Resource allocation and post-reproductive degeneration in the freshwater cnidarian Hydra oligactis (Pallas, 1766)
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.
Section snippets
Animals and culture conditions
Animals for the present study were derived from ten polyps collected from an oxbow lake of the Tisza river near Tiszadorogma, Hungary (47.67N, 20.86E; Fig. 1) in May 2015. We collected animals that were at least 2 m apart to increase the chance that both males and females were found and to reduce the chance that multiple asexual members of the same genetic clone were collected. Species identity was determined based on morphological traits and investigation of nematocysts (under 400×
Results
The pattern of asexual and sexual reproduction and survival changed over the course of the experiment as shown in Fig. 2. Lowering the temperature inhibited budding for approximately two weeks; then animals produced buds again for two weeks, which was followed by initiation of sexual reproduction. Of the ten clones five were found to be males and five to be females. The number of days elapsed from the start of the temperature manipulation to the initiation of sexual reproduction was 38 ± 3.91
Discussion
In the present study we investigated the fecundity/survival trade-off at different food levels in male and female H. oligactis undergoing sexual reproduction. We found that polyps initiated gonadogenesis irrespective of food availability, but the number of gonads (testes or detached eggs) increased with increasing food availability. Following sexual reproduction there was high mortality (>30% of the initial cohort died during the course of the experiment), but the survival rate was not related
Acknowledgements
We are grateful to Csongor Freytag for his help in photographing hydra. Three anonymous reviewers provided comments that substantially improved the manuscript. We thank Renate Schilling for improving the English in this paper. This study was supported by the National Talent Program (NTP-EFÖ-P-15), by the Human Capacities Grant Management Office and the Hungarian Ministry of Human Capacities. J.T. was supported by the János Bolyai Research Scholarship of the Hungarian Academy of Sciences.
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