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Copulatory plugs inhibit the reproductive success of rival males.

ABSTRACT: Ejaculated proteins play important roles in reproductive fitness. In many species, seminal fluid coagulates and forms what has been referred to as a copulatory plug in the female's reproductive tract. In mice, previous work demonstrated that knockout males missing a key seminal fluid protein were unable to form a plug and less successful at siring litters in noncompetitive matings (one female, one male), probably the result of reduced sperm transport or insufficient stimulation of the female. Here, we extend these previous studies to competitive matings (one female, two males) and make two key insights. First, when first males were unable to form a plug, they lost almost all paternity to second males to mate. Thus, the copulatory plugs of second males could not rescue the reduced fertility of first males. Second, we showed that the copulatory plug of first males effectively blocked fertilization by second males, even if first males were vasectomized. Taken together, our experiments demonstrated that first males lost almost all paternity if they never formed a plug. We discuss our results in the context of natural populations, where in spite of the strong effects seen here, pregnant female mice regularly carry litters fertilized by more than one male.

SUBMITTER: Mangels R

PROVIDER: S-EPMC5089918 | biostudies-literature | 2016 Nov

REPOSITORIES: biostudies-literature

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Copulatory plugs inhibit the reproductive success of rival males.

Mangels Rachel R Tsung Kathleen K Kwan Kelly K Dean Matthew D MD

Journal of evolutionary biology 20160823 11

Ejaculated proteins play important roles in reproductive fitness. In many species, seminal fluid coagulates and forms what has been referred to as a copulatory plug in the female's reproductive tract. In mice, previous work demonstrated that knockout males missing a key seminal fluid protein were unable to form a plug and less successful at siring litters in noncompetitive matings (one female, one male), probably the result of reduced sperm transport or insufficient stimulation of the female. He ...[more]

PMID: 27488082

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Project description:The start of actual breeding in male social mammals can occur long after individuals attain sexual maturity. Mainly prevented from reproduction by older and dominant males, young males often queue until strong enough to compete for favorable social positions and, in this way, to obtain access to females. However, to what extent maturing males also apply tactics to reproduce before this time is largely unknown. Therefore, the aim of the present study was to elucidate male socio-sexual development from onset of sexual maturity through first mating success until the achievement of a stable social position in a complex social environment. For this purpose, guinea pigs were used as a model system and reproductive success of males living in large mixed-sex colonies was assessed during their first year of life. As a reference, males in a mixed-sex pair situation were examined. Pair-housed males reproduced for the first time around the onset of sexual maturity whereas colony-housed males did so much later in life and with a considerably higher variance. In colonies, reproductive success was significantly affected by dominance status. Dominance itself was age-dependent, with older males having significantly higher dominance ranks than younger males. Surprisingly, both younger and older colony-housed males attained substantial reproductive success of comparable amounts. Thus, younger males reproduced irrespective of queuing and already before reaching a high social status. This mating success of maturing males was most likely achieved via several reproductive tactics which were flexibly applied with the onset of sexual maturity. The period of socio-sexual development before a stable social position is established may, therefore, be a time during which male mammals use flexible behavioral tactics to achieve reproductive success more frequently than commonly is presumed. In addition, the findings strongly indicate that high behavioral plasticity exists well beyond sexual maturity.

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.

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Copulatory plugs inhibit the reproductive success of rival males.

Publications

Copulatory plugs inhibit the reproductive success of rival males.

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