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

Abstract

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.

Age‐dependent plasticity in reproductive investment, regeneration capacity and survival in a partially clonal animal (Hydra oligactis)

“…Regeneration ability in H. oligactis is a highly plastic trait, for example, it is impaired or delayed in sexual individuals (Galliot, Buzgariu, Schenkelaars, & Wenger, 2018; Sebestyén, Barta, & Tökölyi, 2018; Tomczyk et al., 2017). Loss of regeneration in this species may be a consequence of their unique life history within the genus Hydra : they switch from asexual reproduction to sexual reproduction during autumn, in order to produce a relatively high number of sexual organs and resting eggs (compared to other Hydra species: Schuchert, 2010) then the polyps regularly degenerate and die (Schenkelaars et al., 2017; Tökölyi, Ősz, Sebestyén, & Barta, 2017; Yoshida, Fujisawa, Hwang, Ikeo, & Gojobori, 2006).…”

Seasonal variation in sexual readiness in a facultatively sexual freshwater cnidarian with diapausing eggs

“…The median starting day in this group was 63 days after cooling. In the groups exposed for 225 18°C for 4 weeks, 31 out of 37 (84%) in the female strain and 40 out of 47 (85%) in the male strain In natural populations, sexual reproduction in H. oligactis occurs exclusively from late summer to early 239 winter (Welch and Loomis 1924, Reisa 1973, Ribi et al 1985, Sebestyén et al 2018. Sexual 240 reproduction results in the production of resting eggs that can survive the winter which the adults are 241 thought to be less likely to tolerate due to freezing of water bodies and/or reduced food availability 242 (Reisa 1973).…”

“…Sexual reproduction appears to be highly costly to the adults. Polyps that 96 produce gametes have reduced numbers of interstitial stem cells and nematocytes necessary for food 97 capture, they have substantially impaired regeneration capacity, lose their ability to feed and ultimately 98 experience high mortality (Yoshida et al 2006, Sebestyén et al 2018, Tomczyk et al 2020. 99 100 Given these apparent costs of sexual reproduction in H. oligactis, it is perhaps not surprising that not all 101 polyps reproduce sexually even if exposed to the same environmental stimulus.…”

“…99 100 Given these apparent costs of sexual reproduction in H. oligactis, it is perhaps not surprising that not all 101 polyps reproduce sexually even if exposed to the same environmental stimulus. In the wild, only a 102 subset of the population reproduces sexually at any time during the autumn (Welch and Loomis 1924, 103 Ribi et al 1985, Sebestyén et al 2018. Strains derived from the same population and kept under 104 standard conditions in the laboratory differ in their propensity for sex (Tökölyi et al 2017b).…”

“…Furthermore, to see whether differences in sexual readiness between seasons is due to 120 phenotypic plasticity, as predicted by our hypothesis, we performed warm exposure experiments in two 121 lab strains (one male and one female) and looked at changes in sexual readiness in response to 122 exposure to elevated temperature. Hydra (Tökölyi et al 2017a, 2017b, Sebestyén et al 2018. The asexual propagation phase lasted for 10 weeks.…”