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 both phases has 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 assisted fertilization. It has been a long-standing dogma that, unlike in plants, selection at the haploid gametic level in animals is of no great importance. However, empirical evidence for postmeiotic haploid gene expression is increasing and with the recent recognition of the importance of epigenetic effects for evolutionary mechanisms it is paramount to revisit haploid selection in animals. The aim of the proposed project is to reconsider haploid selection in animals and to investigate the relative importance of genetic and epigenetic effects in sperm for the subsequent generation. The project consists of three logically connected parts, which tackle the question from different angles using the zebrafish Danio rerio as the main model system. In Part I, I will disentangle genetic from epigenetic effects and identify epigenetic effects that affect sperm and offspring performance by combining experimental evolution with next-generation sequencing data. In Part II, I will pinpoint genes that are expressed at the postmeiotic haploid stage of spermatogenesis and determine which of these genes may be under haploid selection. In Part III, I will get to the core of the question and perform single-cell genotyping to explore possible links between sperm phenotype and the underlying sperm genotype. By combining aspects from evolutionary biology, mathematical modeling, genomics and developmental biology this project will advance our understanding of how epigenetic and genetic differences among gametes shape phenotypes and mediate evolutionary change in animals.
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