Dodecylsulfate ◽  
Rapid Evolution ◽  
Accessory Gland ◽  
Protein Networks ◽  
Reproductive Proteins ◽  
Seminal Fluid Proteins ◽  
Search Tool ◽  
Reproductive Protein

Polyandry drives postcopulatory sexual selection (PCSS), resulting in rapid evolution of male ejaculate traits. Critical to male and female fitness, the ejaculate is known to contain rapidly evolving seminal fluid proteins (SFPs) produced by specialized male secretory accessory glands. The evidence that rapid evolution of some SFPs is driven by PCSS, however, is indirect, based on either plastic responses to changes in the sexual selection environment or correlative macroevolutionary patterns. Moreover, such studies focus on SFPs that represent but a small component of the accessory gland proteome. Neither how SFPs function with other reproductive proteins, nor how PCSS influences the underlying secretory tissue adaptations and content of the accessory gland, has been addressed at the level of the proteome. Here we directly test the hypothesis that PCSS results in rapid evolution of the entire male accessory gland proteome and protein networks by taking a system-level approach, combining divergent experimental evolution of PCSS in Drosophila pseudoobscura (Dpse), high resolution mass spectrometry (MS) and proteomic discovery, bioinformatics and population genetic analyses. We demonstrate that PCSS influences the abundance of over 200 accessory gland proteins, including SFPs. A small but significant number of these proteins display molecular signatures of positive selection. Divergent PCSS also results in fundamental and remarkably compartmentalized evolution of accessory gland protein networks in which males subjected to strong PCSS invest in protein networks that serve to increase protein production whereas males subjected to relaxed PCSS alters protein networks involved in protein surveillance and quality. These results directly demonstrate that PCSS is a key evolutionary driver that shapes not only individual reproductive proteins, but rewires entire reproductive protein networks.The abbreviations used are:BLASTBasic Local Alignment Search ToolDpseDrosophila pseudoobscuraPCSSpostcopulatory sexual selectionSFPsseminal fluid proteinsDmelD. melanogasterSDSsodium dodecylsulfateSDS-PAGEsodium dodecylsulfate polyacrylamide gel electrophoresisMSmass spectrometryLC-MS/MSliquid chromatography-MS/MSAcgPaccessory gland proteomeFDRsFalse Discovery RatesAcgSaccessory gland secretomeexoPexoproteomeLFQlabel-free quantitationPpolyandryMmonandryGOgene ontologyCCcellular componentMFmolecular functionBPbiological processSTRINGSearch Tool for the Retrieval of Interacting Genes/ProteinsDIOPTDRSC Integrative Ortholog Prediction ToolsERendoplasmic reticulum

scholarly journals Rapid divergence of the copulation proteins in the Drosophila dunni group is associated with hybrid post-mating-prezygotic incompatibilities

2020 ◽  
Author(s):  
Tom Hill ◽  
Hazel-Lynn Rosales-Stephens ◽  
Robert L. Unckless
Keyword(s):  
Seminal Fluid ◽  
Rapid Evolution ◽  
Species Group ◽  
Egg Laying ◽  
Reproductive Proteins ◽  
Seminal Fluid Proteins ◽  
Prezygotic Isolation ◽  
Caribbean Islands ◽  
Female Survival ◽  
Rapid Divergence

AbstractProteins involved in post-copulatory interactions between males and females are among the fastest evolving genes in many species and this has been attributed to reproductive conflict. Likely as a result, these proteins are frequently involved in cases of post-mating-prezygotic isolation between species. The Drosophila dunni subgroup consists of a dozen recently diverged species found across the Caribbean islands with varying levels of hybrid incompatibility. We sought to examine how post-mating-prezygotic factors are involved in isolation among members of this species group. We performed experimental crosses between species in the dunni group and find evidence of hybrid inviability. We also find an insemination reaction-like response preventing egg laying and leading to reduced female survival post-mating. To identify that genes may be involved in these incompatibilities, we sequenced and assembled the genomes of four species in the dunni subgroup and looked for signals of rapid evolution between species. Despite low levels of divergence, we found evidence of rapid evolution and divergence of some reproductive proteins, specifically the seminal fluid proteins. This suggests post-mating-prezygotic isolation as a barrier for gene flow between even the most closely related species in this group and seminal fluid proteins as a possible culprit.

scholarly journals Rapid divergence of the male reproductive proteins in theDrosophila dunnigroup and implications for postmating incompatibilities between species

2021 ◽  
Vol 11 (4) ◽  
Author(s):  
Tom Hill ◽  
Hazel-Lynn Rosales-Stephens ◽  
Robert L Unckless
Keyword(s):  
Seminal Fluid ◽  
Rapid Evolution ◽  
Reproductive Proteins ◽  
Closely Related Species ◽  
Seminal Fluid Proteins ◽  
Hybrid Incompatibility ◽  
Caribbean Islands ◽  
Rates Of Evolution ◽  
Rapid Divergence ◽  
Postmating Prezygotic Isolation

AbstractProteins involved in post-copulatory interactions between males and females are among the fastest evolving genes in many species, usually attributed to their involvement in reproductive conflict. As a result, these proteins are thought to often be involved in the formation of postmating-prezygotic incompatibilities between species. The Drosophila dunni subgroup consists of a dozen recently diverged species found across the Caribbean islands with varying levels of hybrid incompatibility. We performed experimental crosses between species in the dunni group and see some evidence of hybrid incompatibilities. We also find evidence of reduced survival following hybrid mating, likely due to postmating-prezygotic incompatibilities. We assessed rates of evolution between these species genomes and find evidence of rapid evolution and divergence of some reproductive proteins, specifically the seminal fluid proteins. This work suggests the rapid evolution of seminal fluid proteins may be associated with postmating-prezygotic isolation, which acts as a barrier for gene flow between even the most closely related species.

scholarly journals Rapid Divergence Of The Copulation Proteins In The Drosophila Dunni Group Is Associated With Hybrid Post-Mating-Prezygotic Incompatibilities

2020 ◽  
Author(s):  
Tom Hill ◽  
Hazel-Lynn Rosales-Stephens ◽  
Robert L. Unckless
Keyword(s):  
Seminal Fluid ◽  
Rapid Evolution ◽  
Reproductive Proteins ◽  
Closely Related Species ◽  
Seminal Fluid Proteins ◽  
Hybrid Incompatibility ◽  
Prezygotic Isolation ◽  
Caribbean Islands ◽  
Rates Of Evolution ◽  
Rapid Divergence

Abstract Background: Proteins involved in post-copulatory interactions between males and females are among the fastest evolving genes in many species and this has been attributed to reproductive conflict. Likely as a result, these proteins are frequently involved in cases of post-mating-prezygotic isolation between species. The Drosophila dunni subgroup consists of a dozen recently diverged species found across the Caribbean islands with varying levels of hybrid incompatibility.Results: We performed experimental crosses between species in the dunni group and find evidence of hybrid inviability likely due to post-mating-prezygotic incompatibilities. We next assessed rates of evolution between these species genomes and find evidence of rapid evolution and divergence of some reproductive proteins, specifically the seminal fluid proteins.Conclusions: This work suggests the rapid evolution of seminal fluid proteins can lead to post-mating-prezygotic isolation, which acts as a barrier for gene flow between even the most closely related species.

scholarly journals Sexual Selection Shapes Seminal Vesicle Secretion Gene Expression in House Mice

2019 ◽  
Vol 37 (4) ◽  
pp. 1114-1117 ◽  
Author(s):  
Leigh W Simmons ◽  
Nadia S Sloan ◽  
Renée C Firman
Keyword(s):  
Sexual Selection ◽  
Positive Selection ◽  
Seminal Vesicle ◽  
Seminal Fluid ◽  
Experimental Manipulation ◽  
Female Reproductive Tract ◽  
House Mice ◽  
Evolutionary Divergence ◽  
Reproductive Proteins ◽  
Seminal Fluid Proteins

Abstract Reproductive proteins typically have high rates of molecular evolution, and are assumed to be under positive selection from sperm competition and cryptic female choice. However, ascribing evolutionary divergence in the genome to these processes of sexual selection from patterns of association alone is problematic. Here, we use an experimental manipulation of postmating sexual selection acting on populations of house mice and explore its consequences for the expression of seminal vesicle secreted (SVS) proteins. Following 25 generations of selection, males from populations subjected to postmating sexual selection had evolved increased expression of at least two SVS genes that exhibit the signature of positive selection at the molecular level, SVS1 and SVS2. These proteins contribute to mating plug formation and sperm survival in the female reproductive tract. Our data thereby support the view that sexual selection is responsible for the evolution of these seminal fluid proteins.

scholarly journals Conceptual developments in sperm competition: a very brief synopsis

2020 ◽  
Vol 375 (1813) ◽  
pp. 20200061 ◽  
Author(s):  
Geoff A. Parker
Keyword(s):  
Sexual Selection ◽  
Sperm Competition ◽  
Seminal Fluid ◽  
Female Reproduction ◽  
Internal Fertilization ◽  
Seminal Fluid Proteins ◽  
Competition Theory ◽  
Past Half Century ◽  
Mate Acquisition ◽  
Gamete Competition

The past half century has seen the development of the field of post-ejaculatory sexual selection, the sequel to sexual selection for mate-acquisition (pre-ejaculatory) described by Darwin. In richness and diversity of adaptations, post-ejaculatory selection rivals that of pre-ejaculatory sexual selection. Anisogamy—and hence two sexes—likely arose by primeval gamete competition, and sperm competition remains a major force maintaining high sperm numbers. The post-ejaculatory equivalent of male–male competition for matings, sperm competition was an intense ancestral form of sexual selection, typically weakening as mobility and internal fertilization developed in many taxa, when some expenditure became diverted into pre-ejaculatory competition. Sperm competition theory has been relatively successful in explaining variation in relative testes size and sperm numbers per ejaculate and is becoming more successful in explaining variation in sperm phenotype. Sperm competition has generated many other male adaptations such as seminal fluid proteins that variously modify female reproduction towards male interests, and copulatory plugs, prolonged copulations and post-ejaculatory guarding behaviour that reduce female remating probability, many of which result in sexual conflict. This short survey of conceptual developments is intended as a broad overview, mainly as a primer for new researchers. This article is part of the theme issue ‘Fifty years of sperm competition'.

scholarly journals Differences in Postmating Transcriptional Responses between Conspecific and Heterospecific Matings in Drosophila

2020 ◽  
Author(s):  
Yasir H Ahmed-Braimah ◽  
Mariana F Wolfner ◽  
Andrew G Clark
Keyword(s):  
Reproductive Tract ◽  
Evolutionary Dynamics ◽  
Seminal Fluid ◽  
Female Reproductive Tract ◽  
Additional Stress ◽  
Reproductive Proteins ◽  
Transcriptional Responses ◽  
Seminal Fluid Proteins ◽  
Reproductive Genes ◽  
Imd Pathway

Abstract In many animal species, females undergo physiological and behavioral changes after mating. Some of these changes are driven by male-derived seminal fluid proteins and are critical for fertilization success. Unfortunately, our understanding of the molecular interplay between female and male reproductive proteins remains inadequate. Here, we analyze the postmating response in a Drosophila species that has evolved strong gametic incompatibility with its sister species; Drosophila novamexicana females produce only ∼1% fertilized eggs in crosses with Drosophila americana males, compared to ∼98% produced in within-species crosses. This incompatibility is likely caused by mismatched male and female reproductive molecules. In this study, we use short-read RNA sequencing to examine the evolutionary dynamics of female reproductive genes and the postmating transcriptome response in crosses within and between species. First, we found that most female reproductive tract genes are slow-evolving compared to the genome average. Second, postmating responses in con- and heterospecific matings are largely congruent, but heterospecific matings induce expression of additional stress-response genes. Some of those are immunity genes that are activated by the Imd pathway. We also identify several genes in the JAK/STAT signaling pathway that are induced in heterospecific, but not conspecific mating. While this immune response was most pronounced in the female reproductive tract, we also detect it in the female head and ovaries. These results show that the female’s postmating transcriptome-level response is determined in part by the genotype of the male, and that divergence in male reproductive genes and/or traits can have immunogenic effects on females.

scholarly journals Differences in post-mating transcriptional responses between conspecific and heterospecific matings in Drosophila

2020 ◽  
Author(s):  
Yasir H. Ahmed-Braimah ◽  
Mariana F. Wolfner ◽  
Andrew G. Clark
Keyword(s):  
Reproductive Tract ◽  
Evolutionary Dynamics ◽  
Seminal Fluid ◽  
Female Reproductive Tract ◽  
Additional Stress ◽  
Reproductive Proteins ◽  
Transcriptional Responses ◽  
Seminal Fluid Proteins ◽  
Reproductive Genes ◽  
Imd Pathway

AbstractIn many animal species, females undergo physiological and behavioral changes after mating. Some of these changes are driven by male-derived seminal fluid proteins, and are critical for fertilization success. Unfortunately, our understanding of the molecular interplay between female and male reproductive proteins remains superficial. Here we analyze the post-mating response in a Drosophila species that has evolved strong gametic incompatibility with its sister species; D. novamexicana females produce only 1% fertilized eggs in crosses with D. americana males, compared to ~98% produced in within-species crosses. This incompatibility is likely caused by mismatched male and female reproductive molecules. In this study we use short-read RNA sequencing to examine the evolutionary dynamics of female reproductive genes and the post-mating transcriptome response in crosses within and between species. First, we found that most female reproductive tract genes are slow-evolving compared to the genome average. Second, post-mating responses in con- and heterospecific matings are largely congruent, but heterospecific mating induces expression of additional stress-response genes. Some of those are immunity genes that are activated by the Imd pathway. We also identify several genes in the JAK/STAT signaling pathway that are induced in heterospecific, but not conspecific mating. While this immune response was most pronounced in the female reproductive tract, we also detect it in the female head and ovaries. Our results show that the female’s post-mating transcriptome-level response is determined in part by the genotype of the male, and that divergence in male reproductive genes and/or traits can have immunogenic effects on females.

scholarly journals Rapid evolution of reproductive proteins in abalone and Drosophila

2006 ◽  
Vol 361 (1466) ◽  
pp. 261-268 ◽  
Author(s):  
Tami M Panhuis ◽  
Nathaniel L Clark ◽  
Willie J Swanson
Keyword(s):  
Protein Evolution ◽  
Sexual Conflict ◽  
Reproductive Tract ◽  
Rapid Evolution ◽  
Theoretical Data ◽  
Pathogen Resistance ◽  
Accessory Gland ◽  
Female Reproductive Tract ◽  
Reproductive Proteins ◽  
Accessory Gland Proteins

Observations from different taxa, including plants, protozoa, insects and mammals, indicate that proteins involved in reproduction evolve rapidly. Several models of adaptive evolution have been proposed to explain this phenomenon, such as sexual conflict, sexual selection, self versus non-self recognition and pathogen resistance. Here we discuss the potential role of sexual conflict in the rapid evolution of reproductive genes in two different animal systems, abalone ( Haliotis ) and Drosophila . In abalone, we reveal how specific interacting sperm–egg proteins were identified and discuss this identification in the light of models for rapid protein evolution and speciation. For Drosophila , we describe the genomic approaches taken to identify male accessory gland proteins and female reproductive tract proteins. Patterns of protein evolution from both abalone and Drosophila support the predicted patterns of rapid protein evolution driven by sexual conflict. We stress however that other selective pressures may contribute to the rapid evolution that is observed. We conclude that the key to distinguishing between sexual conflict and other mechanisms of protein evolution will be an integration of genetic, experimental and theoretical data.

scholarly journals Male Seminal Fluid Proteins Are Essential for Sperm Storage in Drosophila melanogaster

Genetics ◽  
1999 ◽  
Vol 153 (2) ◽  
pp. 837-844 ◽  
Author(s):  
Uyen Tram ◽  
Mariana F Wolfner
Keyword(s):  
Drosophila Melanogaster ◽  
Seminal Fluid ◽  
Accessory Gland ◽  
Sperm Storage ◽  
Competitive Pcr ◽  
Seminal Fluid Proteins ◽  
Pcr Assays ◽  
Transgenic Drosophila ◽  
Direct Counts

AbstractThe seminal fluid that is transferred along with sperm during mating acts in many ways to maximize a male’s reproductive success. Here, we use transgenic Drosophila melanogaster males deficient in the seminal fluid proteins derived from the accessory gland (Acps) to investigate the role of these proteins in the fate of sperm transferred to females during mating. Competitive PCR assays were used to show that while Acps contribute to the efficiency of sperm transfer, they are not essential for the transfer of sperm to the female. In contrast, we found that Acps are essential for storage of sperm by females. Direct counts of stored sperm showed that 10% of normal levels are stored by females whose mates transfer little or no Acps along with sperm.

scholarly journals Endocycles support tissue growth and regeneration of the adult Drosophila accessory gland

2019 ◽  
Author(s):  
Allison M. Box ◽  
Samuel Jaimian Church ◽  
David Hayes ◽  
Shyama Nandakumar ◽  
Russell S. Taichman ◽  
...  
Keyword(s):  
Cell Size ◽  
Seminal Fluid ◽  
Cell Types ◽  
Accessory Gland ◽  
Tissue Growth ◽  
Critical Function ◽  
Seminal Fluid Proteins ◽  
Functional Analog ◽  
Secretory Epithelial Cell ◽  
Adult Drosophila

AbstractThe Drosophila melanogaster accessory gland is a functional analog of the mammalian prostate made up of two secretory epithelial cell types, termed main and secondary cells. This tissue is responsible for making and secreting seminal fluid proteins and other molecules that contribute to successful reproduction. Here we show that similar to the mammalian prostate, this tissue grows with age. We find that the adult accessory gland grows in part via endocycles to increase DNA content and cell size, independent of mating status. The differentiated, bi-nucleated main cells remain poised to endocycle in the adult gland and upregulation of signals that promote endocycling and tissue growth are sufficient to trigger dramatic endocycling leading to increases in cell size and ploidy. The main cells of this tissue remain poised to enter the cell cycle and endocycling of main cells increases during recovery from severe tissue damage. Our data establish that the adult accessory gland is not quiescent, but instead uses endocycles to maintain the accessory gland’s critical function throughout the fruit fly’s lifespan.

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