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 http://onlinelibrary.wiley.com/doi/10.1111/1365-2435.13189/suppinfo is available for this article.

Facultative clonality is associated with complex life cycles where sexual and asexual forms can be exposed to contrasting selection pressures. Facultatively clonal animals often have distinct developmental capabilities that depend on reproductive mode (e.g., negligible senescence and exceptional regeneration ability in asexual individuals, which are lacking in sexual individuals). Understanding how these differences in life history strategies evolved is hampered by limited knowledge of the population structure underlying sexual and asexual forms in nature. Here we studied genetic differentiation of coexisting sexual and asexual Hydra oligactis polyps, a freshwater cnidarian where reproductive mode‐dependent life history patterns are observed. We collected asexual and sexual polyps from 13 Central European water bodies and used restriction‐site associated DNA sequencing to infer population structure. We detected high relatedness among populations and signs that hydras might spread with resting eggs through zoochory. We found no genetic structure with respect to mode of reproduction (asexual vs. sexual). On the other hand, clear evidence was found for phenotypic plasticity in mode of reproduction, as polyps inferred to be clones differed in reproductive mode. Moreover, we detected two cases of apparent sex change (males and females found within the same clonal lineages) in this species with supposedly stable sexes. Our study describes population genetic structure in Hydra for the first time, highlights the role of phenotypic plasticity in generating patterns of life history variation, and contributes to understanding the evolution of reproductive mode‐dependent life history variation in coexisting asexual and sexual forms.

Freshwater hydra are among the few animal groups that show negligible senescence and can maintain high survival and reproduction rates when kept under stable conditions in the laboratory. Yet, one species of Hydra (H. oligactis) undergoes a senescence-like process in which polyps degenerate and die after sexual reproduction. The ultimate factors responsible for this phenomenon are unclear. High mortality in reproducing animals could be the consequence of increased allocation of resources to reproduction at the expense of somatic maintenance. This hypothesis predicts that patterns of reproduction and survival are influenced by resource availability. To test this prediction we investigated survival and reproduction at different levels of food availability in 10 lineages of H. oligactis derived from a single Hungarian population. Sexual reproduction was accompanied by reduced survival, but a substantial proportion of animals regenerated after sexual reproduction and continued reproducing asexually. Polyps belonging to different lineages showed differences in their propensity to initiate sexual reproduction, gonad number and survival rate. Food availability significantly affected fecundity (number of eggs or testes produced), with the largest number of gonads being produced by animals kept on a high food regime. On the other hand, survival rate was not affected by the amount of food. These results show that survival is conserved at the expense of reproduction in this population when food is low. It remains a question still to be answered why survival is prioritized over reproduction in this population.

This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

No abstract