Understanding the role of selection at the gametic level in adaptation to changing environments

In a rapidly changing world, the ability to swiftly adapt to varying environmental conditions is key for survival. Understanding how organisms cope and adapt to environmental changes is therefore a burning question. Much of our focus has been directed towards understanding how organisms adapt as juveniles and adults, whereas little to no attention is being paid to the gametic (sperm and egg) stages This is surprising because selection for adaptation during the haploid (one copy of the genome) gametic stages is predicted to be much more efficient and cheaper than selection acting on diploid (two copies of the genome) organisms at any other life stage. This is particularly true in male gametes (sperm), which are produced in vast numbers while only very few fertilise an egg, suggesting strong selective pressure. In addition, sperm within an ejaculate vary in their genetic and non-genetic content and this variation is linked to the sperm phenotype. Finally, in external fertilisers, sperm are exposed to similar environmental conditions as the resulting offspring and hence traits favoured in sperm may also benefit the offspring. Research from our lab provides strong evidence for a direct link between individual sperm performance and offspring survival and reproduction later in life in the zebrafish. We also linked sperm phenotype to its genetic content and by that overthrew a long-standing believe that sperm traits are exclusively dependent on the male genotype, but not its own haploid genetic content

Here we explore the importance of gametic selection for adaptation to changing environmental conditions and to varying temperature in particular. Temperature has seen unprecedented rates of change. The thermal environment may be of particular importance for cold-blooded ectotherms and in externally fertilising species, where gametes are exposed to varying environmental conditions. We will use the externally-fertilising zebrafish to test how variation in temperature affects selection among sperm produced by a single male during fertilisation, and how these effects compare to effects experienced during the diploid embryos or adult fish stages. The zebrafish is ideal because it is an ectotherm with external fertilisation, which allows for powerfully balanced experimental comparisons using in vitro fertilisation under different thermal regimes, and how they translate into offspring performance under different thermal regimes. In addition, the zebrafish has a sequenced genome so it also provides the right genetic tools to look deeper at the underlying mechanism within the genome, epigenome, or expression systems.

At the conclusion of our project, we aim to: a) have measured the impact of selection through the gamete level for offspring fitness, b) have documented the source of genetic variation within the haploid genome or through epigenetic mechanisms, and c) explained whether selection on phenotypic and genetic variation within the haploid sperm stage of life can speed adaptation under rapid environmental change. Our recent discoveries indicate the potential for selection at the gametic level in animals to play a crucial role in rapid response to environmental change. Here, we will combine carefully-designed experiments in an externally fertilising fish system with cutting-edge sequencing technologies, to provide novel insights into the role of gametic selection in adaptation. Our project will have implications not only for the fields of ecology and evolution, but also for applied areas such as livestock breeding, conservation programs, and human health.

The proposed work is expected to generate significant impacts - we describe below who will benefit and the mechanisms in place to show how that impact will be achieved.

1. DISSEMINATION OF FUNDAMENTAL SCIENCE ACROSS ACADEMIC AND PUBLIC DOMAINS: The data and results produced in this project will be made accessible to the scientific community by placing the sequencing data on pblicly-available databanks. Such data will for one be highly informative but also useful for further processing and combination with other existing data. Furthermore the PI, the PDRAs and the CoIs commit themselves to communicate the results widely through published papers, press releases, science blogs, twitter, conference presentations and reports. We see several possibilities for research outcomes to gain the attention of a broad audience:

(i) Sexual reproduction: there are strong potential impacts arising from understanding basic processes involved in reproductive processes and fertility. This impact will be disseminated to researchers in relevant fields such as biologists, clinicians and animal breeders as well as the general public by accessing the respective platforms of dissemination.

(ii) Adaptation: Providing insight into processes involved in adaptation will be of interest to biologists, conservationists and the general public alike due to its immediate timeliness related to the ever growing evidence of the impact of global warming and change in temperature and its impact on organisms around the globe.

(iii) Molecular mechanisms: The role of non-genetic factors in transferring information on paternal condition to the next generation is a field of growing importance and the complexity of the question is undeniable. Providing information on the mechanisms involved will benefit a wide audience from the scientific as well as the public sector.

2. NOVEL METHODS OF FERTILISATION METHODOLOGIES. The role of selection at the gametic level has crucial implications for the application of assisted fertilisation technologies and helps to improve the methods in use in human fertility but also animal breeding. It will be our goal to disseminate to the respective communities to raise the awareness of how methods currently in use could be improved to increase the success rate and quality of the outcome.