Sperm competition and sperm cooperation: the potential role of diploid and haploid expression

Immler, Simone

doi:10.1530/rep-07-0482

Cited by 82 publications

(83 citation statements)

References 71 publications

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“…Finally, the postmeiotic transcriptional dynamics suggested by our results further strengthen the notion that haploid gamete gene expression may have important consequences for the evolution of sperm competition and sperm cooperation by generating variation in and among sibling spermatozoa (Parker and Begon 1993;Immler 2008 …”

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confidence: 79%

Direct Evidence for Postmeiotic Transcription During Drosophila melanogaster Spermatogenesis

et al. 2010

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Extensive gene expression during meiosis is a hallmark of spermatogenesis. Although it was generally accepted that RNA transcription ceases during meiosis, recent observations suggest that some transcription occurs in postmeiosis. To further resolve this issue, we provide direct evidence for the de novo transcription of RNA during the postmeiotic phases. These results strengthen the newly emerging notion that postmeiotic transcription is dynamic and integral to the overall process of spermatogenesis. SPERMATOGENESIS is a fundamental developmental process producing male sex cells, the spermatozoa. In Drosophila melanogaster, this process occurs in three phases: a diploid mitotic phase, which increases cell numbers and size; a second, diploid meiotic phase characterized by intense transcriptional activity and important structural changes; and a final postmeiotic haploid phase of sperm morphogenesis and maturation. Early experiments using autoradiography demonstrated RNA transcription during mitosis and early meiosis but no transcriptional activity during postmeiosis (Olivieri and Olivieri 1965). On the basis of this and other similar studies, it has generally been accepted that the postmeiotic phase is devoid of transcriptional activity and led to the prevailing notion that proteins required later during the postmeiotic stages were translated from mRNAs produced during meiosis and stored in the cytoplasm (Schäfer et al. 1995). Two contemporary studies have challenged this view, one using a targeted gene expression approach demonstrating mRNA accumulation in postmeiotic spermatids (Barreau et al. 2008) and our recent microarray analysis estimating substantial genome-wide expression during postmeiosis (Vibranovski et al. 2009). This latter study demonstrated that 20-30% of testis genes transcribed are over expressed during postmeiosis in comparison to meiosis. However, both studies failed to provide clear-cut direct evidence for postmeiotic transcription: both studies measured, either qualitatively or quantitatively, mRNA in postmeiotic cells but did not provide direct evidence for the production of nascent RNA. In addition, in the first study, only a small subset of genes was analyzed and the second study measured bulk mRNA levels from dissected tissues and therefore expression at the cellular level remains unclear. Here, we directly visualized RNA transcripts in intact testes using 5-bromouridine (BrU) and we describe their cellular and subcellular distributions during spermatogenesis (Figure 1).As expected, in intact testis, strong BrU signals were observed in somatic cells of the outer sheath, in presumptive nucleoli of primary spermatocytes ( Figure 1A). We also observed a surprisingly strong BrU signal in developing spermatid bundles during postmeiosis ( Figure 1B). Additionally, BrU incorporation in isolated spermatocytes ( Figure 1C) and in isolated postmeiotic spermatid bundles ( Figure 1D) routinely displayed strong BrU signal near spermatid nuclei. The latter result provides direct evidence for d...

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confidence: 79%

Direct Evidence for Postmeiotic Transcription During Drosophila melanogaster Spermatogenesis

et al. 2010

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“…First, the empirical evidence for haploid gene expression is growing [13,14], suggesting that we may need to re-evaluate the possibility that translation of the haploid set of genes within a sperm affects sperm phenotypes and is correlated with offspring performance [15][16][17]. However, haploid gene expression in animals is highly debated [17].…”

Section: Discussionmentioning

confidence: 99%

Sperm variation within a single ejaculate affects offspring development in Atlantic salmon

et al. 2014

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It is generally believed that variation in sperm phenotype within a single ejaculate has no consequences for offspring performance, because sperm phenotypes are thought not to reflect sperm genotypes. We show that variation in individual sperm function within an ejaculate affects the performance of the resulting offspring in the Atlantic salmon Salmo salar. We experimentally manipulated the time between sperm activation and fertilization in order to select for sperm cohorts differing in longevity within single ejaculates of wild caught male salmon. We found that within-ejaculate variation in sperm longevity significantly affected offspring development and hence time until hatching. Whether these effects have a genetic or epigenetic basis needs to be further evaluated. However, our results provide experimental evidence for transgenerational effects of individual sperm function.

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“…The spermatozoon helps the aggregation to move faster towards the egg (Moore et al 2002). This advantage plays a role when the sperm in the aggregation are related by 50% on average (Immler et al 2007;Immler 2008). From a spatiotemporal viewpoint, formation of a sperm aggregation by sperm of a single male is more probable than formation of mixed sperm aggregations from two or more males.…”

Section: Discussionmentioning

confidence: 99%

Changes in the curvature of sperm apical hooks in murine rodents

et al. 2011

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Sperm apical hooks in murine rodents play an important role in sperm competition. Apical hooks are more curved and longer in species with relatively larger testes, that is in species with a higher risk of sperm competition. The sperm can form aggregations, 'trains', that can move faster than individual sperm, thus reaching the egg earlier as was observed in Apodemus sylvaticus. The apical hook plays an important role for train formation. This study focuses on the changes in the curvature of sperm apical hooks during the final stages of spermiogenesis and stages before fertilization (sperm-life span). Apical hook curvatures of field mice (A. agrarius and A. sylvaticus) vary significantly between dormant and active sperm. In contrast, there are no significant differences among the stages in the eastern house mouse. Since there are high ranges of angle values in all stages, the mean angles of apical hook curvature are not appropriate for evaluating risk of sperm competiton. The ranges of angle values point to a level of flexibility of the apical hooks. The lengths of sperm hooks in individual species do not change during particular stages. The length and flexibility of the sperm apical hooks are important for the formation of sperm aggregations, thus these sperm characters indicate the risk of sperm competition and the sperm strategies in murine rodents.

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Sperm competition and sperm cooperation: the potential role of diploid and haploid expression

Cited by 82 publications

References 71 publications

Direct Evidence for Postmeiotic Transcription During Drosophila melanogaster Spermatogenesis

Direct Evidence for Postmeiotic Transcription During Drosophila melanogaster Spermatogenesis

Sperm variation within a single ejaculate affects offspring development in Atlantic salmon

Changes in the curvature of sperm apical hooks in murine rodents

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