Can paternal effects via seminal fluid contribute to the evolution of polyandry?
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ABSTRACT:
SUBMITTER: Simmons LW
PROVIDER: S-EPMC7728675 | biostudies-literature |
REPOSITORIES: biostudies-literature
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Project description:Mounting evidence suggests that nongenetic paternal effects on offspring may be widespread among animal taxa, but the mechanisms underlying this form of nongenetic inheritance are not yet fully understood. Here, we show that seminal fluids underlie paternal effects on early offspring survival in an insect, the cricket Teleogryllus oceanicus, and quantify the contribution of this paternal effect to the inheritance of this important fitness trait. We used castrated males within a full-sib half-sib experimental design to show that seminal fluid donors were responsible for variation in the survival of developing embryos to hatching, and in their subsequent survival to adulthood. Increased expression of two seminal fluid protein genes, previously found to be positively associated with sperm quality, was found to be negatively associated with embryo survival. These nongenetic paternal effects hold important implications for the evolution of adaptive maternal responses to sperm competition, and more broadly for the interpretation of sire effects from classic quantitative genetic breeding designs.
| S-EPMC6675144 | biostudies-other
Project description:Paternal characteristics and exposures influence physiology and disease risks in progeny, but the mechanisms are mostly unknown. Seminal fluid, which affects female reproductive tract gene expression as well as sperm survival and integrity, provides one potential pathway. We evaluated in mice the consequences for offspring of ablating the plasma fraction of seminal fluid by surgical excision of the seminal vesicle gland. Conception was substantially impaired and, when pregnancy did occur, placental hypertrophy was evident in late gestation. After birth, the growth trajectory and metabolic parameters of progeny were altered, most profoundly in males, which exhibited obesity, distorted metabolic hormones, reduced glucose tolerance, and hypertension. Altered offspring phenotype was partly attributable to sperm damage and partly to an effect of seminal fluid deficiency on the female tract, because increased adiposity was also evident in adult male progeny when normal two-cell embryos were transferred to females mated with seminal vesicle-excised males. Moreover, embryos developed in female tracts not exposed to seminal plasma were abnormal from the early cleavage stages, but culture in vitro partly alleviated this. Absence of seminal plasma was accompanied by down-regulation of the embryotrophic factors Lif, Csf2, Il6, and Egf and up-regulation of the apoptosis-inducing factor Trail in the oviduct. These findings show that paternal seminal fluid composition affects the growth and health of male offspring, and reveal that its impact on the periconception environment involves not only sperm protection but also indirect effects on preimplantation embryos via oviduct expression of embryotrophic cytokines.
| S-EPMC3926084 | biostudies-literature
Project description:Seminal fluid proteins (SFPs) are a group of reproductive proteins that are among the most evolutionarily divergent known. As SFPs can impact male and female fitness, these proteins have been proposed to evolve under postcopulatory sexual selection (PCSS). However, the fast change of the SFPs can also result from nonadaptive evolution, and the extent to which selective constraints prevent SFPs rapid evolution remains unknown. Using intra- and interspecific sequence information, along with genomics and functional data, we examine the molecular evolution of approximately 300 SFPs in Drosophila. We found that 50-57% of the SFP genes, depending on the population examined, are evolving under relaxed selection. Only 7-12% showed evidence of positive selection, with no evidence supporting other forms of PCSS, and 35-37% of the SFP genes were selectively constrained. Further, despite associations of positive selection with gene location on the X chromosome and protease activity, the analysis of additional genomic and functional features revealed their lack of influence on SFPs evolving under positive selection. Our results highlight a lack of sufficient evidence to claim that most SFPs are driven to evolve rapidly by PCSS while identifying genomic and functional attributes that influence different modes of SFPs evolution.
| S-EPMC8457112 | biostudies-literature
Project description:As a class, seminal fluid proteins are expected to exert strong effects on mating partners due to the selection pressures of sperm competition and sexual conflict. But because of the complexity of this secretion, linking specific proteins to downstream effects on own fitness-via manipulating the reproductive behavior, physiology, and ultimately the sperm utilization of mating partners-is not straightforward. Here, we adopted a systematic gene knockdown approach to screen for seminal fluid-mediated fitness effects in the simultaneously hermaphroditic flatworm Macrostomum lignano. We focused on 18 transcripts in M. lignano seminal fluid, testing how their RNA interference-induced knockdown impacted on three aspects of donor (male) reproductive success: (a) fertility (offspring production of the partner); (b) defensive sperm competitive ability, P 1; and (c) offensive sperm competitive ability, P 2. In general, the knockdown of most individual transcripts appeared to have only a minor impact on male reproductive success, though we found evidence that the knockdown of up to five different transcripts impacted on fertility; the knockdown of two other transcripts resulted in reduced P 2; and knockdown of a further transcript actually increased P 2. We thus identify a number of candidate seminal fluid transcripts that appear to modulate offspring production and sperm competitiveness in M. lignano. That only a minority of transcripts exhibit such a pattern likely reflects both the difficulty of accurately estimating sperm competitiveness and the functional redundancy of seminal fluid.
| S-EPMC6953679 | biostudies-literature
Project description:Highly precise, yet flexible and responsive coordination of expression across groups of genes underpins the integrity of many vital functions. However, our understanding of gene regulatory networks (GRNs) is often hampered by the lack of experimentally tractable systems, by significant computational challenges derived from the large number of genes involved or from difficulties in the accurate identification and characterization of gene interactions. Here we used a tractable experimental system in which to study GRNs: the genes encoding the seminal fluid proteins that are transferred along with sperm (the 'transferome') in Drosophila melanogaster fruit flies. The products of transferome genes are core determinants of reproductive success and, to date, only transcription factors have been implicated in the modulation of their expression. Hence, as yet, we know nothing about the post-transcriptional mechanisms underlying the tight, responsive and precise regulation of this important gene set. We investigated this omission in the current study. We first used bioinformatics to identify potential regulatory motifs that linked the transferome genes in a putative interaction network. This predicted the presence of putative microRNA (miRNA) 'hubs'. We then tested this prediction, that post-transcriptional regulation is important for the control of transferome genes, by knocking down miRNA expression in adult males. This abolished the ability of males to respond adaptively to the threat of sexual competition, indicating a regulatory role for miRNAs in the regulation of transferome function. Further bioinformatics analysis then identified candidate miRNAs as putative regulatory hubs and evidence for variation in the strength of miRNA regulation across the transferome gene set. The results revealed regulatory mechanisms that can underpin robust, precise and flexible regulation of multiple fitness-related genes. They also help to explain how males can adaptively modulate ejaculate composition.
| S-EPMC6170815 | biostudies-literature
Project description:BackgroundPolyandry is a common mating strategy in animals, increasing female fitness through direct (material) and indirect (genetic) benefits. Most theories about the benefits of polyandry come from studies of terrestrial animals, which have relatively complex mating systems and behaviors; less is known about the potential benefits of polyandry in sessile marine animals, for which potential mates may be scarce and females have less control over pre-copulatory mate choice. Here, we used microsatellite markers to examine multiple paternity in natural aggregations of the Pacific gooseneck barnacle Pollicipes elegans, testing the effect of density on paternity and mate relatedness on male reproductive success.ResultsWe found that multiple paternity was very common (79% of broods), with up to five fathers contributing to a brood, though power was relatively low to detect more than four fathers. Density had a significant and positive linear effect on the number of fathers siring a brood, though this relationship leveled off at high numbers of fathers, which may reflect a lack of power and/or an upper limit to polyandry in this species. Significant skew in male reproductive contribution in multiply-sired broods was observed and we found a positive and significant relationship between the proportion of offspring sired and the genetic similarity between mates, suggesting that genetic compatibility may influence reproductive success in this species.ConclusionsTo our knowledge, this is the first study to show high levels of multiple paternity in a barnacle, and overall, patterns of paternity in P. elegans appear to be driven primarily by mate availability. Evidence of paternity bias for males with higher relatedness suggests some form of post-copulatory sexual selection is taking place, but more work is needed to determine whether it operates during or post-fertilization. Overall, our results suggest that while polyandry in P. elegans is driven by mate availability, it may also provide a mechanism for females to ensure fertilization by compatible gametes and increase reproductive success in this sessile species.
| S-EPMC4021092 | biostudies-literature
Project description:Over the last decades, the field of sexual selection underwent a paradigm shift from sexual-stereotype thinking of "eager" males and "coy" females towards a more nuanced perspective acknowledging that not only males but also females can benefit from multiple mating and compete for mating partners. Yet, sexual selection in females is still considered a peculiarity, and the evolution of polyandry is often viewed to result from a higher mating interest of males. Here, we present meta-analytic evidence from 77 species across a broad range of animal taxa to demonstrate that female reproductive success is overall positively correlated with mating success, suggesting that females typically benefit from multiple mating. Importantly, we found that these fitness gains likely promote the evolution of polyandry. Our findings offer support for the idea that sexual selection is widespread in females and to play a key role for the evolution of animal mating systems. Thereby, our results extend our understanding of the evolutionary consequences of sexual reproduction and contribute to a more balanced view of how sexual selection operates in males and females.
| S-EPMC9831318 | biostudies-literature
Project description:Paternal life experiences impact offspring health via germline, and epigenetic inheritance provides a potential mechanism. However, global reprogramming during offspring embryogenesis and gametogenesis represents the largest hurdle to conceptualize it. Yet, detailed characterization of how sperm epigenetic alterations carrying "environmental memory" can evade offspring embryonic reprogramming remains elusive. Here, mice exposed to long-term restraint stress were employed to study the mechanisms underlying inter- and transgenerational effects of paternal exposure to a long-term psychological stress. We found that stress could induce paternal inheritance of reproductive, behavioral, and metabolic disorders. Bisulfite methylation profiling of 18 sperm and 12 embryo samples of three consecutive generations identified inter- and transgenerational inheritance of paternal Differential DNA Methylation Regions (DMRs) at frequencies ~11.36% and 0.48%, respectively. These DMRs related to genes with functional implications for psychological stress response, and tissue inheritance of these DMRs passed paternal disorders epigenetically to offspring. More importantly, these DMRs evaded offspring embryonic reprogramming through erasure and subsequent reestablishment, but not via un-erasure way. Nonetheless, their reestablishment proportions in the primitive streak (E7.5) stage were altered. Furthermore, sncRNA-seq revealed that stress-induced tsRNA, miRNA and rsRNA dysregulation in paternal sperm might play important roles in DMRs occurrence and paternal inheritance. These finding implied that sperm epigenetic alterations contribute to inter- and transgenerational effects of paternal exposure to long-term psychological stress, and highlighted the possible underlying molecular mechanism.
| S-EPMC8553786 | biostudies-literature
Project description:In most animal species, males and females communicate during sexual behavior to negotiate reproductive investments. Pre-copulatory courtship may settle if copulation takes place, but often information exchange and decision-making continue beyond that point. Here, we show that female Drosophila sing by wing vibration in copula. This copulation song is distinct from male courtship song and requires neurons expressing the female sex determination factor DoublesexF. Copulation song depends on transfer of seminal fluid components of the male accessory gland. Hearing female copulation song increases the reproductive success of a male when he is challenged by competition, suggesting that auditory cues from the female modulate male ejaculate allocation. Our findings reveal an unexpected fine-tuning of reproductive decisions during a multimodal copulatory dialog. The discovery of a female-specific acoustic behavior sheds new light on Drosophila mating, sexual dimorphisms of neuronal circuits and the impact of seminal fluid molecules on nervous system and behavior.
| S-EPMC7080721 | biostudies-literature
Project description:Postcopulatory sexual selection can select for sperm allocation strategies in males [1, 2], but males should also strategically allocate nonsperm components of the ejaculate [3, 4], such as seminal fluid proteins (Sfps). Sfps can influence the extent of postcopulatory sexual selection [5-7], but little is known of the causes or consequences of quantitative variation in Sfp production and transfer. Using Drosophila melanogaster, we demonstrate that Sfps are strategically allocated to females in response to the potential level of sperm competition. We also show that males who can produce and transfer larger quantities of specific Sfps have a significant competitive advantage. When males were exposed to a competitor male, matings were longer and more of two key Sfps, sex peptide [8] and ovulin [9], were transferred, indicating strategic allocation of Sfps. Males selected for large accessory glands (a major site of Sfp synthesis) produced and transferred significantly more sex peptide, but not more ovulin. Males with large accessory glands also had significantly increased competitive reproductive success. Our results show that quantitative variation in specific Sfps is likely to play an important role in postcopulatory sexual selection and that investment in Sfp production is essential for male fitness in a competitive environment.
| S-EPMC2737339 | biostudies-literature