Haploid selection within a single ejaculate increases offspring fitness

Abstract

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.

Cryptic haplotype-specific gamete selection yields offspring with optimal MHC immune genes

“…Indeed, a recent study found evidence for haploid selection in zebrafish, presumably based on genetic differences among haploid gametes (Alavioon et al. ). The self‐incompatibility mechanisms in some plants and ascidians, which prevent self‐fertilization, also require expression of the haploid gamete allele (Takayama and Isogai ; Harada and Sawada ), indicating that such fine‐tuned mechanisms have evolved multiple times.…”

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

“…In a previous study, we looked for a trade‐off between sperm swimming speed and sperm longevity, but did not find any (Alavioon et al. ). Whether a trade‐off may be found in any other aspect is currently unclear.…”

“…While increased sperm competition between different males can result in the evolution of trade-offs between sperm quantity and quality versus other traits, such as immune response (Simmons 2012), we currently have no evidence for any trade-off between selection for sperm longevity and offspring fitness with any other trait. In a previous study, we looked for a trade-off between sperm swimming speed and sperm longevity, but did not find any (Alavioon et al 2017). Whether a trade-off may be found in any other aspect is currently unclear.…”

“…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. ). These findings suggest that selection on sperm is likely to have a general impact on offspring fitness and will affect an organism throughout life.…”

Differential sperm motility mediates the sex ratio drive shaping mouse sex chromosome evolution

“…Studying these aspects of the phenotype will require improved methods to separate sperm with differing motility and probe their biochemistry and chromosomal content, with recent advances in microfluidics providing a potential route forward [47]. This work adds to the growing body of experimental and theoretical work demonstrating that even in animal sperm that undergo postmeiotic transcriptional shutdown, haploid selection within a single ejaculate is an important and underappreciated evolutionary force [49][50][51][52][53][54]. Our findings are supported by over two decades' worth of research by multiple groups that have demonstrated the evolutionary consequences of this sex ratio conflict for mouse genome structure and population genetics.…”