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Tardigrades Are They Really Miniaturized

Dwarfs?
Article in Zoologischer Anzeiger - A Journal of Comparative Zoology December 2001
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Zool. Anz. 240 (2001): 549555

by Urban & Fischer Verlag
http://www.urbanfischer.de/journals/zoolanz

Tardigrades Are They Really Miniaturized Dwarfs?*

Andreas SCHMIDT-RHAESA
Zoomorphology and Systematics, University of Bielefeld, Faculty of Biology, Bielefeld, Germany

Abstract. Tardigrades are animals of small body size which is often regarded to be a secondary phenomenon. This
interpretation makes sense in the traditional concept that tardigrades are closely related to Onychophora, Euarthropoda and Annelida. A large body size in the ancestor of this common taxon (Articulata) is probable. Small size and
the absence of organs such as a dorsal heart, segmental coelomic cavities and metanephridia must then be interpreted as derived in tardigrades. However, when Cycloneuralia are taken as an outgroup instead of Annelida
(taxon Ecdysozoa), an interpretation of small body size as a primary feature is plausible. This also accounts for the
absence of heart, coelom and nephridia.The choice of outgroup influences hypotheses about sister-group relationships within Panarthropoda, with either Onychophora (Articulata-concept) or Tardigrada (Ecdysozoa-concept)
being basal.
Key words. Tardigrada, Panarthropoda, Articulata, Ecdysozoa, miniaturization, phylogeny.

1. INTRODUCTION
The relationship of tardigrades to other taxa has been
regarded for some time as more or less uncertain,
because they show characters resembling either those
of aschelminth groups or those of onychophorans
and euarthropods. Therefore, some authors preferred to
treat them as enigmatic groups (BRUSCA & BRUSCA
1990; AX 1999), but most recent morphological and
molecular analyses suggest a close relationship of
Tardigrada, Onychophora and Euarthropoda (e.g.
NIELSEN 2001; GAREY et al. 1996; GIRIBERT et al.
1996). The common taxon of Tardigrada, Onychophora and Euarthropoda is either termed Arthropoda or
Panarthropoda (NIELSEN 2001). Although the latter
name leads to confusion with the Pan-concept in phylogeny (LAUTERBACH 1989), this name is currently
abundantly applied and will be used in this paper.
All tardigrades are small animals with body lengths
usually less than 1 mm. They lack some characters of
their close relatives such as a dorsal heart, segmental
coelomic cavities or metanephridia. This lack has often
been explained by a reduction due to a miniaturization
(DEWEL & DEWEL 1997), probably through the process
*

Contribution to the 8th International Symposium on

Tardigrada, Copenhagen, Denmark, 30 July5 August 2000.

of paedomorphosis. This explanation seems plausible

in the traditional hypothesis that Annelida is the sister
group of Panarthropoda. If heart, coelomic cavities and
metanephridia are homologous between annelids, onychophorans and euarthropods, then it is most parsimonious to assume that they were present in the common
stem species of Panarthropoda and Annelida and they
must have been lost in tardigrades.
Recently, the traditional relationship between annelids
and panarthropods has been challenged by the hypothesis that moulting aschelminthes (taxon Cycloneuralia) are closely related to panarthropods in a taxon
Ecdysozoa (AGUINALDO et al. 1997; SCHMIDT-RHAESA
et al. 1998). Cycloneuralia contain Nematoda, Nematomorpha, Priapulida, Kinorhyncha and Loricifera.
This Ecdysozoa-hypothesis challenges the reinvestigation of the interpretation of body size in tardigrades
and their phylogenetic position within panarthropods.
If aschelminth taxa are closest relatives to panarthropods, then it has to be checked if small body size could
be primary in tardigrades.

2. IS PAEDOMORPHOSIS PROBABLE
IN TARDIGRADES?
Paedomorphosis, i.e. the combination of juvenile characters and sexual maturation might be achieved by
0044-5231/01/240/0304-549 $ 15.00/0

550

A. SCHMIDT-RHAESA

Fig. 2. Three possibilities for relationships within

Panarthropoda. E = Euarthropoda, O = Onychophora, T =
Tardigrada.

3. THE BRANCHING ORDER WITHIN

PANARTHROPODA

Fig. 1. A. Test for paedomorphosis: a character from the

stem lineage of two taxa is present in juveniles of one taxon
but in sexually mature taxa of the paedomorphic one. B.
Miniaturization can be postulated after a phylogenetic analysis by the interpretation of character distribution.

accelerated gonad maturation (progenesis) or by retarded somatic development (neoteny) (GOULD 1977).
The most elegant way to detect metamorphosis is to
find a character which occurs in mature specimens of
the probably paedomorphic taxon but only in juvenile
representatives of closely related taxa (Fig. 1A) (see
also AX 1999). Such a character is not evident for tardigrades in comparison with onychophorans and euarthropods. Small body size alone seems not to be a sufficient character for this category, because it is too broadly distributed and a general character of all taxa.
A second approach might be an a posteriori conclusion
from a phylogenetic analysis. If it is the most parsimonious explanation of a cladogram that the ancestor of a
taxon including tardigrades was large in size, then
small size in tardigrades must be secondary. However,
this a posteriori explanation only indicates a miniaturization that is not automatically synonymous with paedomorphosis. This second approach will be examined
in more detail below.
The discussion about body size of one taxon is not
directly dependant on hypotheses of the body size of
the metazoan or bilaterian ancestor. Although different
hypothesis exist (see RIEGER et al. 1991; DEWEL 2000),
it is evident that multiple body size changes occurred
through evolution and that it is important to reconstruct
the body size of each taxon separately. Even if the bilaterian ancestor was large, we have to ask if miniaturization occurred in the stem lineage of tardigrades or
a higher taxon such as e.g. Panarthropoda or Gastroneuralia.

There are three different possibilities for the branching

order within Panarthropoda (Fig. 2): Tardigrada (T)
and Euarthropoda (E) as a sister group and Onychophora (O) as the basal taxon, O and E as sister
groups with basal T or O and T as sister groups (sometimes named Protarthropoda or Lobopodia). Molecular
analyses to date do not support any one of these possibilities, because either the topology is not resolved
with significant statistical support (AGUINALDO et al.
1997; GAREY in press) or because onychophorans were
not included in the analyses (GAREY et al. 1996; GIRIBERT et al. 1996; MOON & KIM 1996). The hypothesis
most often suggested is a sister-group relationship of
Tardigrada and Euarthropoda (NIELSEN 2001; WILLS et
al. 1995, 1997, 1998; BUDD 1996; NIELSEN et al. 1996;
DEWEL & DEWEL 1997; ZRZAVY et al. 1998; EDGECOMBE et al. 2000). Other analyses, especially of
approaches combining morphological and molecular
data, remain unclear (WHEELER 1997; GIRIBERT & RIBERA 2000) or favour a sister-group relationship of
Tardigrada and Onychophora (WAGGONER 1996;
GIRIBERT et al. 2000).
The sister-group relationship of tardigrades and euarthropods is supported by three characters that are independant of the choice of the outgroup:
(1) sclerotization of dorsal and ventral plates
(2) disintegration of muscular sheets below the
epidermis
(3) bismuth staining of the golgi complex
Character (1) is dependant on the homology of dorsal
and ventral plates of tardigrades with tergites and sternites of euarthropods. Furthermore, it must be a character present in the tardigrade ancestor. This is generally assumed (KRISTENSEN 1987; DEWEL & DEWEL 1997)
and the absence of such plates in halechiniscid heterotardigrades (BELLO & DE ZIO GRIMALDI 1998;
DADDABBO GALLO et al. 1999) and in eutardigrades is
thought to be secondary. The disintegration of muscles
from a continuous sheet into separated muscle strands
might be dependant on the stronger sclerotization of

Tardigrades as Miniaturized Dwarfs?

large parts of the cuticle, because cuticular plates functionally substitute a continuous muscular layer in the
sense of stability and protection. The staining of the
golgi complex with bismuth (3) (LOCKE & HUIE 1977)
is present in the tardigrade Hypsibius sp. and several
euarthropods, but not in the onychophoran Epiperipatus sp. and representatives of annelids, molluscs,
nematodes, plathelminthes and cnidarians. The basis
for this different staining, however, is unknown.
Several additional characters which have been mentioned in the literature for a sister-group relationship of
tardigrades and euarthropods might not be as strong
arguments. DEWEL & DEWEL (1997) mention that the
fine structure of sensilla is not specific for tardigrades
and euarthropods as proposed by KRISTENSEN (1981),
but that a similar structure also occurs in nematodes.
BUDD (1996) mentions the reflection of the internal
segmentation on the surface (= external segmentation)
as a probable synapomorphy of tardigrades and euarthropods, in contrast to the multiple annuli in onychophorans that do not reflect internal segmentation.
This character is dependant on the phylogenetic position of several fossils with an annulated cuticle, but the
external reflection of internal segmentation might also
be the plesiomorphic condition. Cross-striated muscles
are taken as a synapomorphy of tardigrades and euarthropods (NIELSEN 2001), but cross-striated muscles
are widely distributed among metazoans and are also
present in mandibular muscles of onychophorans
(H. RUHBERG, pers. comm. 2000).
The sister-group relationship of onychophorans and
euarthropods is supported by one character which is
independent of the choice of the outgroup. This refers
to a shift of the mouth opening from a terminal to a
ventral position. The ventral position is typical for
Onychophora and Euarthropoda, as well as for fossils
from the euarthropod stem-group such as Pambdelurion, Anomalocaris and Parapeytoia (DEWEL et al.
1999). In tardigrades, the mouth opening is either terminal or slightly ventral (both states are e.g. present in
Styraconyx, see KRISTENSEN & HIGGINS 1984), but not
as extreme as e.g. in onychophorans. DEWEL et al.
(1999) presented a possible scenario of a posterior
movement of the mouth opening which also explains
patterns in the association of the stomodeal nervous
system with the brain. This shift of the mouth region
can be observed in the embryogenesis of onychophorans and in the pathway of nerves innervating
the mouth region which run anteriorly and then turn
posterior to the mouth region (ERIKSSON & BUDD
2001). Tardigrades represent in this model the basal
condition, from which movement of the mouth cone as
well as incorporation of further ganglia into the head
started. If this interpretation is true, the shift of the
mouth region could be interpreted as a character sup-

551

porting a sister-group relationship between Onychophora and Euarthropoda. One problem is the position of Kerygmachela kierkegaardi (BUDD 1993,
1999), which has a terminal mouth, but is placed, due
to its frontal appendages, close to the likely paraphyletic group of anomalocaridid-like animals (BUDD
1993, 1999; CHEN et al. 1994) which in turn are probable stem-group euarthropods. This means that Kerygmachela either has returned to a terminal position of
the mouth or that the posterior shift of the mouth
region occurred convergently in onychophorans and
euarthropods (including fossil stem-group taxa).
A character complex that is difficult to evaluate is the
nervous system. This is particularly due to the highly
aberrant nervous system of Onychophora (SCHRMANN
1987, 1995; STORCH & RUHBERG 1993). The onychophoran brain is tripartite only in early development
(PFLUGFELDER 1948), but these results should be newly
documented with modern methods. In tardigrades, a
tripartition is recognizable and is often homologized
with proto-, detuto- and tritocerebrum of euarthropods
(NIELSEN 2001), but according to DEWEL & DEWEL
(1996), the whole tardigrade brain is homologous to
the protocerebrum of euarthropods. The main nerve
cords are widely separated in onychophorans which
probably is a derived feature. Onychophorans lack
clearly separated ganglia, instead, somata occur along
the nerve cord which are connected by 910 commissures per segment (SCHRMANN 1995). If these characters are also derived, then it is not clear if the structure
of the nervous system in tardigrades and euarthropods
is a synapomorphy between both taxa or plesiomorphic
within Panarthropoda.

4. ANNELIDA AS SISTER GROUP

OF PANARTHROPODA
If Articulata (Annelida + Panarthropoda) is a valid
taxon, then it is inevitable to homologize segmentation
and associated segmental characters such as coelomic
cavities, metanephridia and ganglia. The most parsimonious explanation is that the common ancestor of
annelids and panarthropods was segmented and possessed these characters. The body size of the articulate
ancestor was probably large. Although the basal organization of annelids is still highly discussed (see WESTHEIDE et al. 1999) with either a polychaete-like (WESTHEIDE 1997) or an oligochaete-like organism (CLARK
1964; ROUSE & FAUCHALD 1997) being ancestral, both
hypotheses favour a large body size. Small body size in
annelids has been shown in several cases to be a secondary phenomenon (e.g. WESTHEIDE 1985, 1987,
1990; EIBYE-JACOBSEN & KRISTENSEN 1994). Large
body size in the ground pattern of annelids corresponds

552

A. SCHMIDT-RHAESA

to the large body size of extant onychophorans and

many stem-lineage fossils (see below) and was therefore probably also present in the articulate ancestor.
Therefore, tardigrades must be considered to be miniaturized organisms under this hypothesis.

5. CYCLONEURALIA AS SISTER GROUP

OF PANARTHROPODA
If Ecdysozoa (Cycloneuralia + Panarthropoda) is
favoured, the complex of segmentation has either to be
assumed to have evolved convergently in annelids and
arthropods or to be a plesiomorphic feature within
Bilateria (KIMMEL 1996; DE ROBERTIS 1997). According to phylogenetic hypotheses, an origin of segmentation in the Bilateria seems implausible, because segmentation does not occur in likely basal bilaterian taxa
(e.g. Platyhelminthes, Gnathostomulida, Gastrotricha,
Nemertini, Nematoda). If it evolved convergently, then
the following characters could be evaluated as synapomorphies between Onychophora and Euarthropoda:
(1) dorsal heart with ostiae and a pericardial septum
(2) segmental coelomic cavities
(3) metanephridia
Tardigrades show no trace of a circulatory (1) or excretory (3) system. The nature of the cavities (2) occurring
in early development of tardigrades could not be definitely resolved, but they do not develop through enterocoely as has been the traditional view and they are
probably not coelomic cavities (EIBYE-JACOBSEN
1996). In comparison with Cycloneuralia, these lacks
seem to be plesiomorphic features.
The Cycloneuralia comprise Nematoda, Nematomorpha, Priapulida, Kinorhyncha and Loricifera. Kinorhyncha and Loricifera are small interstitial animals,
the same is likely for the nematode stem species.
Nematomorpha are large in body size, but this probably arose secondarily in connection with the parasitic
phase in the life cycle, as it occurs in parallel within
nematodes. Priapulida include large and small, interstitial taxa. According to the phylogenetic analysis of
LEMBURG (1999), the small taxa (Tubiluchus, Meiopriapulus, Maccabeus) are basal within extant Priapulida,
although large fossil taxa probably branched off before
the small extant priapulids (WILLS 1998). An original
small size of priapulids is contrasted by arguments
connecting the primitive type of spermatozoon with
free spawning, the need to store large quantities of
gametes and therefore large body size (LORENZEN
1985, 1996). However, this line of argument is not a
strict constraint, because the primitive type of spermatozoon can also be present in small taxa such as Meiopriapulus (STORCH et al. 1989). Additionally, this

hypothesis does not correspond to the parsimonious

explanation that suggests small body size as primary in
Cycloneuralia.
Most often, Cycloneuralia are regarded as the sister
group of Panarthropoda, but recently (GAREY in press)
Cycloneuralia have been regarded as paraphyletic with
Nematoda + Nematomorpha being related most closely to Panarthropoda than Priapulida + Kinorhyncha
(Loricifera were not analyzed). However, this does not
change the interpretation of small body size as being
basal.
Small body size in Cycloneuralia would make large
body size another possible synapomorphy of Onychophora and Euarthropoda. Tardigrades would therefore fit well as the basal panarthropod taxon under the
Ecdysozoa-hypothesis. This position could also
explain the composition of tardigrades of aschelminth and arthropod characters. At least some of the
aschelminth characters (see KINCHIN 1994; SCHMIDTRHAESA et al. 1998; KRISTENSEN in press) could be plesiomorphies taken from the common ancestor with
Cycloneuralia. However, this will not apply to all such
characters and some will likely turn out to be convergences.

6. DO FOSSILS HELP?
Only a few fossil tardigrades have been described. Two
tardigrades were discovered in cretaceous amber:
Beorn leggi (COOPER 1964) and Milnesium sp.
(BERTOLANI & GRIMALDI 2000). Four specimens were
extracted from about 530 million year old Middle
Cambrian Orsten-type rock in Siberia (MLLER et al.
1995). These show remarkable resemblance to extant
tardigrades with the exception that they have only
three pairs of legs. A developmental precursor of a
fourth pair may be present. Assuming this fossil is a
real tardigrade, it indicate that tardigrades recognizable as such have existed since the Cambrian.
Assignments of further fossils to tardigrades are not
unambiguous. For several lobopod fossils such as
Aysheaia, Microdictyon, Xenusion, Onychodictyon,
Hallucigenia and others, a close relationship to extant
Onychophora has been assumed (ROBISON 1985;
RAMSKLD & HOU 1991; RAMSKLD 1992; HOU &
BERGSTRM 1995), but some authors also hint at similarities of tardigrades with some of these taxa (e.g.
DELLE CAVE & SIMONETTA 1975; WHITTINGTON 1978).
Most of these similarities may be superficial or plesiomorphic, as has been pointed out by ROBISON
(1985).
It has become clear that a number of fossils, including
weird wonders such as Hallucigenia, Anomalocaris
and Opabinia can be placed in the stem lineages within

Tardigrades as Miniaturized Dwarfs?

Panarthropoda (e.g. BUDD 1997; BUDD & JENSEN

2000). This approach is very promising because it
offers the chance to reconstruct panarthropod evolution in more detail. Although tardigrades seem not to
be tied to a certain position by fossil taxa to date, this
might be expected through further analyses (see BUDD
2001). Interestingly, most fossil panarthropods from
Cambrian locations such as the Burgess Shale or the
Chengjiang Fauna are large in size. This could hint at a
large body size as plesiomorphic for Panarthropoda or
at a preservation bias towards large animals.

7. CONCLUSIONS
Deciding if small body size in tardigrades is primary or
secondary is dependant on the outgroup choosen for
Panarthropoda. Under the Articulata-hypothesis, it
seems evident that tardigrades must be miniaturized
and have lost some characters that their ancestors must
have possessed such as coelomic cavities and
metanephridia. Under the Ecdysozoa-hypothesis,
tardigrades might be the basal taxon within Arthropoda
and their small body size can be explained as a primary
feature. It is out of the scope of this paper to evaluate
the evidence for or against both hypotheses (see
SCHMIDT-RHAESA et al. 1998; WGELE et al. 1999;
BUDD in press; GAREY in press; KRISTENSEN in press;
SCHMIDT-RHAESA in press; SCHOLTZ in press).
Acknowledgements. The topic of this paper gained much
stimulation through discussions with participants of the
eighth International Symposium on Tardigrada in Copenhagen, particularly with Graham Budd, Ruth Dewel, Jim
Garey, Reinhardt Mbjerg Kristensen and Hilke Ruhberg.
Thanks also to Roberto Bertolani and Dieter Waloek for
informations concerning fossil tardigrades.

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Authors address: Andreas SCHMIDT-RHAESA, Zoomorphology and Systematics, University of Bielefeld, Faculty of
Biology, P.O.Box 100131, D-33501 Bielefeld, Germany;
Tel.: ++49 (0)521/106 2720; Fax: ++49 (0)521/106 6426,
e-mail: a.schmidt-rhaesa@biologie.uni-bielefeld.de
Received: 31. 10. 2000
Reviewed: 20. 04. 2001
Accepted: 30. 08. 2001
Corresponding Editor: R. M. KRISTENSEN