0044-5231/01/240/03–04-409 $ 15.00/0
The Nature of Selection on Anhydrobiotic Capacity
in Tardigrades
*
K. Ingemar JÖNSSON
Department of Theoretical Ecology, Lund University, Lund, Sweden
Abstract. Tardigrades are well known for their capacity to enter an anhydrobiotic state, and remain ametabolic for
several years. Yet the evolutionary background, and the forces of natural selection that act on anhydrobiotic capac-
ity have remained unexplored. In this paper, I review the basic problem of anhydrobiosis and the phenotypic traits
that may be the main targets of natural selection for improved anhydrobiotic capacity. I also make an attempt to
put anhydrobiosis into a life history perspective, and discuss this life form in the perspective of energetic and
genetic constraints.
Key words. Tardigrada, anhydrobiosis, cryptobiosis, natural selection, adaptation.
1. INTRODUCTION
The ability of some micrometazoan taxa (Rotifera,
Nematoda, Tardigrada) to undergo repeated periods of
desiccation, in which the organism loses most or all of
its water with a dramatically reduced metabolism as a
consequence, has been known for 300 years (KEILIN
1959). While desiccation tolerance during embryonic
stages is found in other animal taxa, rotifers, nema-
todes and tardigrades show this ability at all life history
stages. SPALLANZANI (1776) was apparently the first to
study anhydrobiosis in tardigrades, and his experi-
ments were followed up by several others during the
19
th
century, in particular by DOYÈRE (1842) and F. A.
POUCHET (see BROCA 1860). In the early part of the 20
th
century, numerous experimental studies were done by
RAHM (1923, 1926) and BAUMANN (1922), with much
focus on the question whether organisms in anhydro-
biosis should be considered as dead (i.e. ametabolic) or
alive (i.e. with maintained metabolism). PIGON &
WEGLARSKA (1953) attempted to resolve this long-
standing controversy by directly measuring the respira-
tion of anhydrobiotic tardigrades, and documented a
very low rate of oxygen turnover. Although this sug-
gested that anhydrobiotic tardigrades were not strictly
ametabolic, later work on anhydrobiotic cysts of the
crustacean Artemia (e.g., CLEGG 1973, 1986) have
established the current paradigm that considers anhy-
drobiosis as a truly ametabolic state.
Anhydrobiosis represents a latent life form qualitative-
ly distinct from metabolically active life forms by the
absence of energy turnover and replication, which in
turn prohibits any processes of reproduction and
growth. The only life history characteristic that the
active and latent states have in common is therefore
survival. Thus, anhydrobiotic life forms offer organ-
isms nothing more than survival, which nevertheless is
of paramount importance, since it provides the oppor-
tunity of continuous persistence in an otherwise hostile
habitat. However, indirectly anhydrobiosis may affect
also reproduction and growth, by withdrawing energy
from potential use in the latter functions. Anhydrobiot-
ic periods also have an obvious impact on the genera-
tion time, which in turn influences the potential rate of
evolution. Consequently, anhydrobiotic life stages may
have strong effects on the evolution of life histories.
Despite a considerable interest in anhydrobiosis, the
evolutionary background to this biological phe-
nomenon has received little attention, and there exist
very few studies on the nature of selection on anhy-
drobiosis. This is true both in general, and regarding
tardigrades. The main purpose of this review is there-
fore to encourage biologists to consider evolutionary
Zool. Anz. 240 (2001): 409–417
© by Urban & Fischer Verlag
http://www.urbanfischer.de/journals/zoolanz
*
Contribution to the 8th International Symposium on
Tardigrada, Copenhagen, Denmark, 30 July–5 August 2000.