Invited Review
Blackwell Publishing Ltd.
The scientific status of metazoan cladistics: why current
research practice must change
RONALD A. JENNER
Accepted: 14 August 2003
Jenner, R. A. (2004). The scientific status of metazoan cladistics: why current research practice
must change. — Zoologica Scripta, 33, 293– 310.
Metazoan phylogenetics is bustling with activity. The use of comprehensive morphological
data sets in recent phylogenetic analyses of the Metazoa indicates that morphological evidence
continues to play a key role in the reconstruction of metazoan deep history. In this paper I review
the scientific status of morphological metazoan cladistics from the perspective of cladistic research
cycles. Each research cycle consists of three main steps: (1) the compilation of a data matrix
(2) the simultaneous evaluation of all possible cladograms in a character congruence test, and
(3) the assessment of the relationship between evidence and hypothesis after finding the optimal
tree. I identify a striking discrepancy between the sophistication of the analysis of given data
sets (Step 2), and their compilation and the interpretation of the results (Steps 1 and 3). The
latter two steps deserve far greater attention than is current practice. Uncritical and nonexplicit
character selection, character coding, and character scoring seriously compromise Step 1.
Careful comparative morphological study prior to data matrix construction is necessary to
remedy this problem in future cladistic analyses. Step 2 is the locus of most recent advances
in metazoan cladistics through the increasing availability of computing power, and the
development of increasingly efficient phylogenetic software that allows analysis of large data
sets. Failure to identify problems and errors generated in Step 1 of the research cycle is testament
to the general failure of Step 3. Consequently, recent progress in metazoan cladistics is primarily
analytical, while the only empirical anchor of the discipline receives surprisingly little attention.
Not surprisingly, the first generation of modern metazoan phylogeneticists used computers
principally as a relatively quick and easy means to generate abundant phylogenies from
morphological data. The next phase should build on this foundation by critically testing these
alternative hypotheses by a thorough qualitative reassessment and elaboration of morphological
data matrices, and a more critical approach to data selection. A rigorous research program
for metazoan cladistics can only be established when the cladistic research cycle is properly
completed, and when subsequent research cycles are effectively linked to previous efforts.
Ronald A. Jenner, University Museum of Zoology, University of Cambridge, Downing Street, Cambridge CB2 3EJ, UK. E-mail: [email protected]
Introduction
Whereas the first blossoming of phylogenetic zoology in the
second half of the 19th century was boosted by a wholesale conceptual change (the advent of evolutionism; Bowler
1996), it appears that current enthusiasm for metazoan phylogenetics derives largely from technological advances. The
ability to discover phylogenetic signal in molecular sequence
data, the availability of increasingly powerful computers, and
the development of efficient software suitable for the analysis
of large molecular and morphological data sets has lifted
metazoan phylogenetics to a level unprecedented in the history of biology.
© The Norwegian Academy of Science and Letters • Zoologica Scripta, 33, 4, July 2004, pp293– 310
The current state of metazoan cladistics stands in sharp
contrast with that prevailing just 15 years ago. The first generation of molecular phylogeneticists was hard-pressed to
find reliable morphology-based hypotheses with which to
compare their findings. Typically they either resorted to presenting unreferenced ‘traditional views’, or they presented
(or misrepresented) the alleged views of Libbie Hyman
( Jenner 2000). The new millennium began with an explosion of
new phylogenetic analyses of the animal phyla (throughout
this paper I use the term ‘phylum’ as a general descriptor of
higher-level taxa without any Linnaean rank connotations). If
only those studies are counted that analyse the entire Bilateria
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Scientific status of metazoan cladistics • R. A. Jenner
or Metazoa, using morphological data, no fewer than seven
have been published over the last 3 years (Giribet et al. 2000;
Sørensen et al. 2000; Nielsen 2001; Peterson & Eernisse 2001;
Zrzavy et al. 2001; Zrzavy 2003; Brusca & Brusca 2003). If we
also count analyses of smaller scope, purely molecular papers,
and papers published from the late 1980s onward, we are
confronted with a veritable forest of metazoan phylogenies.
In addition, the phylogenetic relationships within many different phyla are currently being analysed as well. This makes
the phylogenetic systematics of the Metazoa a very active
research area. In contrast, far fewer papers have been expressly
concerned with the methodology of morphological metazoan
cladistics in order to identify the nature of progress in this
field ( Jenner & Schram 1999; Jenner 2000, 2003), while
some further methodological comments can be found in
Zrzavy (2001) and Giribet (2002). The wave of publications
in the new millennium invites another detailed look at the
practice of metazoan cladistics.
Consensus and controversy in metazoan cladistics
The easiest way to assess the degree of consensus in metazoan
phylogenetics is by assessing topological congruence among
the results of different studies; this is how all recent papers
sketch established consensus and identify remaining controversy. For example, in a recent review of metazoan phylogenetics Giribet (2002: 352) outlines the beginning of a ‘stable
hypothesis’ of metazoan relationships that is purported to be
in agreement with at least the most recent comprehensive
analyses. The split of the Bilateria into a monophyletic Protostomia and Deuterostomia, the division of the protostomes
into the clades Ecdysozoa and Lophotrochozoa, and the division of the latter into the clades Trochozoa and Platyzoa are
nominated as the strongest areas of consensus (see also Zrzavy
2001, 2003). Indeed, a glance at the current literature leaves
no doubt that these patterns of deep divergences within the
Metazoa are generally accepted as current consensus.
Recent phylogenetic studies also show consensus on a finer
scale, especially if one considers only one type of evidence,
for example morphological data. There is at least agreement
among morphological cladistic analyses published over the
last 3 years about the monophyly of the Cephalorhyncha
sensu Nielsen (2001) (= Scalidophora sensu Lemburg 1995),
which comprises the Kinorhyncha, Loricifera, and Priapulida
(Giribet et al. 2000 retrieved a paraphyletic Cephalorhyncha,
but excluded the loriciferans from the analysis). The monophyly of the Panarthropoda (Tardigrada, Onychophora, and
Arthropoda) is also supported, as is the sister-group relationship of the Phoronida and Brachiopoda (Zrzavy et al. 2001
resolved the phoronids and the brachiopods as successive
sister taxa to a clade of Echinodermata, Chordata, and Hemichordata). The monophyly of the Syndermata (the rotifers
and acanthocephalans) is also supported. However, beyond
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the monophyly of these clades, their positions within the
Metazoa and placement of other phyla within the Bilateria
are still very much uncertain. Taking molecular and total
evidence analyses into consideration as well does not greatly
clarify the picture as relationships within the Ecdysozoa, and
even more so in the Lophotrochozoa, remain uncertain. In
fact, I would argue that the previously mentioned consensus
of even the deepest divergences within the Metazoa is much
more tentative than recent review papers depict.
First, the most recent cladistic analyses frequently disagree
with respect both to the placement of single phyla and to the
monophyly of larger supraphyletic clades. Topologies of molecular and total evidence analyses are sensitive to parameter changes
and differences in taxon selection. This becomes especially clear
when the total evidence analyses of Zrzavy et al. (1998) and
Giribet et al. (2000) are compared. Although they employ the
same morphological data set, differences in taxon sampling,
molecular sequence alignment procedure and analysis parameters
lead to a remarkable degree of incongruence. More generally,
a comparison of the most recent cladistic analyses shows that
the phylogenetic positions of several phyla are far from certain.
These include the ectoprocts, chaetognaths, gastrotrichs, brachiopods + phoronids, entoprocts, cycliophorans, and platyhelminths,
to mention just some of the most prominent examples.
Second, the appearance of consensus concerning even some
of the most basal animal divergences may be misleading. The
sister-group relationship between the monophyletic deuterostomes and protostomes is heralded as one of the clearest
signs of current consensus (Giribet 2002; Zrzavy 2003). However,
various of the most comprehensive phylogenetic analyses of
18S rDNA and total evidence (using either maximum parsimony or maximum likelihood methods) show instead a
paraphyletic Protostomia with the deuterostomes variously
related to the lophotrochozoans, the ecdysozoans, or both
(Peterson & Eernisse 2001; Jondelius et al. 2002; Zrzavy
2003). The fact that similar topologies with a paraphyletic
Protostomia are found with other molecules as well, such as
mitochondrial gene sequences ( Jondelius et al. 2002) or
myosin II sequences (Ruiz-Trillo et al. 2002) indicate that the
monophyly of the protostomes is not yet firmly established.
These findings cannot simply be dismissed as artifacts of
cladogram rooting because a paraphyletic Protostomia is
found in analyses with widely accepted basal metazoan relationships, viz. the acoels (or acoelomorphs) as sister group to
the remaining bilaterians, and the nonbilaterians as sister
group(s) to the Bilateria. Furthermore, morphological study
indicates that various characters that have previously been
taken to suggest a fundamental division between the protostomes and the deuterostomes are unreliable. This holds
true, for example, for the sources of mesoderm, the relationship between the larval apical organ and the adult brain, and
the possession of cerebral ganglia (Jenner, in press).
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R. A. Jenner • Scientific status of metazoan cladistics
Third, and of particular relevance to phylogenies based
upon morphological evidence, even identical cladogram
topologies do not necessarily reflect an agreement of underlying data. For example, many comprehensive morphological
cladistic analyses published during the last decade have
yielded apparent support for a monophyletic Plathelminthomorpha (Platyhelminthes + Gnathostomulida) (e.g. Schram
1991; Eernisse et al. 1992; Zrzavy et al. 1998; Giribet et al.
2000; Peterson & Eernisse 2001). However, as discussed in
detail in Jenner (in press), the morphological support for
Plathelminthomorpha in these different studies may not even
be in agreement due to problems in character scoring. Similarly, the morphological phylogenies of both Zrzavy et al.
(1998) and Peterson & Eernisse (2001) supported the nesting
of the acoels within the Platyhelminthes rather than at the base
of the Bilateria as had been suggested before (Haszprunar
1996). However, the power of these analyses properly to
test the position of the acoels within the Metazoa differed
markedly as a result of differences in character selection
(Jenner, in press). Consequently, the results of these studies
cannot be meaningfully interpreted as support for the same
conclusion.
In the remainder of this paper I will focus on morphological cladistic analyses of the Metazoa. Morphological evidence continues to play a key role in the reconstruction of
metazoan deep history, as is witnessed by the analysis of
morphological data sets in all recent cladistic analyses of the
animal phyla. Despite the fact that molecular data, in particular 18S rDNA sequences, have come to play a major role in
metazoan phylogenetics, these data offer little reliable finescale resolution within the major bilaterian clades. Here morphology still has a lot to offer. In any case, reliably compiled
morphological data sets provide invaluable information for
studying the evolution of animal body plans, if only to flesh
out a molecular phylogenetic skeleton. Specifically, I want to
address the question of whether recent advances in metazoan
cladistics are producing a deeper understanding of metazoan
phylogeny and character evolution, or merely a stochastic
change of opinion. It should be noted that several of the general points made in this paper have been elaborated elsewhere
(Jenner & Schram 1999; Jenner 2000, 2001, 2002, 2003).
This contribution integrates all aspects into a single coherent
framework, that of the cladistic research cycle, that can function as the basis from which to reform current practice into
an efficiently operating research program.
The science of cladistics: research cycles and
hypothesis testing
The goal of cladistics is to gain an understanding of phylogeny and synapomorphies. To gain such knowledge, cladistic
research proceeds through different steps that can be related
as parts of a research cycle (Kluge 1998). Three steps may be
© The Norwegian Academy of Science and Letters • Zoologica Scripta, 33, 4, July 2004, pp293– 310
distinguished. The first involves the selection of terminal taxa
and characters, which leads to the construction of the data
matrix. This crucial step (hereafter referred to as Step 1)
involves all the science of selecting monophyletic taxa and
determining primary homologies, i.e. studying organismic
variation, and identifying, coding, and scoring of characters
and character states. When higher-level taxa are used as terminals, many difficult issues need to be addressed, such as
how to deal with character variation within terminals, and
how to infer or assume ground pattern states for characters.
The second step (Step 2) is the simultaneous testing of all
possible cladograms during the character congruence test
(the cladogram building phase). This is for the most part an
automated process involving computers and specialized software, and it results in one or more most parsimonious cladograms. These cladograms provide the best explanation of
observed similarity as homologies that are the result of descent
with modification. During the third step (Step 3) the relationship between evidence (data matrix) and hypothesis (cladogram)
is assessed, and it is in this phase that an increased understanding of phylogeny and character evolution may be
achieved. This stage may involve the performance of clade
support analysis, the reappraisal of character state identity
and character state polarity, or the reevaluation of homoplasies incongruent with the favoured hypothesis. It may also
include the performance of a test of consilience with independent data, such as comparing the phylogenies of hosts and
parasites, or phylogenies derived from molecular and morphological data sources (Lee & Doughty 1997; Kluge 1998).
The conclusions reached in Step 3 may subsequently be fed
into a new cladistic research cycle, for example as modifications
of character coding and scoring. In this manner taxonomic
relationships and character homologies can be further assessed,
while increasing our understanding of the relationship between
evidence and hypothesis.
Because the results of one research cycle need not provide
a complete understanding of relationships and homologies,
they may be used as a starting point for an emended analysis.
This is, of course, especially relevant for a highly diverse
taxon such as the Metazoa, for which a consensus of relationships is still elusive. A healthy cladistic research program
therefore consists of repeated rounds through the research
cycle in which new analyses take previous efforts explicitly
into account as the goal of research shifts from providing an
intial phylogenetic estimate of a group to the effective testing
of alternative phylogenetic hypotheses. One can test previously
proposed hypotheses by introducing incongruent synapomorphies, adding additional taxa, or reappraising homologies
(e.g. Kluge 1997; Rieppel & Kearney 2002; Jenner 2003, in press).
In order to qualify as good science, cladistic studies have to
pay due attention to all steps of the cladistic research cycle.
This means that for Step 1 the decisions that feed into the
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Scientific status of metazoan cladistics • R. A. Jenner
construction of the data matrix need to be made explicit. This
is done by explicitly justifying the criteria used to select characters and taxa, and by performing a rigorous study of comparative morphology to justify character coding and scoring.
For taxa where one research cycle has already been performed,
previous work needs to be explicitly incorporated into the
new analysis, that is, older data sets need to be taken into
account when compiling a new one. A detailed comparison of
data selection and character coding and scoring are necessary
ingredients. In Step 2 a proper computer-assisted phylogenetic analysis needs to be performed to find the optimal tree
under the adopted optimality criterion (as in maximum
parsimony), or under the adopted model of evolution (as in
maximum likelihood). In Step 3 the robustness of the results
needs to be assessed with a variety of methods, such as quantitative clade support measures, bootstrap analysis, parsimony
jackknifing, and Bremer support analysis. However, this final
step also provides the opportunity to explore the relationship
between hypothesis and evidence from the viewpoint of a
biologist. For example, we may analyse what the character
state transformations tell us about body plan evolution, and
we may reevaluate character state identity, character independence, and homoplasies. A survey of current practice in
metazoan cladistics leads to a striking conclusion: in general,
only Step 2 receives adequate attention. Many serious shortcomings of Steps 1 and 3 can be identified that cannot simply
be explained as occasional errors. As I will argue in this paper,
the practice of metazoan cladistics should be revised significantly by improving Steps 1 and 3 if we are to deepen
our understanding of metazoan phylogeny and character
evolution.
Hypothesis testing and selection of characters
and taxa
It is an acknowledged dictum of cladistics that all known pertinent information should be included within an analysis, lest
the results be unjustifiably biased towards certain conclusions. Discovering incongruent synapomorphies can refute
cladistic hypotheses, and the severity of a cladistic test is
therefore correlated with the empirical content of the data set
because a larger data set contains a greater number of potential falsifiers of a given cladistic hypothesis (Kluge 1997;
Siddall & Kluge 1997). In order to find the most corroborated
and most severely tested cladogram, it thus becomes critical
to establish ‘how honestly the relevant data are surveyed for
those synapomorphies that actually have the potential to
refute a cladistic hypothesis, those synapomorphies that can
count as independent ad hoc hypotheses of homoplasy’
(Kluge 1998: 350).
Strikingly, recent phylogenetic analyses of the Metazoa or
Bilateria (for simplicity I will only refer to Metazoa hereafter)
differ markedly in the number of included characters, and
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consequently in the amount of organismic variation represented by their data matrices. For example, recent cladistic
analyses have data sets ranging from 64 characters (Nielsen
2001) to 276 (Zrzavy et al. 1998). This difference indicates
that analyses differ significantly in the power to test competing phylogenetic hypotheses. Unfortunately, although some
studies justify the exclusion of several characters from their
analyses, explicit justification for the inclusion and exclusion
of all previously proposed and potentially informative
characters is never given.
How are we to choose between contending hypotheses based
on different data matrices? With high empirical content as a
desired epistemic value, it appears reasonable to use sheer size
of the morphological data sets as one criterion to select among
available cladistic hypotheses. Zrzavy et al. (1998) compiled
the largest morphological data set to date, comprising 276 morphological characters. However, the quality of the included data
leaves much to be desired ( Jenner 2001, 2002, 2003, in press).
The myriad hidden details in which published metazoan
cladistic analyses differ from each other prevent at this time
any straightforward conclusion about the relative merit of the
different cladogram topologies generated by these studies. To
start with the logic of character selection in recent studies, I
will discuss one example of how insufficient attention to the
relationship between character selection and hypothesis testing
has hampered our understanding of the phylogenetic position
of a phylum.
A case study of arbitrary character selection:
placing Entoprocta
The entoprocts are notoriously difficult to place in the
animal kingdom (Nielsen 2000, 2002). A broad phylogenetic
assignment, however, can relatively easily be made. They
possess spiral quartet cleavage, mesoderm derived from a 4d
mesentoblast, and trochophore larvae, which are characters
that at least appear to indicate a close relationship with other
spiralian protostomes such as the neotrochozoans (Mollusca,
Echiura, Sipuncula, Annelida), and the nemerteans. This
conclusion is compatible with all recent cladistic studies.
However, if we want to be able to test different hypotheses
proposed to explain the evolution of the entoproct body plan
(the adult plan has, for example, been derived through loss of
the coelom in a sessile ectoproct-like ancestor, or by paedomorphosis from a coelomate or noncoelomate motile ancestor: Bergström 1997; Cavalier-Smith 1998; Nielsen 2001) we
need a better idea about the sister group of the entoprocts.
Recent morphological phylogenetic studies have suggested various different candidates, including Ectoprocta
(Nielsen 2001), Mollusca (Bartolomaeus 1993; Haszprunar
1996, 2000; Ax 1999), Cycliophora (Zrzavy et al. 1998;
Sørensen et al. 2000; M. Obst, pers. comm.), Lobatocerebromorpha (Zrzavy et al. 2001), Rotifera + Gnathostomulida
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R. A. Jenner • Scientific status of metazoan cladistics
(Nielsen 2001), Neotrochozoa (Rouse 1999), or the entoprocts be placed in an unresolved position in a clade of varying membership including coelomate and noncoelomate
protostomes (Giribet et al. 2000; Peterson & Eernisse 2001).
So far, 18S rDNA sequence data have not been able to resolve
the issue. The phylogenetic position of the entoprocts is
highly sensitive to parameter variation and method of analysis (maximum parsimony or maximum likelihood) in molecular studies, and in molecular analyses entoprocts have been
united with a variety of phyla or members thereof, including
Nemertea, Annelida, Sipuncula, Echiura, Mollusca, and Ectoprocta ( Zrzavy et al. 1998, 2001; Giribet et al. 2000; Peterson
& Eernisse 2001; Jondelius et al. 2002). Analyses of combined
molecular and morphological evidence suggest that the entoprocts are at least closely related to the neotrochozoans and
nemerteans, but their exact position with respect to these taxa
is uncertain (Zrzavy et al. 1998, 2001; Giribet et al. 2000;
Peterson & Eernisse 2001).
If we focus on the most recent generation of comprehensive phylogenetic analyses (Giribet et al. 2000; Sørensen et al.
2000; Nielsen 2001; Peterson & Eernisse 2001; Zrzavy et al.
2001; Zrzavy 2003), can we determine whether these cladistic
analyses are effective tests of competing hypotheses using the
criterion of character selection? For example, let us consider
whether the sister-group relationship of Entoprocta and
Mollusca, which was proposed by Bartolomaeus (1993) and
named Lacunifera by Ax (1999), and Sinusoida by Haszprunar (2000), is properly tested in the latest studies.
Haszprunar (1996: 22) considered the existence of ‘quite
an impressive number of possible synapomorphies between
molluscs and kamptozoans [entoprocts]’ if both larval and adult
morphology are taken into account. The six chief potential
synapomorphies of the molluscs and the entoprocts suggested
by this and several other studies are the presence of a dorsal
chitin-containing proteinaceous cuticle, a pedal sole with anterior
compound cilia, pedal glands, a glandular midgut, a similar
position of the anus, and a circulatory system of sinusoidal
spaces in a largely noncoelomate body (Bartolomaeus 1993;
Haszprunar 1996, 2000; Ax 1999). These were all proposed
in the context of manual or computerized cladistic analyses of
only a subset of the animal phyla. Subsequent more comprehensive cladistic analyses are therefore ideally suited for
testing the phylogenetic significance of these characters. It
should be noted that the primary homology of several of these
characters is uncertain at best, in particular the latter two, but
here I want to focus only on the logic of character selection.
Giribet et al. (2000) used the data set compiled by Zrzavy
et al. (1998), which included most of the potential synapomorphies supporting Lacunifera, with the exception of a
glandular midgut and a sinusoidal circulatory system. Although
a character on glands in the midgut was only introduced in
Haszprunar (2000), a study that was published after the
© The Norwegian Academy of Science and Letters • Zoologica Scripta, 33, 4, July 2004, pp293– 310
analysis of Zrzavy et al. (1998), the sinusoidal nature of the circulatory system was left out of the analysis without argument.
Neither Zrzavy et al. (1998) nor Giribet et al. (2000) recovered a monophyletic Lacunifera.
The analysis by Sørensen et al. (2000) omitted most potential lacuniferan synapomorphies: pedal sole, pedal gland, anus
position, sinusoidal circulatory system, and glandular midgut.
A monophyletic Lacunifera was not recovered by this cladistic analysis. The same conclusions hold true for the cladistic
analyses of Nielsen (2001) and Peterson & Eernisse (2001).
The cladistic analysis by Zrzavy et al. (2001) excluded
characters coding for a pedal sole, anus position, glandular
midgut, and sinusoidal circulatory system without explicit
justification. A monophyletic Lacunifera was not found.
The phylogenetic analysis by Zrzavy (2003) excluded characters coding for anus position and midgut glands, again
without argument. The entoprocts were resolved as the sister
group to the Cycliophora instead.
The only potential lacuniferan synapomorphy included in
all recent analyses is that coding for a chitinous cuticle. However, the exact coding and scoring may differ among studies
so that the initial primary homology proposal may not be
maintained. For example, Zrzavy et al. (2001) and Zrzavy
(2003) code a character for the presence of a cuticle with
α-chitin, while the characters defined by Bartolomaeus (1993)
and Haszprunar (1996) disregard the specific chemical
composition of chitin in the cuticle. This leads to different
character scorings, and consequently, the phylogenetic significance of the originally defined character remains untested.
This case study makes clear that recent phylogenetic studies have not selected characters with the express purpose of
constructing an effective test of available hypotheses for the
position of the entoprocts within the Metazoa. Or, if they
have done so, the decisions underlying character selection
remain entirely hidden. The arbitrary selection of characters
becomes even more strikingly clear when we compare the
choice of characters in subsequent analyses of the same research
group. Zrzavy et al. (1998) identified nine potential synapomorphies for Entoprocta + Cycliophora which coded for such
diverse features as anus position, frequency of asexual reproduction, nervous system morphology, fate of larval apical
organ, and muscle cytology (characters 34, 73, 128, 130, 132,
148, 234, 261, 266). In contrast, Zrzavy et al. (2001) merely
included two characters comparable to characters 148 and
234 of the first analysis, whereas Zrzavy (2003) only included
character 266 as part of a more complex character. Why the
other seven characters most relevant for placing the entoprocts in Zrzavy et al. (1998) were excluded from the analysis
of Zrzavy et al. (2001), and why eight of the nine characters
are excluded from the analysis of Zrzavy (2003) is totally
unclear as they are neither mentioned nor discussed. Consequently, the change in the phylogenetic placement of the
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Scientific status of metazoan cladistics • R. A. Jenner
entoprocts and Cycliophora from Zrzavy et al. (1998) to
Zrzavy et al. (2001) and Zrzavy (2003) does not reflect any
increased understanding of phylogeny and synapomorphies.
Moreover, most of the potential synapomorphies of Entoprocta + Cycliophora found by Zrzavy et al. (1998) were not
included or explicitly rejected in other recent cladistic analyses such as Peterson & Eernisse (2001).
The power of cladistics to test alternative phylogenetic
hypotheses breaks down when potential synapomorphies
incongruent with the obtained results are left out of the analysis without justification. The largely arbitrary selection of
characters without apparent link to the testing of available
phylogenetic hypotheses is by no means unique for the placement of Entoprocta. I discuss additional examples for different phyla in Jenner (2003, in press). In these studies I show
that recent attempts at the cladistic placement of Acoelomorpha,
Platyhelminthes, Myzostomida, Nemertea, and Gnathostomulida suffer from problems caused by unjustified character
selection. A survey of the literature leaves no doubt that
uncritical character selection contributes significantly to the
existence of multiple competing hypotheses for the phylogenetic position of phyla ranging from the gastrotrichs and
brachiopods to the arthropods and tardigrades. These findings
are in agreement with the study of Poe & Wiens (2000), who
concluded that phylogeneticists seldom make their criteria
for character selection explicit.
I consider uncritical selection of characters in recent phylogenetic analyses of the Metazoa as an important factor crippling the objectivity and testing efficacy of these studies. Of
course, it would not be fair to criticize workers for not
considering all possible evidence that could bear on a phylogenetic problem. However, good scholarship necessitates
inclusion, or at least discussion, of available data treated in
previous studies. In this sense, recent phylogenetic hypotheses
are no better than the older precladistic scenarios that cladistics
was intended to supersede. Only when criteria for character
selection are made explicit with specific reference to the
hypotheses to be tested can we hope to fully exploit the rigour
of the cladistic approach to phylogeny reconstruction.
Selection of taxa
Generally, criteria for the selection of terminal taxa in analyses of metazoan cladistics vary considerably between different studies. Some authors do not justify the selection of taxa
at all, such as Nielsen et al. (1996). Peterson & Eernisse (2001)
simply stated that taxa such as Myzostomida and Lobatocerebromorpha, which had been included in previous analyses,
were excluded from the analysis. However, no reasons were
given. Others, such as Giribet et al. (2000) and Zrzavy et al.
(2001), explicitly justify taxon selection with respect to the
availability of molecular sequence information so that total
evidence analyses may be carried out. Others, such as
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Haszprunar (1996), base the exclusion of taxa on the difficulty
of relating certain of their features to those in some of the
included taxa. For example, Haszprunar (1996: 5) left the
aschelminth phyla out of his analysis because their cleavage
‘is difficult to relate to typical spiralian development.’ He
excluded other taxa, such as the arthropods, in order to ‘restrict
the scope’ of the analysis, even though several of the included
taxa were previously proposed to be related to the arthropods.
The recent studies by Rouse (1999, 2000a,b) are a particularly clear example of problematic taxon selection (Jenner
2003). Rouse used a cladistic analysis to elucidate the
evolution of trochophore larvae and the homology of larval
ciliary bands in the protostomes. It is particularly interesting
to note how Rouse treats taxa that lack trochophore larvae
and ciliary bands. These potentially pertinent phyla that have
previously been grouped with several of the included taxa are
all excluded from the analysis. This is justified by reasoning
that even if the excluded taxa were ‘placed among the taxa
selected here for study, they will have either lost the features
in question (e.g. a prototroch) or be primitively lacking
them.’ But how can we uncover convergent evolution and
character losses in this case? Obviously, such a procedure
entirely removes any power of the cladistic analysis to test the
homology and evolutionary dynamics of the features in question. Astonishingly, several recent authors (Nielsen 2001:
496; Zrzavy 2003: 66) have excluded taxa from their phylogenetic analyses because their relationships are uncertain! For
example, Zrzavy (2003) excludes Xenoturbella from his analysis
because its position is ‘still contentious.’ But what is phylogenetics all about, if not the testing of the phylogenetic placement
of taxa? Unjustified differences in data selection in recent
phylogenetic studies hinder progress in understanding, and
foster the existence of multiple opinions of uncertain merit.
Character coding and scoring: the quality of cladistic
data matrices
‘In reality the most intractable barrier to settling disputes
about systematic conclusions of a particular group of organisms usually centres on the coding of characters rather than
methods of analysis’ (Forey & Kitching 2000: 55).
Disagreement among workers on metazoan phylogenetics
is rife on many topics, but one issue stands out as universally
agreed upon: the difficulty of character coding. Character
coding and scoring are the most challenging steps in the cladistic research cycle. Character coding in metazoan cladistics
is generally perceived as posing ‘enormous problems’ (Nielsen
2001: 499). The chief difficulty is that different workers can,
and do, perceive and define characters in different ways (e.g.
Forey & Kitching 2000; Hawkins 2000). Importantly, different
coding decisions, such as to use nonadditive binary (absence/
presence), multistate, or conventional (see Hawkings et al.
1997) codes, may result in different cladogram topologies
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R. A. Jenner • Scientific status of metazoan cladistics
(Rouse & Fauchald 1997; Hawkins et al. 1997; Hawkings
2000; Forey & Kitching 2000; Donoghue et al. 2000; Rouse
2001), and different coding strategies have their own specific
strengths and weaknesses. Therefore, coding and scoring
decisions need to be carefully explained.
Because different coding strategies may produce different
results, it may come as a surprise to learn that in recent studies
of metazoan cladistics the most comprehensive and detailed
justification for the choice of a coding method is merely this:
‘[we] acknowledge that these coding issues are contentious
but feel that at the moment this [binary absence/presence
coding] is the most conservative coding scheme available’
Peterson & Eernisse (2001: 173). Because the use of binary
absence/presence coding in phylogenetic parsimony analysis
has recently been strongly criticized, this short statement
falls far short of a valid justification (Hawkins et al. 1997;
Strong & Lipscomb 1999; Hawkins 2000; Forey & Kitching
2000; Jenner 2002). In this regard it is important to note that
more than 92% of the total number of characters in the seven
most recently published metazoan cladistic analyses (Giribet
et al. 2000; Sørensen et al. 2000; Nielsen 2001; Peterson &
Eernisse 2001; Zrzavy et al. 2001; Zrzavy 2003; Brusca &
Brusca 2003) are coded as absence/presence characters
without any justification. Similarly, character scoring typically
receives equally short shrift. Discussion of the morphological
data used to build the data matrix is typically relegated to a
marginal summary in an appendix at the end of the paper. I
consider this a rather peculiar attitude towards the only
empirical lifeline of metazoan cladistics. Perhaps data matrix
compilation is, after all, more straightforward than we initially imagined. Nothing could be further from the truth.
Before I illustrate my concerns with a variety of examples,
it is important to recognize the strong effect that single changes
in a data matrix may have on the resulting phylogeny. One
might argue that as long as the percentage of errors in a given
matrix remains low, the cladistic analysis may not be fatally
weakened. I think this claim cannot be upheld. The overall
reliability of a cladistic analysis is not simply inversely correlated with the percentage of errors because a matrix does not
contain a single phylogenetic signal. A data matrix is a mosaic
of characters with distinct phylogenetic signals at different
levels. The hierarchical structuring of phylogenetic signal
implies that certain characters disproportionately determine
the placement of certain taxa rather than others. Any errors
in the set of features most important for placing a particular
phylum (or supraphyletic clade), even when they constitute
only a small percentage of the overall information content of
the matrix, will mislead us about the relationships of these
taxa. This is also to be expected given the frequently small
number of robust synapomorphies that can be identified for
uniting different phyla. Experiments in character selection,
and character coding and scoring in different data matrices
© The Norwegian Academy of Science and Letters • Zoologica Scripta, 33, 4, July 2004, pp293– 310
confirm that simple changes in data sets may have far reaching consequences for the placement of individual taxa, clades,
or even for the overall topology and resolution of the cladogram
(e.g. Rouse & Fauchald 1997; Hawkins et al. 1997; Hawkings
2000; Forey & Kitching 2000; Donoghue et al. 2000; Rouse
2001; Jenner 2002, 2003, in press; Turbeville 2002). With this
understanding, let us consider the current state of character
coding and scoring in metazoan cladistics in more detail.
Character analysis in metazoan cladistics: where is the
comparative morphology?
In a series of papers I identified many problems with the quality
of character coding and scoring in recent analyses of metazoan
cladistics ( Jenner 2001, 2002, 2003, in press). Rather than
representing occasional lapses of judgement, most of the
identified errors are symptomatic of a generally cavalier
attitude towards character study. A major aim of future
cladistic analyses of the Metazoa must therefore be the correction of the many errors through a more detailed and explicit
approach to character study. To this end I critically evaluated
the coding and scoring of more than 70 characters across all
published morphological cladistic analyses of the Metazoa to
identify the limits in our understanding of their phylogenetic
significance (Jenner, in press). I also tried to correct misscorings, and to resolve the many scoring conflicts for characters
that are shared between different studies. These efforts are
necessary steps towards a foundation for a new cladistic
analysis of metazoan relationships.
It is a striking observation that none of the recent cladistic
studies of the Metazoa comprehensively support all data
matrix entries with source citations. The ground patterns
that are scored in the published matrices are frequently very
uncertain due to scarcity of observations within a terminal,
variation of a feature within a terminal, or uncertainty about
the internal phylogeny of the terminal and its bearing on the
reconstructed or assumed ground pattern states. This does
not become obvious from the unambiguous ‘0’s and ‘1’s that
fill the data matrices. For example, the unambiguous scoring
of protonephridia for phyla such as the Acanthocephala, Echiura,
and Mollusca in recent cladistic analyses does not reflect the
ambiguity of these ground patterns. Protonephridia have
only been described for some archiacanthocephalans within
Acanthocephala, the larva of Echiurus and the dwarf male of
Bonellia within Echiura, and not for the basal molluscan taxa
Solenogastres and Caudofoveata (Conway Morris & Crompton
1982; Schuchert 1990; Dunagan & Miller 1991; Bartolomaeus
& Ax 1992; Salvini-Plawen & Steiner 1996; Rouse 1999;
Haszprunar 2000). In extreme cases, as is shown below, the
coding and scoring of characters are not rooted in observations,
but instead embody unsupported a priori assumptions about
character evolution. The requirement to cite the source for
each character scoring would force researchers to consider
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carefully each data matrix entry, and supply useful information about the robustness of the evidence underlying each
character scoring. This would constitute a marked improvement of current practice.
Here I provide additional examples of incorrect data
matrix entries that are clear illustrations that the study of
comparative morphology should be significantly improved in
future analyses of metazoan cladistics. The examples will
focus on the study of Zrzavy (2003) because it represents the
most recently published analysis of metazoan phylogeny and
had maximum opportunity to scrutinize and incorporate evidence from previous analyses. Only several characters coding
for the morphology of nervous systems will be discussed. In
the following the numbers of the characters in question will
be given in parentheses after their source.
Zrzavy et al. (1998, 2001) (238, 46), Sørensen et al. (2000)
(55), and Zrzavy (2003) (92) scored a dorsal brain or cerebral
ganglion as present in the echinoderms. However, echinoderms lack a centralized ganglion altogether (Harrison &
Chia 1994). A basic error such as this indicates that authors
do not explicitly think about each data matrix entry. Even a
casual check of a completed matrix would easily allow one to
pinpoint such errors.
Peterson & Eernisse (2001) (104) scored the tardigrades as
lacking a circumoesophageal nerve ring. However, the tardigrades do have a circumoesophageal nerve ring (Dewel &
Dewel 1996). Nevertheless, Zrzavy (2003) (95) copied this
character, including this misscoring. In addition, a circumoesophageal nerve ring is present in many other taxa, including the
nematodes, nematomorphs, gastrotrichs, priapulids, kinorhynchs, and loriciferans (Harrison & Ruppert 1991; Nielsen
2001), but neither Peterson & Eernisse (2001), nor Zrzavy
(2003) score these taxa correctly. Notably, Zrzavy (2003)
introduces logical conflict into his data set for these phyla as
he scores them at the same time as having a circumoesophageal brain (93: collar-shaped circumpharyngeal brain), and
as lacking it (95). Even though both Peterson & Eernisse
(2001) and Zrzavy (2003) score the echinoderms and hemichordates as lacking a circumoesophageal nerve ring, they do
have circumoesophageal nerves (Hyman 1955; Harrison &
Chia 1994; Benito & Pardos 1997; Nielsen 2001).
Zrzavy (2003) codes a character (96) for the presence or
absence of a ventral longitudinal nerve cord. Sørensen et al.
(2000) (54) and Nielsen (2001) (46) are cited as the sources
for this character, and the three studies exhibit identical
character scoring for the taxa that are shared between them
and that possess a ventral nerve cord. However, the character definition adopted in these latter two studies is not
identical to the one in Zrzavy (2003). Sørensen et al. (2000)
and Nielsen (2001) present a more restricted character
definition, viz. ventral nerve cords that are paired or secondarily fused during ontogeny. Consequently, the less restrictive
300
definition used in Zrzavy (2003) should be reflected in a
revised scoring, which is not the case. Many phyla are misscored as lacking ventral nerve cords. These include the
hemichordates (based upon enteropneust anatomy, which
is considered to be representative of the hemichordate
ground pattern by Zrzavy), cycliophorans (all motile stages
of the life cycle have ventral nerve cords, Funch 1996; Funch
& Kristensen 1997; Obst & Funch 2003), micrognathozoans (Kristensen & Funch 2000), and rotifers (Clément &
Wurdak 1991). Moreover, if the homology between midventrally and somewhat more laterally placed longitudinal
nerve cords is allowed (as is indicated by Zrzavy’s scoring of
Lobatocerebrum, which has more laterally placed longitudinal
nerve cords; Rieger 1980), then there is no reason to score
phyla such as Acanthocephala, Platyhelminthes and Nemertea
as lacking ventral nervous systems (Dunagan & Miller 1991;
Rieger et al. 1991; Turbeville 1991; see Jenner, in press for
additional discussion).
A unique type of brain organization is present in the introvertans sensu Nielsen (2001) (= cycloneuralians sensu Ahlrichs
1995), which comprise the nematodes, nematomorphs, priapulids, kinorhynchs, and loriciferans. Their circumoesophageal
brains are tripartite with anterior and posterior pericarya
regions separated by a middle neuropil region (e.g. SchmidtRhaesa 1996, 1997/1998; Nielsen 2001). The exception is the
brain of the nematomorphs, for which the only available
evidence indicates an equal distribution of pericarya around
the brain (Schmidt-Rhaesa 1996). Nevertheless, Zrzavy (2003)
(94) scored the nematomorphs as ‘?’ for a tripartite brain.
This scoring might be explained by Zrzavy’s assumption (p.
80) that the equally distributed pericarya in the nematomorphs may be derived from a tripartite ancestral state. However, rather than letting an unproven scenario of evolutionary
change influence character scoring, instead the only available
morphological evidence suggests the lack of tripartite brains
in the nematomorphs. Peterson & Eernisse (2001) (102) incorrectly score the nematomorphs as possessing a tripartite brain.
Zrzavy (2003) (93) scored the onychophorans as having a
collar-shaped circumpharyngeal brain comparable to that
characterizing the cycloneuralians sensu Nielsen (2001) (Priapulida, Kinorhyncha, Loricifera, Nematoda, Nematomorpha,
and Gastrotricha). However, the tardigrades are scored as ‘?’
and the arthropods as lacking this brain configuration. Zrzavy
(2003) cites the work of Eriksson & Budd (2000) in support
of this scoring. Eriksson & Budd (2000) compared the onychophoran and cycloneuralian nervous systems because they
believed that onychophorans provided evidence for the derivation of panarthropod nervous systems from less complex
cycloneuralian precursors, consistent with the Ecdysozoa
hypothesis (Dewel et al. 1999). However, the primary homologies scored in a cladistic data matrix should be strictly
grounded in morphological study, and should not be infused
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R. A. Jenner • Scientific status of metazoan cladistics
with unsupported assumptions about evolutionary pathways.
Strictly adopting morphological evidence reveals that the
onychophoran anterior nervous system is not more similar to
the cycloneuralian condition than that found in the arthropods,
tardigrades, annelids, or other bilaterians with circumoesophageal nerve rings. Accordingly, this would necessitate the
rescoring of the Onychophora.
The character scoring for the presence of an orthogonal
(ladder-like) nervous system in Zrzavy (2003) (97) shows an
even greater divorce between comparative morphology
and data matrix entry as is discussed in Jenner (in press). The
scoring of an orthogonal nervous system as present in phyla
such as Nematoda, Nematomorpha, and Priapulida can only
be explained by assuming that Zrzavy based his scoring upon
an unsupported theory of nervous system evolution that was
accepted prior to data matrix construction. These phyla do
not exhibit any signs of a ladder-like nervous system (Harrison & Ruppert 1991).
The above examples clearly show the unwarranted influence of unsupported evolutionary assumptions, which creates
a chasm between morphological evidence and data matrix
entry. The diversity and complexity of metazoan morphology
and development poses a huge challenge for systematic biologists. In order to use these data to reconstruct metazoan
phylogeny we should try to record organismic variation as
completely and as accurately as possible in our cladistic data
matrices. Therefore detailed comparative morphological
study is an absolute requirement for properly conducted cladistic research. Shortcuts are simply not available, and the
potential sensitivity of phylogenetic results to small changes
in a data matrix should inspire careful matrix construction.
Instead, a surprising degree of authoritarianism characterizes
many of the recent analyses in that opinions of other authors
are frequently uncritically accepted. That is not necessarily a
problem for certain unproblematic features, but the many
difficulties that plague the scoring of ground pattern states
for higher-level taxa make critical character evaluation essential for progress in cladistics.
The foregoing examples leave no doubt that morphological scholarship must be considerably improved in studies of
metazoan cladistics (Step 1). I will end this section by addressing
one general aspect of character coding in metazoan cladistics
that has so far not received any explicit attention at all: the
definition of absence character states.
Unspecified character states: the collapse of phylogenetic
parsimony
Sometimes a habit is so ingrained within a discipline that
potential weaknesses become invisible. I believe this applies
to an integral part of standard practice in metazoan cladistics:
the coding of characters, and specifically the definition of
absence character states. A full account of this issue is given
© The Norwegian Academy of Science and Letters • Zoologica Scripta, 33, 4, July 2004, pp293– 310
in Jenner (2002), so here I only summarize the most important conclusions, and provide some new examples.
If we focus on the character coding observed in the seven
most recently published metazoan cladistic analyses (Giribet
et al. 2000; Sørensen et al. 2000; Nielsen 2001; Peterson &
Eernisse 2001; Zrzavy et al. 2001; Zrzavy 2003; Brusca &
Brusca 2003), we see that more than 96% of the 819 characters
are coded as binary, with over 92% coded as binary absence/
presence (a / p). Only 35 are multistate. Strikingly, the absence
states in more than 40% of the total number of a/p characters
are not properly defined (up to more than 50% in individual
studies). That is, taxa scored for the same unspecified absence
state actually do not exhibit any special similarity in morphology
or development. That means that the character state is empirically empty, and this conflicts with some major requirements
of standard cladistic analysis.
First, in standard cladistic analysis character states are
alternative conditions (‘the same but different’) of the same
thing (character), that can evolve or transform into each other.
Consequently, careful morphological study is used to ensure
that character states embody precisely defined hypotheses of
primary homology. If only one state of binary a/p characters
is defined, outgroups lose their function in polarizing character state transformations. This furthermore implies that
informative character states are known prior to the analysis,
which can only lead to circular reasoning. One of the two
main goals of cladistic analysis is to reconstruct character
evolution, and parsimony analysis provides a straightforward
way to do this. A state shared between two or more terminal
taxa reflects homologous similarity if optimization attributes
that state to all nodes (stem species) lying between the terminals.
However, when character states are not defined, cladistic
analysis may teach us very little about body-plan evolution.
For example, it is impossible to determine the exact morphology of taxa lacking the presence state for character four
in Zrzavy (2003), which codes for an annelid cross. The annelid
cross is a supposedly unique configuration of cleavage blastomeres at a certain stage during the spiral cleavage of the
annelids and echiurans. The phyla scored as ‘absent’ for an
annelid cross in Zrzavy (2003) are a mix of animals for which
the cleavage pattern is: (a) unknown (placozoans); (b) known,
but not spiral and may be very different between the scored
taxa (from acoels with duet cleavage to phoronids with radial
cleavage); (c) spiral, but apparently not showing an annelid
cross (molluscs, nemerteans) (Henry et al. 2000; Nielsen
2001). The same holds true for character 5, which codes for
a molluscan cross (see Jenner 2003, for in-depth discussion of cleavage cross patterns). The coding and scoring for
these taxa of the same character state scarcely reflects any
shared similarity. To code variations of cleavage geometries
either as parts of a multistate character, or to adopt conventional coding with the proper use of ‘inapplicability’ scoring
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Scientific status of metazoan cladistics • R. A. Jenner
(Hawkins et al. 1997; Hawkins 2000), would allow one to
remove unspecified character states and resulting meaningless character state transformations.
Second, phylogenetic parsimony analysis permits evolution between character states in both directions (Farris et al.
1970; Farris 1983; Omland 1999). This assumption of symmetrical transformation allows for character reversals to be
phylogenetically informative. The failure to delimit absence
character states in binary a / p characters a priori denies the
value of reversals, and may thus lead to meaningless transformations. For example, character 97 in Zrzavy (2003) codes
for the absence or presence of an orthogonal (ladder-like)
nervous system. One of the unambiguous synapomorphies
that unites the phylogenetically problematic brachiopods and
phoronids with the deuterostomes is the reversal of this
character. However, this character reverses to a meaningless
unspecified absence state. The disparate nervous system
configurations in the sessile brachiopods and phoronids,
and in the free-living echinoderms, hemichordates and
chordates, share no features that convincingly indicate their
unique homology as an alternative to an orthogonal nervous
system. This logical inconsistency is especially pertinent
under the widely used ACCTRAN (accelerated transformation) character optimization, which favours reversals over
convergence.
Failure to properly specify all states within a character
eliminates the prime objective of coding information: to
translate original data into a coded format as faithfully as
possible without loss or gross distortion of information. This
is as much true for the coding of cladistic characters as for
the writing of codes for computer programs. With knowledge
of the coding process it should be possible to recreate the
original data from the coded information. When character
state identity is not properly specified the decoding process
becomes impossible. That is, the original data are not accurately represented by the coded data, and accordingly can no
longer be retrieved from the coded data set.
To resolve these problems, characters will have to be
recoded and / or rescored, for example either by properly
using inapplicability scoring if binary a / p coding is preferred,
or by recoding as multistate. Because all available coding
strategies have their own strengths and weaknesses, and
because not all phylogenetic software can deal with all coding
methods, it may not be possible to nominate one method as
superior to all others. However, nonadditive binary coding is
the most problematic method for standard parsimony
analysis, and its dominance in recent analyses should
therefore be reassessed. Other methods are available, and
should be explored in future studies. One can, of course,
use available programs to analyse improperly coded characters, but that does not necessarily generate meaningful
results.
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Completing the cladistic research cycle: qualitative
assessment of phylogenetic hypotheses
After the compiled data sets are subjected to a character congruence test, it is essential to evaluate the resulting phylogenetic hypotheses in terms of both topology and supporting
synapomorphies. During Step 3 of the cladistic research cycle
the relationship between evidence (data matrix) and hypothesis (cladogram) is assessed, and it is therefore only in this
phase that an increased understanding of phylogeny and
character evolution is achieved (Kluge 1998). In published
morphological cladistic analyses of the Metazoa it typically
consists of comparing the topology of the most parsimonious
cladogram(s) with that of previously published cladograms,
and clade support is only sometimes (Giribet et al. 2000;
Peterson & Eernisse 2001) assessed in terms of quantitative
support measures such as bootstrap percentages or Bremer
support values. Additionally, some authors may formalize the
established clades with new names, but unfortunately, this is
where published analyses terminate the analytical process. A
qualitative study of the character state transformations that
underlie the clades is not carried out, and if conflicting topologies between studies are identified, no attempt is made to
determine the cause of this difference. As is shown above in
relation to character selection, new topologies are simply
accepted, even when character selection has biased the results.
The succession of recent attempts to place the phylogenetically problematic myzostomids in the Metazoa is emblematic
of this problem. Their fluctuating placement in different
studies can be precisely correlated with differences in character
selection in different studies (Jenner 2003). That in itself
may not be a problem if character selection is explicitly justified on the basis of detailed character study. However, that is
not the case. For example, the traditional idea that the myzostomids are highly modified polychaetes seems to have been
refuted by the recent analyses of Zrzavy et al. (2001) and
Zrzavy (2003). However, this conclusion cannot hold because
neither of these two studies included several important
characters uniquely shared between (certain) polychaetes and
the myzostomids, including a nectochaete larva (postmetamorphic juvenile with long chaetae), aciculae (internalized
chaetae functioning as support rods inside the parapodia),
and cirri (assumed sensory organs) with a characteristic pattern
of innervation (see Jenner 2003 for references). Clearly,
biased character selection cripples the testing power of these
two studies.
In addition, recent studies make no attempt to evaluate
their cladograms in terms of character state transformations.
The most telltale sign of this problem is the prevalence of
unspecified character states in recent analyses. If only one of
the character states of a binary character is defined it is
impossible to meaningfully interpret steps on a cladogram.
Studying character changes on a cladogram makes this clear
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R. A. Jenner • Scientific status of metazoan cladistics
at once. The resulting breakdown of phylogenetic parsimony
is most clearly brought home by the existence of several character reversals to unspecified states in the studies of Giribet
et al. (2000), Peterson & Eernisse (2001), Nielsen (2001), and
Zrzavy (2003).
The value of character reappraisal after a cladistic analysis
is easily illustrated. For example, it could help provide a better understanding of the homoplasies on a preferred cladogram. In the section on character coding above I discussed
character 96 in Zrzavy (2003), which codes for the absence or
presence of a ventral longitudinal nerve cord. Optimizing
this character on either the morphological or total evidence
topologies of Zrzavy (2003) unambiguously indicates two
independent origins of ventral nerve cords in two clades of
protostomes. This is a potentially significant result because
the presence of ventral nerve cords has been regarded as one
of the most reliable characteristics of the protostomes
(Nielsen 1994, 2001). We may wonder whether this pattern
of character evolution is trustworthy. Separating the two protostome clades characterized by ventral nerve cords are four
phyla that are scored for the plesiomorphic state, viz. absence
of the cords. These are the cycliophorans, micrognathozoans,
ectoprocts, and entoprocts. The first two taxa are misscored
as they do have ventral nerve cords (see above), and rescoring
them changes character optimization such that ventral nerve
cords are now unambiguously homologous throughout the
protostomes. Furthermore, the scoring of the same character
state for such phyla as the sessile ectoprocts and entoprocts,
and the cnidarians and chordates badly misrepresents the
comparative morphology of their nervous systems. Consequently, reanalysis of this homoplastic character shows that
the favoured optimization is based upon incorrect character
scoring and coding, and the convergent evolution of ventral
nerve cords is therefore not supported.
In conclusion, by not properly completing the research
cycle, recent cladistic analyses of the Metazoa forego a precious opportunity to gain a deeper understanding of the phylogeny of animals and the evolution of their body plans.
Strengthening and elaborating morphological
data sets
Future progress in metazoan cladistics is dependent upon the
consolidation and elaboration of available morphological
data sets. First, the continual reevaluation of existing data sets
in the light of new information is an essential ingredient of
effective cladistic research cycles (Kluge 1998). In view of the
less than optimal quality of prevailing data matrices, this
approach should take centre stage in future work.
Second, the continuing search for new characters may add
valuable phylogenetic information to our data sets, which
will allow more effective tests of competing hypotheses. The
ongoing development of new techniques to study animal
© The Norwegian Academy of Science and Letters • Zoologica Scripta, 33, 4, July 2004, pp293– 310
morphology and development allows older data to be rechecked. For example, studies based on light microscopy can
now be reassessed with the use of more powerful electron
microscopical methods, and the tracing of embryonic cell lineages performed with specific blastomere injections which
allow much more reliable fate maps to be drawn (e.g. Freeman
& Martindale 2002; Gerberding et al. 2002). It is encouraging
to note that recent cladistic studies such as Peterson &
Eernisse (2001), Zrzavy et al. (2001), and Zrzavy (2003) are
incorporating new information, such as the absence or presence
of particular Hox genes, differences in the mitochondrial genetic
code, and expression patterns of developmental genes. Furthermore, new methods to visualize the details of the early development of organ systems, such as the muscular and nervous
system, generate valuable information of potential phylogenetic significance (e.g. Friedrich et al. 2002; Wanninger &
Haszprunar 2002). One area where such studies have particular
significance is in the assessment of problematic absence characters that may reflect secondary loss rather than primitive
absence (Purschke et al. 2000). For example, adult echiurans
and sipunculans are unsegmented coelomate worms, and are
undoubtedly related to the molluscs and annelids. However,
so far their exact relationships remain contentious. The absence
of obvious segmentation in these two phyla could indicate a
primitive absence, or potentially a secondary loss. Recent
immunohistochemical investigations of nervous system development in the echiurans and sipunculans indicated the metameric
organization of nerve cells along the ventral nerve cords, and
this could be taken to indicate that they are derived from
segmented ancestors (Hessling 2002; Hessling & Westheide
2002; E Edsinger Gonzales, pers. comm.). Similarly, the
myzostomids have long been considered a phylogenetic
problematicum (Zrzavy et al. 2001). A recent immunohistochemical study of their nervous system development (Müller
& Westheide 2000) revealed detailed similarities with the
nervous system of polychaetes, which is in agreement with
other available morphological evidence that suggest an
annelidan affinity (Jenner 2003).
Nevertheless, the significance of new morphological and
developmental studies can only be exploited when new
cladistic analyses take new information into account. Unfortunately, a worrying degree of authoritarianism and historical
burden remains detectable in recent cladistic analyses. Entire
data sets, or parts thereof, that are compiled by other authors
may be taken over into new analyses without attention to new
information, and earlier interpretations may be uncritically
accepted by later workers (Jenner 2001, 2003, in press). For
example, Kristensen (1991) showed that traditional reports of
the presence of a spacious pseudocoel in Kinorhyncha were
erroneous, and were instead the results of fixation artifacts.
Yet phylogenetic studies subsequently published over more
than a decade failed to incorporate this new information
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(Eernisse et al. 1992; Wallace et al. 1996; Zrzavy et al. 1998;
Brusca & Brusca 2003). Admittedly, the literature on animal
morphology and development is intimidatingly large, but we
should try our best to reflect available evidence in our data
matrices as accurately as possible.
The quest for new phylogenetic data is not easy. Apart from
being very time consuming I think that the most important
reason for this difficulty is that we find it difficult to adopt a
broad focus. We may find a distinctive similarity in a few phyla,
but our a priori preconceptions about their relationships may
lead us to believe, perhaps unconsciously, that the similarity
is convergent, and further study is thus discouraged. However,
in such cases a comprehensive comparative study could yield
useful information. For example, Ruppert (1991) noted that
the gastrotrichs show a distinctive type of neuromuscular
contact in which the muscle cells send extensions to the nerves,
a situation claimed to be similar to that found in the cephalochordates, nematodes, and nemerteans. A preliminary
survey of the literature shows that the entoprocts and
nematomorphs exhibit similar neuromuscular contacts. This
shows that a comprehensive focus is necessary if the aim is to
elucidate the phylogenetic significance of a character.
That, however, is not always done. Examples of not carrying
out a sufficiently wide-ranging comparative study after finding a potentially promising character can be found throughout
recent data matrices. Noteworthy examples are related to clades
that were recently proposed, or recently received a new name.
For example, Zrzavy et al. (2001) proposed the name Prosomastigozoa to house the problematic myzostomids mentioned
above. They were placed in a new clade together with Cycliophora
and Syndermata. Prosomastigozoa refers to the supposed
unique possession of sperm with flagella that attach anteriorly
to the sperm body, and which curve posteriad. However, similar
sperm have been described for the chaetognaths and phoronids,
as well as for the aberrant echinoderm Xyloplax, but this information was not mentioned in Zrzavy et al. (2001) or Zrzavy
(2003) (Alvario 1983; Rowe et al. 1991; Herrmann 1997).
In similar vein, Ax (1999) proposed the new name Lacunifera for a clade composed of Entoprocta + Mollusca (see also
section on character selection), which was initially proposed
by Bartolomaeus (1993). Haszprunar (1996) suggested the
presence of a circulatory system composed of sinuses and
lacunae as a unique synapomorphy of the molluscs and
entoprocts. This conclusion was supported by a later study, in
which the clade was christened Sinusoida (Haszprunar 2000).
However, the studies of Haszprunar only included a restricted
set of phyla, and the subsequent study of Zrzavy (2003)
included both this character (character 76) and a much
broader sampling of taxa so that the true phylogenetic significance of a lacunar circulatory system could now be tested.
Unfortunately, Zrzavy evidently did not look beyond the
morphology of the molluscs and entoprocts.
304
A lacunar system is composed of widened interstitial spaces
between the cells and organs that fill most of the space
between the gut and the epidermis. It may be contrasted with
a circulatory system with well-defined vessels that are typically located between the basement membranes of epithelia,
for example between coelomic epithelia in the mesenteries
of coelomate animals, or between the coelomic epithelium
and the gut epithelium. These distinctions are grounded in
ultrastructural data, but they have been referred to for a long
time by their textbook names, viz. ‘open’ or ‘closed’ circulatory systems (Hyman 1951). Any system of interstitial spaces
between internal organs not directly bounded by the basement membranes of epithelia answers the definition of a lacunar system. Therefore one can label all interstitial spaces in
noncoelomate bilaterians, as well as particular regions of the
body in coelomate animal lacunar systems. Yet Zrzavy (2003)
only scores a lacunar system present in the molluscs and the
entoprocts, and although both Haszprunar (1996) and Zrzavy
(2003) included Lobatocerebrum in their analyses, neither of
them properly scored it as having a lacunar system, which was
clearly described in the first paper on this taxon (Rieger 1980).
In conclusion, I believe that no matter how hard we try to
be open minded, preconceived notions of what we think
could be important and what is not, will always affect our
choice of characters and taxa, consciously or not. To make the
study of character selection, coding, and scoring explicit is
therefore a first prerequisite of a scientific approach to cladistic analysis. Especially when a character shows a distribution
that conflicts with a previously proposed phylogeny, it is
likely to be excluded from the analysis. The effect of such a
priori constraints on data selection are clearly shown in recent
debates about the phylogenetic position of the turtles and the
snakes (Lee 1995; Lee & Doughty 1997, 1998; Rieppel &
Reisz 1999). Here, important breakthroughs in the understanding of the evolution of snake and turtle body plans are
correlated with the inclusion of previously ignored characters
and taxa into new cladistic analyses. The vigour of cladistics
as a falsificationist research program is inextricably linked to
finding incongruent characters (Kluge 1997). If available disconfirming evidence is excluded from cladistic analyses without justification, cladistics loses its testing power. The search
for characters incongruent with proposed hypotheses will
help progress in cladistic research as much as finding confirming evidence of established hypotheses.
Metazoan cladistics as a research program:
reconsidering current research strategies
Cladistic analysis is a powerful method to tap the extensive
body of morphological and developmental information about
the Metazoa that has been compiled over more than a century. Molecular systematics is a major driving force of recent
progress, but robust morphological data sets can offer a lot of
Zoologica Scripta, 33, 4, July 2004, pp293 – 310 • © The Norwegian Academy of Science and Letters
R. A. Jenner • Scientific status of metazoan cladistics
additional information, especially for resolving relationships
within the large clades of the Bilateria where molecular signal
is weaker. Obviously, if we want to understand the dynamics
of animal body-plan evolution at all levels of the biological
hierarchy, then a reliably compiled morphological data set is
invaluable. To conclude, let us summarize recent progress in
metazoan cladistics for each of the steps in the cladistic
research cycle.
To start with Step 2, the automated testing of all possible
cladograms for a given data set, there is no doubt that this is
where progress in metazoan cladistics is the most visible. The
availability of increasing computing power, and the continuing
development of increasingly efficient phylogenetic software
make phylogenetic analysis of large morphological, molecular,
or combined data sets possible, and these are obviously positive
developments. Technological advances have allowed metazoan phylogenetics to become a blossoming discipline at the
heart of modern integrative biology. However, although
technological advances have repeatedly proven to be positive
driving forces of scientific progress throughout the history of
science, this relationship hides an inherent danger. For example, Lewontin (1991) called the development and widespread
adoption of gel electrophoresis in evolutionary genetics from
the mid-1960s onward both a ‘milestone’ and a ‘millstone.’
‘The introduction of protein gel electrophoresis as a tool to
investigate the standing variation within and between species
almost totally depauperized evolutionary genetics for 20 years’
(Lewontin 2002: 7). The enormous outpouring of data based
on gel electrophoretic studies did not, however, resolve the
many problems that earlier research in population biology
dealt with. This illustrates that the uncritical embrace of a
technological advance may lead to an unwarranted ‘find ’em
and grind ’em’ mentality, yielding plentiful results, the significance of which may remain uncertain at best. Recently,
concern has been aired about whether the increasing use of
computers in different fields of biological research may be
diverting our attention away from attempts to really understand the generated data (Allen 2001). Likewise, we should be
vigilant not to overemphasize Step 2 at the expense of the
other essential steps of the cladistic research cycle. Computers
have assisted greatly in harvesting phylogenetic signal from
available data sets, yielding many phylogenetic hypotheses.
However, it is now obvious that we need to redirect our attention to the primary data of our trade if we are to continue the
momentum of this discipline. Computers are an aid to thinking;
they should not replace it.
Step 1, or all the science that goes into the construction of
a cladistic data matrix could benefit from much more explicit
attention. As pointed out above, the selection, coding, and
scoring of characters are never explicitly justified, or discussed
in any comprehensive way. As an unfortunate result, we can see
that even the most recent morphological and total evidence
© The Norwegian Academy of Science and Letters • Zoologica Scripta, 33, 4, July 2004, pp293– 310
studies exhibit many disagreements; at this time it is simply
impossible to make a reasoned choice between these competing hypotheses. For that, we first need to address the many
problems identified here and elsewhere.
Likewise, Step 3, or the assessment of the relationship between evidence and hypothesis after the most optimal tree(s)
is found, is hardly visible at all in recent studies. As a result,
many problematic character state transformations remain hidden, thus removing the logical foundation upon which cladistic
analysis rests. I think it is a striking finding that exactly those
steps of cladistic research that require the greatest intellectual
effort are the ones that are in the most pressing need of
explicit attention. The late Sir Peter Medawar had the following general insight: ‘the scientific paper is a fraud in the
sense that it does give a totally misleading narrative of the
processes of thought that go into the making of scientific
discoveries’ (Medawar 1996: 38). This characterization is particularly apt for recent papers on metazoan cladistics, where
most steps that involve thought and decision making are
neatly concealed in the black box of the data matrix. The
empirical data underlying the analysis are typically presented
only within a short table or appendix. This attitude towards
the only empirical data of our trade is simply incomprehensible. Because we all agree on the methods used in Step 2, all
prevailing disagreements have their origins in differences
residing in the data sets that we employ. Therefore we have
no choice but to explicitly confront all the difficulties of Steps
1 and 3 if we are to make any real progress.
A cladistic research program can be visualized as a succession of research cycles. The goal of the first research cycle is
to generate an initial phylogenetic estimate of a group of
organisms. Because at this stage we are not yet confronted
with competing hypotheses, the first rotation through the
research cycle is a straightforward process. However, as we
enter into subsequent research cycles, the process becomes
more difficult, for now we have to take previous efforts explicitly into account. That is, at this moment the role of cladistic
analysis shifts from proposing a phylogeny, to the testing of
alternative hypotheses. Cladistics is particularly suited for the
testing of alternative phylogenetic hypotheses, but testing
can only be efficiently achieved if care is taken in the compilation of the data set. Data must be selected very carefully
with respect to the hypotheses to be tested so as not to bias
the results of the analysis, and the differences between previous
and new data matrices have to be carefully compared.
Therefore I think that the transition between the first and
second research cycles is the most crucial point in a cladistic
research program, and so far we have not yet fully completed
this transition.
Encouragingly, there is evidence of progress in that recent
studies identify and resolve some previous scoring mistakes,
and weed out some bad characters, although this essential
305
Scientific status of metazoan cladistics • R. A. Jenner
process is never the explicit focus. I think that current efforts
constitute a more or less parallel series of first cycles that
often generate conflicting results, and which are not efficiently linked to each other even though the analyses have
been published in sequence over more than a decade. This
situation is perhaps not too surprising as computers fostered
the quick and easy exploration of multiple data sets. Now we
need to refocus on the primary data of our trade, which is
unfortunately a much more time-consuming process. The
published studies show a plethora of differences that are not
made explicit. Consequently, it becomes virtually impossible
to separate the arrow of true progress in understanding from
random change of opinion. However, we should not be
discouraged. The incomplete research cycles offer plentiful
frayed ends to start a new round of research. Now is the time
to pick them up and tie them together into a powerful
research program.
Seeds for revision
I here provide a barebones recipe that may be helpful for
improving future cladistic analyses of the Metazoa. For the
three steps of the cladistic research cycle I minimally propose
the following:
Step1
1 Select terminal taxa so that all previously proposed sister
groups of all the included terminals are included. Any
exclusions from this minimal set should be explicitly justified.
Selection should also be considered with respect to the
domain of definition of each included character. I adopt a
modified version of the domain of definition as proposed by
Dayrat & Tillier (2000): all taxa for which the character is
applicable. A failure to fulfil the domain of definition of a
character, i.e. restrictive taxon sampling, compromises the
reliability of the phylogenetic significance ascribed to that
character, so that it may be a symplesiomorphy or homoplasy
rather than a unique synapomorphy.
2 Select all characters that have previously been proposed in
support of all alternative sister-group hypotheses for all
included terminals. Any exclusion from this set of characters
should be explicitly justified. In addition, new characters may
be included.
3 Explicitly define all characters and character states so that
character state transformations can be meaningfully interpreted
on the resulting cladograms. The nature and number of character
states within a given character will have to be based upon a
careful comparative study of morphological variation. The
source of each data matrix entry should be supplied.
Step 2
The computer-assisted simultaneous assessment of all possible
relationships between the selected terminals will yield one or
306
more most parsimonious cladograms for the given data set.
These provide the best explanation of similarities as due to
common descent with modification with a minimal requirement
for ad hoc explanations of homoplasy.
Step 3
1 Perform quantitative clade support analysis (e.g. bootstrap
and Bremer).
2 Provide qualitative evaluation of clade support, such as the
reappraisal of character state identity and character state transformations, and reevaluation of homoplasies. A sensitivity
analysis can be performed in which contentious character
codings and scorings are changed to assess the effect of different
input assumptions on the result of the cladistic analysis. The
sensitivity analysis is an appropriate point to start a new
cladistic research cycle.
Epilogue: lessons from history, from sociobiology to
evolutionary morphology
A comparison of current practice in metazoan cladistics with
the operation of several other evolutionary disciplines during
the history of biology can teach us something important
about the scientific status of recent efforts. The mainstay of
all science, including evolutionary science, is testability. The
efficient operation of a falsificationist research program
depends on the formulation of alternative hypotheses, which
can be tested against each other by the performance of an
experiment or study with alternative possible outcomes. However, it is not enough to merely state the possibility of testing.
For cladistic research this means that all proposed sistergroup hypotheses of the taxa under consideration have to be
identified, and then a data matrix that includes all available
potentially corroborating and disconfirming evidence for all
these hypotheses has to be compiled. The simultaneous
assessment of all these data will then yield the best-supported
phylogeny.
Another strategy that is sometimes used in science is verificationism. At the heart of the verificationist approach is the
use of evidence only to make a persuasive case for a particular
hypothesis. Wilson (2000: 28) called it the ‘advocacy method
of developing science’ as it depends upon the careful selection
of only that evidence that corroborates a particular hypothesis.
For example, in sociobiology myriad theories have been proposed to explain the evolutionary origins of many aspects of
social behaviour in different animal groups. By focusing on
different restricted sets of evidence, authors have come to
radically different conclusions, without it becoming clear which
of the proposed hypotheses is a superior summary of available
evidence. At its worst this practice amounts to nothing more
than speculative storytelling, in which different ‘schools’ of
thought proceed to talk past each other. Consequently
Wilson (2000: 28) claimed that ‘the greatest snare in
Zoologica Scripta, 33, 4, July 2004, pp293 – 310 • © The Norwegian Academy of Science and Letters
R. A. Jenner • Scientific status of metazoan cladistics
sociobiological reasoning is the ease with which it is conducted’ and concluded that ‘sociobiologists of the past have
lost control by their failure to discriminate properly among
the schemes.’ In similar vein, Gould & Lewontin (1979) took
issue with the prevalence of uncritical adaptive storytelling in
evolutionary biology. They pointed out that often the sole
criterion for accepting an adaptive explanation for the origin
of a given organismic feature was the mere plausibility of the
hypothesis. The general weakness of such reasoning identified by Wilson, Gould, and Lewontin is that no attempt is
made to make a clear distinction between the possible or
plausible alternative hypotheses. Too often, workers are willing to uncritically accept a hypothesis erected on the basis of
only part of the available evidence.
Current practice of metazoan cladistics shows some
remarkable similarities to early sociobiological reasoning and
adaptive storytelling. The first generation of metazoan cladistics saw the erection of many alternative phylogenetic
hypotheses as independent research groups analysed data sets
which differed in many details that were not made explicit,
notably character selection. Subsequent analyses were not
expressly designed to test previous efforts, creating a forest of
phylogenies of uncertain merit. Of course, I do not imply that
workers consciously massage their data to generate preferred
results, but an unconsciously introduced bias in input data
has the same result. This is akin to early sociobiological and
adaptive scenarios, which were proposed on the basis of part
of the available evidence, and without the intention to critically test alternative views. A cladistic hypothesis based on an
uncritically compiled data set is just one possibility among
many other plausible outcomes. Only critical simultaneous
assessment of all pertinent information will allow one to test
alternative phylogenies. Moreover, the uncritical attitude
towards character coding and scoring seriously undermines
the quality of our data matrices. If this practice does not
change, we are in danger of recapitulating the fate of the first
generation of phylogeneticists.
The reconstruction of large-scale phylogenies was the
focus of the first evolutionary biologists in the period immediately following the publication of Darwin’s On the Origin of
Species. However, ‘by the last decade of the nineteenth century, their approach was already seen as a wasted effort, since
the evidence stubbornly refused to admit clear evaluation of
the various schemes which had been proposed’ (Bowler 1996:
443). Nyhart (1995, 2002) concluded that the first phylogenetic zoology largely dissolved from within because the conflicting results from comparative anatomy and embryology
could not be reconciled. The evolutionary morphologists
were simply unable ‘to account satisfactorily for contradictory evidence’ (Nyhart 1995: 276). The result was a marked
decline in the attraction of promising young investigators to
the phylogenetic enterprise. To prevent the same situation
© The Norwegian Academy of Science and Letters • Zoologica Scripta, 33, 4, July 2004, pp293– 310
recurring today, we have to abandon the use of cladistics as an
easy tool to generate ‘new’ hypotheses and instead employ it
more critically in the testing of existing ones. In the end, we
may not be able to fully resolve all relationships within the
Metazoa, but only by a proper use of cladistics will we be able
to tell whether we have pushed the morphological evidence
to its limits.
Acknowledgements
I want to thank Eric Edsinger Gonzales for kindly sharing
unpublished information about nervous system development
in sipunculans, and Matthias Obst for discussing cycliophorans. Drs Malte Ebach, Ariel Chipman, Max Telford and an
anonymous reviewer provided incisive comments on the
manuscript. This work is supported by a Marie Curie Individual
Fellowship of the European Community program ‘Improving Human Potential’ under contract number HPMF-CT2002–01712.
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