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

Immler, Simone; Hotzy, Cosima; Alavioon, Ghazal; Petersson, Erik; Arnqvist, Göran

doi:10.1098/rsbl.2013.1040

Cited by 38 publications

(44 citation statements)

References 28 publications

(49 reference statements)

Supporting

Mentioning

Contrasting

Order By: Relevance

“…S1; see SI Materials and Methods for details), but this difference in fertilization success is unlikely to cause the fitness differences observed between the two treatments for two reasons. First, decreasing fertilization success and resulting potential selection among eggs for sperm did not have any fitness effects on offspring in a similar setup (14). Second, in our outcrosses between experimental fish and wild-type fish, the fertilization success was about 4% higher in the LAT treatment than in the SAT treatment in males (Fig.…”

Section: Significancementioning

confidence: 83%

“…In fact, two recent studies suggested a possible link between sperm phenotype and offspring phenotype: In a broadcast spawning ascidian, Styela plicata, longer-lived sperm sired offspring with higher early-life survival (13), and in the Atlantic salmon, Salmo salar, sperm with intermediate longevity sired faster-hatching offspring (14). However, no published study to date has separated sperm aging from the underlying genetic or epigenetic variation among sib sperm or has provided insights into the long-term fitness effects of variation in sperm phenotypes within a single ejaculate.…”

mentioning

confidence: 99%

See 1 more Smart Citation

Haploid selection within a single ejaculate increases offspring fitness

Alavioon

Hotzy

Nakhro

et al. 2017

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

Self Cite

View full text Add to dashboard Cite

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.

show abstract

Section: Significancementioning

confidence: 83%

mentioning

confidence: 99%

Haploid selection within a single ejaculate increases offspring fitness

Alavioon

Hotzy

Nakhro

et al. 2017

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

Self Cite

View full text Add to dashboard Cite

show abstract

“…In animals, evidence is accumulating of selection based on the haploid genotype of sperm at a number of loci [sperm adhesion molecule Spam1 (44); segregation distortion responder Rsp (45); the t-locus responder Tcr (46); and likely Catsper1, a voltage-gated calcium channel located in the plasma membrane of the sperm tail (47)]. In addition, preliminary evidence in Atlantic salmon (Salmo salar) suggests that variation in sperm phenotype at the intraejaculate level impacts performance in the resulting offspring (48). The efficacy of transcript sharing across the syncytium during postmeiotic sperm maturation has been measured only in a few species, and the extent of haploid expression among sperm deserves further empirical work in a broader array of species.…”

Section: Discussionmentioning

confidence: 99%

Evolution of haploid selection in predominantly diploid organisms

Otto

Scott

Immler

2015

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

Self Cite

View full text Add to dashboard Cite

Diploid organisms manipulate the extent to which their haploid gametes experience selection. Animals typically produce sperm with a diploid complement of most proteins and RNA, limiting selection on the haploid genotype. Plants, however, exhibit extensive expression in pollen, with actively transcribed haploid genomes.Here we analyze models that track the evolution of genes that modify the strength of haploid selection to predict when evolution intensifies and when it dampens the "selective arena" within which male gametes compete for fertilization. Considering deleterious mutations, evolution leads diploid mothers to strengthen selection among haploid sperm/pollen, because this reduces the mutation load inherited by their diploid offspring. If, however, selection acts in opposite directions in haploids and diploids ("ploidally antagonistic selection"), mothers evolve to reduce haploid selection to avoid selectively amplifying alleles harmful to their offspring. Consequently, with maternal control, selection in the haploid phase either is maximized or reaches an intermediate state, depending on the deleterious mutation rate relative to the extent of ploidally antagonistic selection. By contrast, evolution generally leads diploid fathers to mask mutations in their gametes to the maximum extent possible, whenever masking (e.g., through transcript sharing) increases the average fitness of a father's gametes. We discuss the implications of this maternal-paternal conflict over the extent of haploid selection and describe empirical studies needed to refine our understanding of haploid selection among seemingly diploid organisms.pollen competition | antagonistic selection | haploid selection | sperm competition | evolutionary theory

show abstract

“…A similar study in the Atlantic salmon Salmo salar showed effects of sperm longevity on time until hatching (Immler et al. ). More recently, a study in the zebrafish Danio rerio provided strong evidence for the impact of selection at the haploid sperm level on offspring survival and reproductive success and linked sperm phenotype to sperm genotype (Alavioon et al.…”

mentioning

confidence: 80%

Selection for longer lived sperm within ejaculate reduces reproductive ageing in offspring

et al. 2019

Self Cite

View full text Add to dashboard Cite

Males produce numerous sperm in a single ejaculate that greatly outnumber their potential egg targets. Recent studies found that phenotypic and genotypic variation among sperm in a single ejaculate of a male affects the fitness and performance of the resulting offspring. Specifically, within‐ejaculate sperm selection for sperm longevity increased the performance of the resulting offspring in several key life‐history traits in early life. Because increased early‐life reproductive performance often correlates with rapid ageing, it is possible that within‐ejaculate sperm selection increases early‐life fitness at the cost of accelerated senescence. Alternatively, within‐ejaculate sperm selection could improve offspring quality throughout the life cycle, including reduced age‐specific deterioration. We tested the two alternative hypotheses in an experimental setup using zebrafish Danio rerio . We found that within‐ejaculate sperm selection for sperm longevity reduced age‐specific deterioration of fecundity and offspring survival but had no effect on fertilization success in males. Remarkably, we found an opposing effect of within‐ejaculate sperm selection on female fecundity, where selection for sperm longevity resulted in increased early‐life performance followed by a slow decline, while females sired by unselected sperm started low but increased their fecundity with age. Intriguingly, within‐ejaculate sperm selection also reduced the age‐specific decline in fertilization success in females, suggesting that selection for sperm longevity improves at least some aspects of female reproductive ageing. These results demonstrate that within‐ejaculate variation in sperm phenotype contributes to individual variation in animal life histories in the two sexes and may have important implications for assisted fertilization programs in livestock and humans.

show abstract

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

Cited by 38 publications

References 28 publications

Haploid selection within a single ejaculate increases offspring fitness

Haploid selection within a single ejaculate increases offspring fitness

Evolution of haploid selection in predominantly diploid organisms

Selection for longer lived sperm within ejaculate reduces reproductive ageing in offspring

Contact Info

Product

Resources

About