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Haploid selection in animals: investigating the importance of genetic and epigenetic effects in sperm

Final Report Summary - HAPSELA (Haploid selection in animals: investigating the importance of genetic and epigenetic effects in sperm)

An inescapable consequence of sex in eukaryotes is the evolution of a biphasic life cycle with alternating diploid and haploid gametic phases. The focus of the majority of research lies on the processes and mechanisms occurring in the diploid organism. The reason for this is that most animals and flowering plants spend most of their life cycle as diploids, whereas the haploid phase is very short and limited to the moments starting after meiosis to the moment of syngamy in the gametes. However, any processes occurring at the - even short - haploid stages may have fundamental consequences for the subsequent generations. Male gametes in animals (sperm) are produced in large numbers in every ejaculate and only very few and up fertilising an egg. The potential for natural selection on sperm is strong, but largely understudied. Until recently, any sperm showing 'normal' morphology and the ability to fertilise an egg was thought to be equivalent at siring healthy and fit offspring. This ERC funded project aimed to test this idea in more detail and test the importance of selection at the haploid gametic levels in animals.

Sperm within an ejaculate show marked phenotypic and genetic variation but this variation has traditionally been viewed as a trait of the diploid male producing them. The sperm haploid genotype was thought to play no role in determining the sperm phenotype. In a first approach, we performed a series of experiments to establish a possible link between sperm phenotype and offspring fitness using the zebrafish as a study species. We used in vitro fertilisation assays to select for different sperm longevity phenotypes within the ejaculates of males. We then monitored the resulting offspring from early development into late adulthood. We found that offspring sired by longer-lived sperm generally performed better in that they had higher survival, higher lifetime reproductive success and longer lifespan than their siblings sired by shorter-lived sperm.

In a next step, we aimed to establish a possible link between the sperm longevity phenotype and the underlying haploid sperm genotypes. To this end we performed genome and transcriptome sequencing in sperm selected by longevity phenotype and offspring sired by longer- and shorter-lived sperm. We found signals of selection and differentiation across the entire genome in different sperm pools selected by phenotype. In addition, we found a clear signal of divergence and a large number of differentially expressed genes between the sibling offspring sired by shorter- and longer-lived sperm. All in all this provides a clear link between the haploid sperm genotype and its phenotype as well as between sperm phenotype and offspring fitness was established.

In parallel with the above approaches, we tested for the importance of paternal effects allowing for the transfer of non-genetic information on paternal condition into the offspring. We again used the zebrafish and ran a series of experiments. In these experiments, we exposed male zebrafish to several environmental stressors such as social competition and dietary restriction and tested how these affected the males, the sperm quality and the resulting offspring. We found that paternal effects play a major role in determining offspring fitness, and investigated some of the possible underlying mechanisms. We sequenced the small RNA profiles in sperm produced by males exposed to environmental stressors, as well as the offspring. We identified a series of differentially expressed RNAs, many enrolled in transcriptional and translational regulations.

In a final stage, we started investigating the possible role of haploid gametic selection in humans, by running similar in vitro assays in humans as we performed in the zebrafish. Linking sperm longevity phenotypes within a males ejaculate with the underlying haploid sperm genotype as well as with offspring fitness from early development into late life has key implications far beyond the field of evolutionary biology into animal breeding and human fertility and reproduction.