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Partitioning sexual selection into its mating success and fertilization success components.

ABSTRACT: Postcopulatory sexual selection due to sperm competition and/or cryptic female choice has been documented in a diversity of taxonomic groups and is considered a pivotal component of sexual selection. Despite this apparent importance, the relative contribution of postcopulatory fertilization success to overall sexual selection has not yet been measured in any species. Here, we used a laboratory-adapted population of the promiscuous fruit fly Drosophila melanogaster to partition the variance in male reproductive success into mating success (a major component of precopulatory sexual selection) and fertilization success (a major component of postcopulatory sexual selection). We found that fertilization success contributed nearly as strongly as mating success to a male's net performance in sexual selection, but that most of this postcopulatory component was attributable to variation in male mating order (the tendency to be the last male to mate a female). After adjusting for mating order, only ?2% of the residual variation in male reproductive success was attributable to differential fertilization success. We found no correlation between male mating success and fertilization success in this system. Unlike natural populations of Drosophila, our laboratory population is adapted to a semelparous lifecycle, so our findings will be most applicable to other promiscuous species with strong sperm precedence and one short breeding period per year or lifetime. In these species, fertilization success may have as much influence on male reproductive success as mating success, but the timing of mating (mating order) may be the predominant factor contributing to variation in fertilization success.

SUBMITTER: Pischedda A

PROVIDER: S-EPMC3277537 | biostudies-literature | 2012 Feb

REPOSITORIES: biostudies-literature

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Partitioning sexual selection into its mating success and fertilization success components.

Pischedda Alison A Rice William R WR

Proceedings of the National Academy of Sciences of the United States of America 20120123 6

Postcopulatory sexual selection due to sperm competition and/or cryptic female choice has been documented in a diversity of taxonomic groups and is considered a pivotal component of sexual selection. Despite this apparent importance, the relative contribution of postcopulatory fertilization success to overall sexual selection has not yet been measured in any species. Here, we used a laboratory-adapted population of the promiscuous fruit fly Drosophila melanogaster to partition the variance in ma ...[more]

PMID: 22308337

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Project description:BackgroundThe determination of genetic variation in sperm competitive ability is fundamental to distinguish between post-copulatory sexual selection models based on good-genes vs compatible genes. The sexy-sperm and the good-sperm hypotheses for the evolution of polyandry require additive (intrinsic) effects of genes influencing sperm competitiveness, whereas the genetic incompatibility hypothesis invokes non-additive genetic effects. A male's sperm competitive ability is typically estimated from his fertilization success, a measure that is dependent on the ability of rival sperm competitors to fertilize the ova. It is well known that fertilization success may be conditional to genotypic interactions among males as well as between males and females. However, the consequences of effects arising from the random sampling of sperm competitors upon the estimation of genetic variance in sperm competitiveness have been overlooked. Here I perform simulations of mating trials performed in the context of sibling analysis to investigate whether the ability to detect additive genetic variance underlying the sperm competitiveness phenotype is hindered by the relative nature of fertilization success measurements.ResultsFertilization success values render biased sperm competitive ability values. Furthermore, asymmetries among males in the errors committed when estimating sperm competitive abilities are likely to exist as long as males exhibit variation in sperm competitiveness. Critically, random effects arising from the relative nature of fertilization success lead to an underestimation of underlying additive genetic variance in sperm competitive ability.ConclusionThe results show that, regardless of the existence of genotypic interactions affecting the output of sperm competition, fertilization success is not a perfect predictor of sperm competitive ability because of the stochasticity of the background used to obtain fertilization success measures. Random effects need to be considered in the debate over the maintenance of genetic variation in sperm competitiveness, and when testing good-genes and compatible-genes processes as explanations of polyandrous behaviour using repeatability/heritability data in sperm competitive ability. These findings support the notion that the genetic incompatibility hypothesis needs to be treated as an alternative hypothesis, rather than a null hypothesis, in studies that fail to detect intrinsic sire effects on the sperm competitiveness phenotype.

Project description:RNA transcripts are distributed non-uniformly in the oocytes of many animals, such that newly-divided embryo cells (blastomeres) inherit distinct transcriptomes following fertilization. In animals such as the frog, Xenopus laevis, programmed transcript regionalization directs early embryonic axis formation and is essential for normal development. However, it is unknown whether such transcriptome asymmetry directs embryogenesis in mammals, or indeed, whether it occurs at all. We here address this by transcript profiling of matching sub-cellular structures and single cells in mouse oocytes and early embryos and analytical strategies exploiting the paired data structure. Spindle samples contained a set of transcripts that was distinguishable from that of the unfertilized metaphase II (mII) oocytes from which each spindle was microsurgically dissected. Immediately following fertilization, cytokinesis produces a 1-cell embryo (zygote) and associated spindle-enriched second polar body (Pb2) whose transcript profiles also differed one from the other, partially reflecting the enrichment of spindle-associated transcripts. Non-uniform transcript distribution within zygotes did not lead to programmed transcriptome asymmetry between the blastomeres of nascent two-cell embryos, or between the second mitotic products of 3-cell embryos. These findings suggest that mammalian oocytes and zygotes exhibit transcript regionalization without subsequent transcriptome asymmetries between respective early mitotic products. This contrasts the situation in Xenopus and places constraints on the ability of maternal transcriptomic prepatterning to prescribe early mammalian development. 16 Zygote vs. Polar body pairs, 10 spindle vs. oocyte pairs, 22 2-cell embryos and 8 3-cell embryos were analysed. Although the raw data are two channel, only the Cy5 signal of each file was analyzed. The Cy5 channel for each gene is normalized to the average Cy5 intensity of the gene across all samples.

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Partitioning sexual selection into its mating success and fertilization success components.

Publications

Partitioning sexual selection into its mating success and fertilization success components.

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