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 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 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

Post-Copulatory Sexual Selection

2021 ◽  
Author(s):  
Patricia L.R. Brennan ◽  
Dara N. Orbach
Keyword(s):  
Sexual Selection ◽  
Sperm Competition ◽  
Female Choice ◽  
Reproductive Tract ◽  
Seminal Fluid ◽  
Fertilization Success ◽  
Female Reproductive Tract ◽  
Cryptic Female Choice ◽  
Trade Offs ◽  
Morphological Criteria

The field of post-copulatory sexual selection investigates how female and male adaptations have evolved to influence the fertilization of eggs while optimizing fitness during and after copulation, when females mate with multiple males. When females are polyandrous (one female mates with multiple males), they may optimize their mating rate and control the outcome of mating interactions to acquire direct and indirect benefits. Polyandry may also favor the evolution of male traits that offer an advantage in post-copulatory male-male sperm competition. Sperm competition occurs when the sperm, seminal fluid, and/or genitalia of one male directly impacts the outcome of fertilization success of a rival male. When a female mates with multiple males, she may use information from a number of traits to choose who will sire her offspring. This cryptic female choice (CFC) to bias paternity can be based on behavioral, physiological, and morphological criteria (e.g., copulatory courtship, volume and/or composition of seminal fluid, shape of grasping appendages). Because male fitness interests are rarely perfectly aligned with female fitness interests, sexual conflict over mating and fertilization commonly occur during copulatory and post-copulatory interactions. Post-copulatory interactions inherently involve close associations between female and male reproductive characteristics, which in many species potentially include sperm storage and sperm movement inside the female reproductive tract, and highlight the intricate coevolution between the sexes. This coevolution is also common in genital morphology. The great diversity of genitalia among species is attributed to sexual selection. The evolution of genital attributes that allow females to maintain reproductive autonomy over paternity via cryptic female choice or that prevent male manipulation and sexual control via sexually antagonistic coevolution have been well documented. Additionally, cases where genitalia evolve through intrasexual competition are well known. Another important area of study in post-copulatory sexual selection is the examination of trade-offs between investments in pre-copulatory and post-copulatory traits, since organisms have limited energetic resources to allocate to reproduction, and securing both mating and fertilization is essential for reproductive success.

scholarly journals Evolution of species-specific major seminal fluid proteins in placental mammals by gene death and positive selection

2015 ◽  
Vol 84 (3) ◽  
pp. 217-235 ◽  
Author(s):  
Camille Meslin ◽  
Michel Laurin ◽  
Isabelle Callebaut ◽  
Xavier Druart ◽  
Philippe Monget
Keyword(s):  
Amino Acids ◽  
Positive Selection ◽  
Statistical Power ◽  
Animal Species ◽  
Seminal Fluid ◽  
Domestic Animal ◽  
Secreted Proteins ◽  
Seminal Fluid Proteins ◽  
Species Specific ◽  
Complex Substance

The seminal fluid is a complex substance composed of a variety of secreted proteins and has been shown to play an important role in the fertilisation process in mammals and also in Drosophila. Several genes under positive selection have been documented in some rodents and primates. Our study documents this phenomenon in several other mammalian taxa. We study the evolution of genes that encode for 20 proteins that are quantitatively predominant in the seminal fluid of at least one out of seven domestic animal species. We analyse the amino acid composition of these proteins for positive selection and for the presence of pseudogenes. Genes that disappeared through pseudogenisation include KLK2 in cattle, horse and mice. Traces of positive selection are found in seven genes. The identified amino acids are located in regions exposed to the protein surface, suggesting a role in the interaction of gametes, with possible impact on the process of speciation. Moreover, we found no evidence that the predominance of proteins in seminal fluid and their mode of evolution are correlated, and the uncoupled patterns of change suggest that this result is not due solely to lack of statistical power.

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 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 Sex-biased genes expressed in the cricket brain evolve rapidly

2020 ◽  
Author(s):  
Carrie A. Whittle ◽  
Arpita Kulkarni ◽  
Cassandra G. Extavour
Keyword(s):  
Gene Expression ◽  
Sexual Selection ◽  
Positive Selection ◽  
Protein Sequence ◽  
Seminal Fluid ◽  
Sequence Evolution ◽  
Evolutionary Trend ◽  
A Genome ◽  
The Brain ◽  
Protein Sequence Evolution

AbstractBackgroundSex-biased gene expression, particularly male-biased expression in the gonad, has often been linked to rapid protein sequence evolution (dN/dS) in animals. This evolutionary trend may arise from one or both of sexual selection pressures during mating or low pleiotropy. In insects, research on sex-biased transcription and dN/dS remains largely focused on a few holometabolous species, with variable findings on male and female gonadal effects. The brain is central to the mating process, and provides neurological foundation for mating behaviors, such as courtship, intrasex competition and mate choice. However, there is a striking paucity of research on sex-biased expression of genes in the brain and the rate of protein sequence evolution in such genes.ResultsHere, we studied sex-biased gene expression in a hemimetabolous insect, the cricket Gryllus bimaculatus. We generated novel RNA-seq data for two sexual tissue types, the gonad and somatic reproductive system, and for two core components of the nervous system, the brain and ventral nerve cord. From a genome-wide analysis of genes expressed in these tissues, we report the accelerated evolution of testis-biased genes and seminal fluid proteins (SFPs) genes, as compared to ovary-biased and unbiased genes in this cricket model, which includes an elevated frequency of positive selection events. With respect to the brain, while sex-biased brain genes were much less common than for the gonads, they exhibited exceptionally rapid evolution, an effect that was stronger for the female than for the male brain. Certain sex-biased brain genes were predicted to be involved in mating or sex-related functions, which we suggest may cause exposure to sexual selection. Moreover, the sex-biased brain genes exhibited remarkably low cross-tissue expression breadth, or pleiotropy. We speculate that this feature may permit relaxed purifying selection, and allow the freedom for adaptive protein functional changes in these brain-expressed genes.ConclusionsOur results demonstrate that sex-biased expression in the male gonad, and sex-biased gene expression in the brain, especially the female brain, are associated with rapid protein sequence evolution in a cricket model system. We discuss the results with respect to our findings on pleiotropy and positive selection, and consider the potential role of the dynamic mating biology of this cricket model in shaping these patterns.

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