Reproductive mode, stem cells and regeneration in a freshwater cnidarian with postreproductive senescence

In 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 cnidarian Hydra oligactis, both 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 harsh abiotic conditions which neither the parental animals, nor asexual offspring can survive (e.g., freezing). Therefore, when facing unfavourable conditions and increased mortality risk, hydra polyps are expected to show higher level of differentiation of interstitial stem cells into germ cells (i.e., sexual reproduction) than other cell types needed for self‐maintenance or asexual reproduction. Here, by comparing sexually and asexually reproducing individuals to nonreproductives, 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) in H. oligactis polyps from a free‐living Hungarian population prior to the onset of winter. Sexual individuals were characterized by significantly smaller interstitial stem cell pools, fewer nematoblasts involved in food capture and lower regeneration ability compared to nonreproductives, but asexuals did not differ from nonreproductive animals. We also found a negative correlation between germ cell counts and stem cell numbers in males (but not in females). We suggest that the lower numbers of these cell types and lower regenerative ability in sexual individuals reflect a somatic cost of sexual reproduction. Our results 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 postreproductive senescence observed in this species. A plain language summary is available for this article.