Original ArticlesMortality Patterns Suggest Lack of Senescence in Hydra
Introduction
The potential immortality of hydra has generated close to a hundred years of controversy. However, most studies report only anecdotal information that cannot be used as evidence for (Hertwig 1906; Berninger 1910; Boecker 1914; David 1925) or against (Goetsch 1925; Schlottke 1930; Brien 1953) senescence. The only study in which actual data are presented (Hase 1909) seems to support the presence of senescence in hydra (Martı́nez 1993). However, the general consensus among modern hydra researchers seems to be that hydra lacks aging because it is capable of constant renewal of its body (Brien 1953; Loomis and Lenhoff 1956).
Hydra has a simple body plan. It is essentially a tube with a head at one end and a foot or basal disk at the other. The head consists of two parts: the apical hypostome, or mouth region, surrounded by the tentacle zone from which typically six tentacles emerge. The body wall is composed of two epithelial layers separated by an acellular basement membrane, the mesoglea. Hydra has only about 20 cell types that are organized into three cell lineages: two epithelial and one interstitial. Each lineages consists of a population of stem cells with indefinite self-renewal capacity, and several differentiation products. Interstitial cells reside in the interstices among the epithelial cells. The epithelial cells of the tentacles, the tip of the hypostome, and the foot are nondividing differentiation products of epithelial cells of the body column (Campbell 1965; Campbell 1967a). Neurons, nematocytes, secretory cells, and gametes are differentiation products of interstitial cells.
A striking characteristic of hydra is its tissue dynamics. The epithelial cells of the body column are continuously in the mitotic cycle. This continuous production of epithelial cells in the body column is balanced by a loss of cells: 85% of the epithelial cells are incorporated into developing buds while the rest are sloughed off at the tip of the tentacles, hypostome, and basal disk (Bosch and David 1984). A result of these dynamics is that epithelial cells are constantly displaced either apically onto the head, or basally onto developing buds, or onto the foot.
A consequence of this dynamic behavior is that an individual cell does not exist long in a hydra body. Nondividing differentiated cells of all three lineages are lost by displacement from the body column within 20 days (Campbell 1967b). Dividing stem cells of the interstitial lineage have a cell cycle time of 18–30 h, while stem cells of the epithelial lineages have a cell cycle time of three to four days (David and Campbell 1972). Hence, cells are either constantly renewing by cell division, or they are lost from the animal in a relatively short period of time. This capacity for constant renewal is the main reason behind the claim that hydra is potentially immortal.
Section snippets
Materials and Methods
To test for the presence or absence of senescence in hydra, the mortality patterns of four groups of individuals of Hydra vulgaris were analyzed. A group of 45 animals was collected from Swan Pond, a freshwater lake in Long Island, New York, on December 1991. These individuals (control) were maintained as controls even though their exact ages were unknown. Three cohorts derived from the control group by asexual reproduction were separated on December 1991 (group 1; 50 animals), January 1992
Mortality Rates
Data on mortality were collected for a period of four years. Fig. 1 shows age-specific mortality rates for the three cohorts of hydra and for the control hydra of unknown age. Mortality curves for the marine oligochaete Paranais litoralis, the aeolosomatid annelid Aeolosoma sp., the fruit fly Drosophila melanogaster, the fish Lebistes reticulatus, and the vole Microtus agrestis, have been included for comparison. These species were chosen because they are known to undergo senescence and
Reproductive Rates
The general deterioration of an individual associated with senescence is sometimes, but not always, reflected by a decline in reproduction. All hydra included in these experiments reproduced both sexually and asexually. In hydra, production of eggs or sperm and budding can occur concomitantly, as it was the case for the animals in these experiments. The actual sexual reproductive output of individual hydra could not be estimated because animals remained isolated so no offspring were produced.
Acknowledgements
I thank H. Bode, P. Bode, L. Gee, O. Leontovych, and M. Parkins for help with the experiments; A. Martı́nez for help transporting the animals from Stony Brook to Irvine; J. Becerra, A. Bely, H. Bode, P. Bode, R. Campbell, D. Futuyma, J. Levinton, D. Promislow, L. Slobodkin, and J. Thomson for reading and commenting on earlier versions of the manuscript; and H. Bode and L. Slobodkin for numerous discussions on immortality and hydra. These experiments were carried out in the laboratories of Dr.
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