Sexual rest and post‐meiotic sperm ageing in house mice

Firman, Renée C.; Young, Fiona; Rowe, D. E.; Duong, Hang; Gasparini, Clelia

doi:10.1111/jeb.12661

Cited by 21 publications

(21 citation statements)

References 71 publications

(95 reference statements)

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“…; but see Firman et al. ). We interpret this finding as a fertilization bias, rather than a bias attributable to variance in embryo viability, as we found no significant effect of sperm age on offspring production (i.e., our fecundity measure) in the noncompetitive fertilization trials.…”

Section: Discussionmentioning

confidence: 98%

Sperm storage by males causes changes in sperm phenotype and influences the reproductive fitness of males and their sons

2017

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Recent studies suggest that environmentally induced effects on sperm phenotype can influence offspring phenotype beyond the classic Mendelian inheritance mechanism. However, establishing whether such effects are conveyed purely through ejaculates, independently of maternal environmental effects, remains a significant challenge. Here, we assess whether environmentally induced effects on sperm phenotype affects male reproductive success and offspring fitness. We experimentally manipulated the duration of sperm storage by males, and thus sperm age, in the internally fertilizing fish Poecilia reticulata. We first confirm that sperm ageing influences sperm quality and consequently males reproductive success. Specifically, we show that aged sperm exhibit impaired velocity and are competitively inferior to fresh sperm when ejaculates compete to fertilize eggs. We then used homospermic (noncompetitive) artificial insemination to inseminate females with old or fresh sperm and found that male offspring arising from fertilizations by experimentally aged sperm suffered consistently impaired sperm quality when just sexually mature (four months old) and subsequently as adults (13 months old). Although we have yet to determine whether these effects have a genetic or epigenetic basis, our analyses provide evidence that environmentally induced variation in sperm phenotype constitutes an important source of variation in male reproductive fitness that has far reaching implications for offspring fitness. K E Y W O R D S :Epigenetics, male sperm storage, paternal effects, sperm ageing, sperm competition, sperm velocity. Impact SummaryProlonged sperm storage is associated with a reduction in sperm quality in many species, including humans. Such effects have potentially important implications for a male's reproductive fitness because males that store sperm for prolonged periods (e.g., because they become isolated from females, or fail to secure mates) may suffer compromised fertility, or reduced fertilization success when their sperm compete with rival (fresher) sperm during sperm competition. However, in addition to such direct costs associated with male sperm storage, recent studies have suggested a link between environmentally induced changes in sperm quality and offspring traits. Sperm ageing therefore constitutes a potentially widespread source of nongenetic (i.e., not linked to genes) variance in offspring fitness. Here, using the live-bearing guppy (Poecilia reticulata), we provide experimental support for these ideas, showing that sperm storage has far reaching implications for male reproductive fitness. First, we show that males whose sperm were held longer inside their reproductive organs fertilize relatively fewer eggs when in competition with those from males who produced fresher sperm. Second, we provide empirical evidence that the reduction in sperm quality caused by long-term sperm storage has effects that transcend generations by influencing the reproductive fitness of adult offspring; offspring sired by males with age...

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Section: Discussionmentioning

confidence: 98%

Sperm storage by males causes changes in sperm phenotype and influences the reproductive fitness of males and their sons

2017

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“…A second sperm sample was taken the day after, and a third sperm sample after 4 days of being sexually rested. This procedure ensured that any differences in sperm characteristics would be intrinsic differences in quality rather than differences due to depletion [8] or fresh sperm effects [41–43] (but see [44]), and only data collected after all males were manually depleted was used. For logistic reasons, males were divided in three sampling batches consisting of 5 aviaries, and all three batches were processed 5 days apart.…”

Section: Methodsmentioning

confidence: 99%

Antioxidant allocation modulates sperm quality across changing social environments

et al. 2017

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In promiscuous species, male reproductive success depends on their ability to mate with fertile females and on the fertilizing ability of their sperm. In such species, theory predicts that, owing to a trade-off between pre- and post-copulatory reproductive traits, males with lesser access to females should increase resource investment into those sperm traits that enhance fertilization success–usually referred to as ejaculate quality. This prediction has been validated in several taxa, yet studies on the physiological mechanisms modulating ejaculate quality are lacking. Sperm cells are highly vulnerable to oxidative stress, which impairs male fertility. Therefore, males that better protect their sperm from oxidative stress are expected to achieve higher ejaculate quality. Based on theoretical expectations, and since social dominance is a major determinant of mating opportunity, we predicted that subordinate males should invest more into the antioxidant protection of their sperm in order to achieve higher ejaculate quality. We maintained 60 male and 60 female wild-caught house sparrows Passer domesticus in outdoor aviaries, where we experimentally manipulated male social status to test our predictions. We measured cellular oxidative stress and enzymatic antioxidant activity in blood and sperm both before and after manipulating social ranks. Before manipulating the social status, we found that ejaculate viability correlated with oxidative stress level in sperm, with dominant males producing more oxidized and less viable ejaculates. Further, males at the lower end of the hierarchy produced ejaculates of similar quality to those of dominant males, suggesting that restricted access to resources might limit male reproductive strategies. After experimentally manipulating the social status, males matched their ejaculate quality to their new rank, while increases in antioxidant investment into ejaculates paralleled increases in ejaculate viability. Oxidative stress has been proposed as a general constraint to the evolution of life histories. Our results highlight oxidative stress and strategic antioxidant allocation as important proximate physiological mechanisms underlying male reproductive strategies.

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“…We found no evidence that the subsample identity and hence preejaculation sperm age had any differential effect on offspring viability (subset effect: χ 2 1 = 0.063, P = 0.97). In many animals, males continuously release unused sperm, apparently to avoid preejaculation sperm aging (22)(23)(24), and this continuous release may explain the lack of an effect.…”

Section: Significancementioning

confidence: 99%

Haploid selection within a single ejaculate increases offspring fitness

Alavioon

Hotzy

Nakhro

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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An inescapable consequence of sex in eukaryotes is the evolution of a biphasic life cycle with alternating diploid and haploid phases. The occurrence of selection during the haploid phase can have farreaching consequences for fundamental evolutionary processes including the rate of adaptation, the extent of inbreeding depression, and the load of deleterious mutations, as well as for applied research into fertilization technology. Although haploid selection is well established in plants, current dogma assumes that in animals, intact fertile sperm within a single ejaculate are equivalent at siring viable offspring. Using the zebrafish Danio rerio, we show that selection on phenotypic variation among intact fertile sperm within an ejaculate affects offspring fitness. Longer-lived sperm sired embryos with increased survival and a reduced number of apoptotic cells, and adult male offspring exhibited higher fitness. The effect on embryo viability was carried over into the second generation without further selection and was equally strong in both sexes. Sperm pools selected by motile phenotypes differed genetically at numerous sites throughout the genome. Our findings clearly link within-ejaculate variation in sperm phenotype to offspring fitness and sperm genotype in a vertebrate and have major implications for adaptive evolution.

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Sexual rest and post‐meiotic sperm ageing in house mice

Cited by 21 publications

References 71 publications

Sperm storage by males causes changes in sperm phenotype and influences the reproductive fitness of males and their sons

Sperm storage by males causes changes in sperm phenotype and influences the reproductive fitness of males and their sons

Antioxidant allocation modulates sperm quality across changing social environments

Haploid selection within a single ejaculate increases offspring fitness

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