Trade-off between somatic and germline repair in a vertebrate supports the expensive germ line hypothesis

Significance “How can we stop aging?” is still a largely unanswered question. Understanding the possible mechanisms that lead to the gradual deterioration of the organism over time is key to answer this question and finding possible antidotes. A central tenet of the evolutionary theory of aging is the possible trade-off between the maintenance of the immortal germ line and the disposable soma. Male vertebrates continue somatic and germline proliferation throughout life, offering an ideal opportunity to study this hypothesis. We show that in male zebrafish exposed to stressful conditions, the experimental removal of the germ line improves somatic recovery. Our results provide direct evidence for the cost of the germ line in a vertebrate.
The disposable soma theory is a central tenet of the biology of aging where germline immortality comes at the cost of an aging soma [T. B. L. Kirkwood, Nature 270, 301–304 (1977); T. B. L. Kirkwood, Proc. R. Soc. Lond. B Biol. Sci. 205, 531–546 (1979); T. B. L. Kirkwood, S. N. Austad, Nature 408, 233–238 (2000)]. Limited resources and a possible trade-off between the repair and maintenance of the germ cells and growth and maintenance of the soma may explain the deterioration of the soma over time. Here we show that germline removal allows accelerated somatic healing under stress. We tested “the expensive germ line” hypothesis by generating germline-free zebrafish Danio rerio and testing the effect of the presence and absence of the germ line on somatic repair under benign and stressful conditions. We exposed male fish to sublethal low-dose ionizing radiation, a genotoxic stress affecting the soma and the germ line, and tested how fast the soma recovered following partial fin ablation. We found that somatic recovery from ablation occurred substantially faster in irradiated germline-free fish than in the control germline-carrying fish where somatic recovery was stunned. The germ line did show signs of postirradiation recovery in germline-carrying fish in several traits related to offspring number and fitness. These results support the theoretical conjecture that germline maintenance is costly and directly trades off with somatic maintenance.