![]() In experiment 1A, we measured sperm longevity for every male and calculated the time until 50% of sperm were no longer motile. Using the split design described above, we performed IVF and measured fitness traits of the resulting offspring from early development to adulthood. Our first aim was to describe any association between variation in sperm longevity and offspring fitness and to estimate its importance (experiment 1 A and B). To avoid any effect of egg aging, eggs were used within 1 min after collection, and previously activated sperm from both treatments were added to each of the two egg clutches at the same moment. So that the fertilization opportunity was equal in the two treatments, we doubled the amount of sperm present in the LAT treatment to compensate for the nonmotile sperm ( SI Materials and Methods for more details). Thus, the LAT treatment directly selected against short-lived sperm. In the “long activation time” (LAT) treatment, the sperm in the other cohort were held until about 50% were no longer motile, and then the sperm were added to the second egg cohort. Sperm were activated with water then, in the “short activation time” (SAT) treatment, one of the sperm cohorts was immediately added to one of the egg cohorts. We divided the ejaculate of a male and the eggs of a female into two cohorts each and exposed each sperm cohort to one of two treatments. Selection on sperm longevity was performed by experimentally manipulating the timing between sperm activation and fertilization. Zebrafish gametes activate upon contact with water, and IVF allows precise control over the activation and fertilization of gametes as well as gamete numbers. We used the externally fertilizing zebrafish Danio rerio for a series of experiments using in vitro fertilizations (IVF) in which we selected on sperm phenotypes based on their longevity. ![]() Here we demonstrate that different cohorts of sperm phenotypes and genotypes, which exhibit varying levels of longevity and differentially affect offspring fitness, coexist within the ejaculate of a single male. Furthermore, the lack of perfect symmetry in sharing of transcripts among haploid cells suggests that phenotypic variation within an ejaculate may have a genetic or epigenetic basis and hence be under selection ( 11, 12). Nevertheless, some empirical evidence shows that genes may be expressed at the haploid stages of spermatogenesis and that the transcripts of these genes are not always perfectly shared through cytoplasmic bridges among haploid spermatids ( 9, 10). The key reason for this lack of knowledge is the current assumption that performance of sperm produced by a male is under diploid control ( 4– 6), a notion that is further supported by the apparent lack of association between the phenotypic variation among sib sperm and their genetic content ( 7, 8). Sperm within an ejaculate exhibit remarkable phenotypic variation ( 1), but little is known about the causes and consequences of such variation and selection among sperm produced by one male. 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. Sperm pools selected by motile phenotypes differed genetically at numerous sites throughout the genome. ![]() The effect on embryo viability was carried over into the second generation without further selection and was equally strong in both sexes. Longer-lived sperm sired embryos with increased survival and a reduced number of apoptotic cells, and adult male offspring exhibited higher fitness. Using the zebrafish Danio rerio, we show that selection on phenotypic variation among intact fertile sperm within an ejaculate affects offspring fitness. 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. ![]() The occurrence of selection during the haploid phase can have far-reaching 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. An inescapable consequence of sex in eukaryotes is the evolution of a biphasic life cycle with alternating diploid and haploid phases.
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