Resource allocation and post-reproductive degeneration in the freshwater cnidarian Hydra oligactis (Pallas, 1766)

Highlights

• Hydra oligactis undergoes a senescence-like degeneration following sexual reproduction.

• We investigated how food availability affects reproduction and survival in a Hungarian hydra population.

• Reproductive intensity increased with food while survival rate was not affected.

• A substantial proportion of the animals regenerated and reproduced asexually following the sexual phase.

Abstract

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.

Introduction

Cnidarians display one of the simplest but most versatile body organizations within the animal kingdom, characterized by high tissue plasticity and extraordinary regenerative capabilities (Holstein et al., 2003). Perhaps due to these regenerative capabilities, some members of this phylum display very low rates of senescence (Brock and Strehler, 1963, Martı́nez, 1998, Boehm et al., 2013, Schaible et al., 2014, Schaible et al., 2015). In a recent study, for instance, Schaible et al. (2015) have shown that Hydra magnipapillata and Hydra vulgaris maintained constant rates of fertility and mortality in the laboratory over a period of eight years.

Despite their ability to forego senescence, some Hydra species under specific conditions show increasing rates of age-dependent mortality along with a senescence-like degeneration. As first observed by Brien (1953) and later studied by Yoshida et al. (2006), individuals of Hydra oligactis initiate sexual reproduction when the temperature is reduced, after which they die within a few months. Sexual reproduction is followed by a reduction in the number of interstitial stem cells, a decline in the rate of food capture and contractile movements, a decrease in body size and an exponential increase in mortality rate (Yoshida et al., 2006). The reasons why H. oligactis undergoes this senescence-like degeneration are unclear.

According to the disposable soma theory of aging, resources invested into the maintenance of the soma are traded off against investment into reproductive functions (Kirkwood and Rose, 1991). As a consequence, animals with high reproductive investment are expected to show lower levels of self-maintenance and higher levels of aging, a prediction that has received broad support (summarized in Boggs, 2009). Although few systematic studies have been performed on reproductive investment in Hydra species, studies generally report a higher number of reproductive organs (testes and ovaries) in H. oligactis compared to other species (e.g., Schuchert, 2010). This raises the possibility that the post-reproductive degeneration observed in this species might be caused by an increased allocation of resources to reproduction at the expense of self-maintenance functions. Indeed, Reisa (1973) suggested that the “depression” observed in sexually reproducing H. oligactis might be the consequence of interstitial stem cells being converted into germ cells instead of nematocysts, which would prevent feeding throughout the sexual cycle.

If post-reproductive degeneration in hydra is caused by the trade-off between survival and reproduction, then the amount of resources available to the animals is expected to influence investment into these functions, with several possible outcomes. First, animals facing a resource shortage might reduce their reproductive investment to increase survival. In some cases experiencing periods of low food availability results in higher levels of stress tolerance and lower rates of aging, a phenomenon termed dietary restriction (e.g., Masoro and Austad, 1996, Partridge et al., 2005, Walker et al., 2005). However, such an effect does not occur in all species (Nakagawa et al., 2012). Within rotifers, for instance, closely related species may show increased or decreased longevity when exposed to the same food restriction treatment (Kirk, 2001). In hydra there is no evidence so far for dietary restriction-mediated increases in self maintenance levels (Bridge et al., 2010, Tökölyi et al., 2016), although species differ in the way in which oxidative stress tolerance is maintained in the face of reduced food availability (Tökölyi et al., 2016). Secondly, food shortage might signal increased future mortality risk, resulting in higher investment into reproduction and a reduction in survival, a strategy termed “terminal investment” (Clutton-Brock, 1984, Fischer et al., 2009, McNamara et al., 2009). Such a strategy is seen, e.g., in some rotifers (Kirk, 2001, Stelzer, 2001) and birds (Velando et al., 2006), which increase reproductive effort when food availability becomes limited or their immune system is experimentally challenged. Thirdly, in the most simplistic scenario, food shortage may reduce both reproduction and survival at the same time.

To test which of these scenarios, if any, occurs in H. oligactis undergoing post-reproductive degeneration, we individually followed hydra polyps kept at different levels of food supply and measured fecundity and survival as two opposing facets of life history trade-offs. Fecundity was quantified as number of eggs in females, while in males we used the number of testes as a proxy for gamete production. We predicted that fecundity and post-reproductive lifespan would be concomitantly reduced if both functions are valued in the same way, while departure from a parallel reduction would indicate that one of the functions is preserved at the expense of the other, giving rise in the most extreme cases to “dietary restriction” (survival increased and fecundity reduced) or “terminal investment” (fecundity increased and survival reduced) effects.