Reproductive mode, stem cells and regeneration in a freshwater cnidarian with post-reproductive senescence

Abstract

AbstractIn many basal metazoans both somatic and reproductive functions are performed by cellular derivatives of a single multipotent stem cell population. Reproduction can drain these stem cell pools, imposing a physiological cost with subsequent negative effects on somatic maintenance functions. In the freshwater cnidarianHydra oligactisboth asexual (budding) and sexual reproductive modes (production of resting eggs) are present, and both of these are dependent on a common pool of interstitial stem cells. Resting eggs tolerate abiotic conditions which neither the parental animals, nor asexual offspring can survive (e.g. freezing). Therefore, when facing unfavorable conditions and increased mortality risk, hydra polyps are expected to show higher differentiation of interstitial stem cells into germ cells (i.e. sexual reproduction), compared to other cell types needed for selfmaintenance or asexual reproduction. Here, by comparing sexually and asexually reproducing individuals to non-reproductives, we studied the physiological costs of reproduction (size of interstitial stem cell pools, their somatic derivatives and regeneration rate, which is dependent on these cell types) inH. oligactispolyps from a free-living Hungarian population prior to the onset of winter. Sexual individuals (but not asexuals) were characterized by significantly smaller interstitial stem cell pools, fewer somatic derivatives (nematoblasts involved in food capture) and lower regeneration ability compared to non-reproductives. We also found a negative correlation between germ cell counts and stem cell numbers in males (but not in females). These results show that the physiological costs of reproduction are higher for sexual individuals. They also suggest that increased differentiation of stem cells into gametes might limit investment into somatic functions in hydra polyps. Exhaustion of cellular resources (stem cells) could be a major mechanism behind the extreme post-reproductive senescence observed in this species.