The trade-off between survival and reproduction lies at the core of the evolutionary theory of ageing. Removal of germ cells extends somatic lifespan implying that reduced reproduction frees up resources for survival. Remarkably, however, the disruption of germline signalling increases lifespan without the obligatory reduction in fecundity, thus challenging the key role of the survival-reproduction trade-off. Recent breakthroughs suggest that protection and repair of the genome and the proteome of the germ cells is costly and compromised germline maintenance increases mutation rate, which can reduce offspring fitness. Thus, expensive germline maintenance can be a missing link in the puzzle of cost-free lifespan extension. This hypothesis predicts that when germline signalling is manipulated to increase investment into somatic cells, the germline maintenance will suffer resulting in increased mutation rate and reduced offspring fitness, even if total fecundity is unaffected. I propose a research program at the interface of evolutionary biology and biogerontology that focuses on phenotypic and evolutionary costs of germline maintenance. First, I will genetically manipulate germline signalling to boost investment into soma and estimate mutation rate and competitive fitness of the resulting offspring using Caenorhabditis elegans nematodes. Second, I will employ experimental evolution in nematodes to assess the long-term evolutionary costs of increased germline maintenance. Third, I will use germline transplantation in zebrafish Dario rerio to directly test whether germline proliferation reduces investment into soma in a vertebrate. Understanding how increased investment into the soma damages the germline and reduces offspring fitness will provide a major advance in our understanding of ageing evolution and will have serious implications for applied research programs aimed at harnessing the power of germline signalling to postpone ageing.
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