Impact Summary One male produces thousands to millions of sperm in a single ejaculate but only very few end up fertilizing an egg. The sperm within an ejaculate vary not only in their shape and performance, but also in the genetic material that each of them carries. The variation among sperm within an ejaculate has long been thought to be of little consequence for the resulting offspring. However, here we show that when we select for the longer lived sperm within the ejaculate of male zebrafish, the resulting offspring is much fitter than their full siblings sired by the shorter lived sperm of the same male. More specifically, offspring sired by longer lived sperm produce more and healthier offspring throughout their life and age at a slower rate. This is a surprising result, which suggests that it is important to understand how sperm selection may contribute to the fitness of the next generations. Our findings not only have important implications for evolutionary biology but potentially beyond into areas that use assisted fertilization technologies.

Sexual reproduction in eukaryotes requires the alteration between a diploid and a haploid phase (Mable and Otto 1998). A large majority of animals spend most of their life as diploid organisms, which alternates with a very short haploid gametic phase. Nevertheless, even a short phase may offer a window for selection to act upon, particularly in male gametes that vary substantially in phenotypes (Holt and Van Look 2004) and genotypes (Wang et al. 2012) and are often exposed to various environmental challenges (Birkhead et al. 1993; Keller and Reeve 1995). However, a long‐standing and common belief holds that selection on mature sperm is of little consequence for the following generation because gene expression is thought to be minimal at the post‐meiotic stages (Eddy 2002). Nevertheless, empirical evidence for gene expression in haploid spermatids is increasing (Fujimoto et al. 1984; Barreau et al. 2008) and the scope for haploid gene expression and hence selection may be more important than assumed so far (Joseph and Kirkpatrick 2004; Immler 2008; Immler and Otto 2018). Even though the haploid phase is rather short in predominantly diploid organisms, selection occurring during the haploid gametic phase may have far reaching consequences for basic evolutionary processes including the rate of adaptation (Orr and Otto 1994), the genetic load (Charlesworth and Charlesworth 1987; Otto et al. 2015), and genetic variation more generally (Immler et al. 2012; Immler and Otto 2018). However, empirical evidence for these effects is still scarce. Selection on longer lived sperm within the ejaculates of a marine ascidian Styela plicata resulted in an increase in hatching success and survival (Crean et al. 2012). A similar study in the Atlantic salmon Salmo salar showed effects of sperm longevity on time until hatching (Immler et al. 2014). 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. 2017). These findings suggest that selection on sperm is likely to have a general impact on offspring fitness and will affect an organism throughout life. In this study, we set out to further test how selection on sperm longevity affects life history traits in male and female offspring.

Previous studies suggest that within‐ejaculate sperm selection on sperm longevity has positive effects on a number of important life‐history traits in the resulting progeny, such as early‐life survival, embryo viability, cell apoptosis, and reproductive fitness of male offspring (Alavioon et al. 2017). Specifically, adult males sired by longer lived sperm produced more and faster swimming sperm, which resulted in a higher fertilization success and more offspring early in life when spawning with control females compared to their male siblings sired by unselected sperm. Because the “disposable soma” theory of ageing (Kirkwood et al. 1979; Kirkwood and Austad 2000) states that ageing results from the resource allocation trade‐offs between investment in reproduction and investment in somatic maintenance, and because increased investment in early‐life fitness can come at the cost of late‐life fitness (Lemaître et al. 2015), it is reasonable to predict that within‐ejaculate sperm selection can contribute to accelerated ageing in both sexes, but especially in males. Sexual selection theory suggests that because male reproductive success is more variable than female reproductive success (Andersson 1994; Bateman 1948), males stand to gain more than females from increased investment in early‐life reproduction to the detriment of their long‐life reproduction and survival (Bonduriansky et al. 2008; Maklakov and Lummaa 2013). Indeed, several studies suggested that increased investment in sperm quality trades off with other costly traits, such as immune response (Simmons 2012), which can have negative implications for survival. For example, one recent study suggested that increased sperm competition led to the evolution of male semelparity in marsupials (Fisher et al. 2013). Such a “live fast, die young” reproductive strategy can result in rapid reproductive ageing in high‐quality males (Hunt et al. 2004; Hooper et al. 2018).

However, the payoffs from strategic investment in early‐life reproduction for males depend on the ecology and the mating system of the species and are far from being universal (Hooper et al. 2018). Therefore, it is also possible that within‐ejaculate sperm selection selects for higher quality offspring of both sexes that will exhibit better reproductive performance throughout their life cycle and will thus not only enjoy increased fitness but also decelerated reproductive ageing. Here, we studied the effect of within‐ejaculate sperm selection on sperm longevity on age‐specific life histories of male and female zebrafish Danio rerio. We were primarily interested in the two following questions: (i) Does within‐ejaculate sperm selection accelerate or decelerate reproductive ageing? (ii) Does within‐ejaculate sperm selection affect male and female offspring differently? In order to address these questions, we investigated the effect of within‐ejaculate sperm selection on sperm longevity on age‐specific fertilization success, embryo survival, and fecundity in the two sexes.