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 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 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 Gene Expression and Alternative Splicing Dynamics Are Perturbed in Head Transcriptomes of Heterospecifically Mated Females

2021 ◽  
Author(s):  
Fernando Diaz ◽  
Carson Allan ◽  
Therese Markow ◽  
Jeremy Bono ◽  
Luciano Matzkin
Keyword(s):  
Gene Expression ◽  
Alternative Splicing ◽  
Reproductive Tract ◽  
Seminal Fluid ◽  
Intron Retention ◽  
Transcriptional Responses ◽  
Seminal Fluid Proteins ◽  
Genome Wide ◽  
Amino Acid Balance ◽  
Postmating Behavior

Abstract Background Despite the growing interest in the female side of copulatory interactions, the roles played by alternative splicing mechanisms of pre-RNA and the epistatic effects of these interactions on tissues outside of the reproductive tract have remained largely unknown. Here we addressed these questions in the context of con- vs heterospecific matings between Drosophila mojavensis and its sister species, D. arizonae. We analyzed transcriptional responses in female heads using an integrated investigation of genome-wide patterns of gene expression, including differential expression (DE), alternative splicing (AS) and intron retention (IR). Results Our results indicated that early transcriptional responses were largely congruent between con- and heterospecific matings but are substantially perturbed over time. Conspecific matings induced functional pathways related to amino acid balance previously associated with the brain’s physiology and female postmating behavior. Heterospecific matings often fail to activate regulation of some of these genes and induce expression of additional genes when compared with those of conspecifically-mated females. These results are consistent for all transcriptional mechanisms with some distinctions: DE genes were mostly linked to pathways of proteolysis and nutrient homeostasis, while AS genes are more related to photoreception and muscle assembly pathways. Conclusions IR seem to be an important mechanism of DE regulation during the female postmating response. While AS genes evolve at slower evolutionary rates than the genome background, DE genes evolve at much higher rates, similar or even higher than those of seminal fluid proteins, which unveil their potential role for reproductive barriers and the extent of sexual conflict.

scholarly journals Seminal fluid protein divergence among populations exhibiting postmating prezygotic reproductive isolation

2020 ◽  
Author(s):  
Martin D. Garlovsky ◽  
Caroline Evans ◽  
Mathew A. Rosenow ◽  
Timothy L. Karr ◽  
Rhonda R. Snook
Keyword(s):  
Reproductive Isolation ◽  
High Throughput ◽  
Reproductive Tract ◽  
Seminal Fluid ◽  
Rapid Evolution ◽  
Female Reproductive Tract ◽  
Reproductive Proteins ◽  
Fertilisation Success ◽  
Accessory Glands ◽  
Ejaculatory Bulb

ABSTRACTDespite holding a central role for fertilisation success, reproductive traits often show elevated rates of evolution and diversification. The rapid evolution of seminal fluid proteins (Sfps) within populations is predicted to cause mis-signalling between the male ejaculate and female reproductive tract between populations resulting in postmating prezygotic (PMPZ) isolation. Crosses between populations of Drosophila montana show PMPZ isolation in the form of reduced fertilisation success in both noncompetitive and competitive contexts. Here we test whether male ejaculate proteins deriving from either the accessory glands or the ejaculatory bulb differ between populations using liquid chromatography tandem mass spectrometry. We find more than 150 differentially abundant proteins between populations which may contribute to PMPZ isolation. These proteins include a number of proteases and peptidases, and several orthologs of D. melanogaster Sfps, all known to mediate fertilisation success and which mimic PMPZ isolation phenotypes. Males of one population typically produced greater quantities of Sfps and the strongest PMPZ isolation occurs in this direction. The accessory glands and ejaculatory bulb have different functions and the ejaculatory bulb contributes more to population differences than the accessory glands. Proteins with a secretory signal, but not Sfps, evolve faster than non-secretory proteins although the conservative criteria used to define Sfps may have impaired the ability to identify rapidly evolving proteins. We take advantage of quantitative proteomics data from three Drosophila species to determine shared and unique functional enrichments of Sfps that could be subject to selection between taxa and subsequently mediate PMPZ isolation. Our study provides the first high throughput quantitative proteomic evidence showing divergence of reproductive proteins implicated in the emergence of PMPZ isolation between populations.IMPACT SUMMARYIdentifying traits that prevent successful interbreeding is key to understanding early stages of the formation of new species, or speciation. Reproductive isolation arising prior to and during fertilisation frequently involves differences in how the sexes interact. In internally fertilising taxa, such interactions are mediated between the female reproductive tract where fertilisation occurs and the receipt of the ejaculate necessary for fertilisation. Because ejaculate proteins are at least partially responsible for these interactions, differences in male ejaculate protein composition could negatively impact fertilisation success, generating reproductive isolation. While the biological classes of ejaculate proteins are shared across all animal taxa, proteins that are secreted by males tend to show rapid evolution in gene expression and genetic sequence. Thus, reproductive proteins are suggested as prime targets facilitating reproductive isolation that arises after mating but before fertilisation (PostMating PreZygotic or PMPZ isolation). Most research on PMPZ isolation has focussed on differences between species for which it is not possible to determine the causative and temporal order of early speciation processes. Here, we test whether populations that exhibit few genetic differences but show strong PMPZ isolation also exhibit variation in ejaculate composition using quantitative high throughput proteomic analyses. We find a number of proteins are differentially abundant between populations including several known to impact fertilisation success in other species. We show that secreted proteins are evolving at an elevated rate, implicating their potential role in PMPZ isolation. We test divergence in ejaculate composition between species, finding a core set of functions that were conserved across species which last shared a common ancestor more than 40 million years ago along with species-specific investment. This work highlights the divergent evolution of reproductive proteins which may contribute to barriers between populations within a species early during speciation, extendable to similar analyses in other taxa in the future.

scholarly journals Quantitative proteomics identification of seminal fluid proteins in male Drosophila melanogaster

2018 ◽  
Author(s):  
Irem Sepil ◽  
Ben R Hopkins ◽  
Rebecca Dean ◽  
Marie-Laëtitia Thézénas ◽  
Philip D Charles ◽  
...  
Keyword(s):  
Drosophila Melanogaster ◽  
Quantitative Proteomics ◽  
Reproductive Tract ◽  
Seminal Fluid ◽  
High Sensitivity ◽  
Female Reproductive Tract ◽  
Label Free ◽  
Seminal Fluid Proteins ◽  
Copy Numbers ◽  
Before And After

AbstractSeminal fluid contains some of the fastest evolving proteins currently known. These seminal fluid proteins (Sfps) play crucial roles in reproduction, such as supporting sperm function, and – particularly in insects – modifying female physiology and behaviour. Identification of Sfps in small animals is challenging, and often relies on samples taken from the female reproductive tract after mating. A key pitfall of this method is that it might miss Sfps that are of low abundance due to dilution in the female-derived sample or rapid processing in females. Here we present a new and complimentary method, which provides added sensitivity to Sfp identification. We applied label-free quantitative proteomics to Drosophila melanogaster male reproductive tissue – where Sfps are unprocessed, and highly abundant – and quantified Sfps before and immediately after mating, to infer those transferred during copulation. We also analysed female reproductive tracts immediately before and after copulation to confirm the presence and abundance of known and candidate Sfps, where possible. Results were cross-referenced with transcriptomic and sequence databases to improve confidence in Sfp detection. Our data was consistent with 124 previously reported Sfps. We found 8 high-confidence novel candidate Sfps, which were both depleted in mated versus unmated males and identified within the reproductive tract of mated but not virgin females. We also identified 31 more candidates that are likely Sfps based on their abundance, known expression and predicted characteristics, and revealed that four proteins previously identified as Sfps are at best minor contributors to the ejaculate. The estimated copy numbers for our candidate Sfps were lower than for previously identified Sfps, supporting the idea that our technique provides a deeper analysis of the Sfp proteome than previous studies. Our results demonstrate a novel, high-sensitivity approach to the analysis of seminal fluid proteomes, whose application will further our understanding of reproductive biology.

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 Copulation, genital damage and early death in Callosobruchus maculatus

2006 ◽  
Vol 274 (1607) ◽  
pp. 247-252 ◽  
Author(s):  
Paul E Eady ◽  
Leticia Hamilton ◽  
Ruth E Lyons
Keyword(s):  
Reproductive Tract ◽  
Callosobruchus Maculatus ◽  
Seminal Fluid ◽  
Negative Impact ◽  
Early Death ◽  
Female Reproductive Tract ◽  
Mating Frequency ◽  
Trade Off ◽  
Female Longevity ◽  
Fluid Transfer

Antagonistic sexual coevolution stems from the notion that male and female interests over reproduction are in conflict. Such conflicts appear to be particularly obvious when male genital armature inflicts damage to the female reproductive tract resulting in reduced female longevity. However, studies of mating frequency, genital damage and female longevity are difficult to interpret because females not only sustain more genital damage, but also receive more seminal fluid when they engage in multiple copulations. Here, we attempt to disentangle the effects of genital damage and seminal fluid transfer on female longevity in the beetle Callosobruchus maculatus (Coleoptera: Bruchidae). Males copulating for the sixth time in succession inflicted greater levels of genital damage, but transferred smaller ejaculates in comparison with virgin males. The number of copulations performed by males was negatively related to female fecundity and positively related to female longevity, suggesting a trade-off between fecundity and longevity. However, inclusion of fecundity as a covariate revealed sperm and/or seminal fluid transfer to have a negative impact on female longevity above that caused by the fecundity–longevity trade-off. The consequences of multiple copulations on female longevity were examined. Females that mated twice laid more eggs and died sooner than those that mated once. However, incorporation of fecundity as a covariate into our statistical model removed the effect of female mating frequency on female longevity, indicating that double-mated females suffer greater mortality owing to the trade-off between fecundity and longevity. Males of this species are known to transfer very large ejaculates (up to 8% of their body weight), which may represent a significant nutritional benefit to females. However, the receipt of large ejaculates appears to carry costs. Thus, the interpretation of multiple mating experiments on female longevity and associated functional explanations of polyandry in this species are likely to be complex.

scholarly journals Inhibition of reverse transcriptases by seminalplasmin

1983 ◽  
Vol 209 (1) ◽  
pp. 183-188 ◽  
Author(s):  
E S P Reddy ◽  
M R Das ◽  
E P Reddy ◽  
P M Bhargava
Keyword(s):  
Dna Polymerase ◽  
Reproductive Tract ◽  
Seminal Fluid ◽  
Potent Inhibitor ◽  
Female Reproductive Tract ◽  
Dna Polymerase I ◽  
Avian Myeloblastosis Virus ◽  
Antibacterial Protein ◽  
Reverse Transcriptases ◽  
Polymerase I

Seminalplasmin, an antibacterial protein present in bovine seminal plasma, is shown to be a potent inhibitor of reverse transcriptases (RNA-dependent DNA nucleotidyltransferases). Seminalplasmin inhibits RNA-directed, hybrid-directed, and DNA-directed DNA-polymerizing activities of purified reverse transcriptase from avian myeloblastosis virus and from crude viral lysates of several retroviruses by binding to the enzyme, at least in the case of avian myeloblastosis virus. Seminalplasmin does not inhibit significantly DNA synthesis either by Escherichia coli DNA polymerase I, or a mammalian alpha-DNA polymerase. The presence of seminalplasmin in the seminal fluid could provide protection to the male and/or the female reproductive tract against retroviruses.

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.

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