Contributions to Zoology, 71 (1/3) 67-91 (2002)

SPB Academic Publishing bv, The Hague

Boolean logic and character state identity: pitfalls of character coding in metazoan cladistics

Ronald+A. Jenner

Institute for Biodiversity and Ecosystem Dynamics, University of Amsterdam, Mauritskade 57, 1092AD

Amsterdam, The Netherlands. Present address: University Museum of Zoology, University of Cambridge,

Downing Street, Cambridge CB2 3EJ, United Kingdom

character character Boolean Keywords: metazoan cladistics, Metazoa, coding, state identity, logic, non-

additive binary coding, absence/presence coding

Abstract Reconstructing body plan evolution with Boolean logic:

narrating history without looking back 75

When becomes congruence meaningless: unspecified A critical study ofthe morphological data sets used for the most “absence” states and uninformative character of rather recent analyses metazoan cladistics exposes a cava- reversals 77 lier attitude towards character coding. Binary absence/presence Reasserting the central role of comparative morphology is but without This coding ubiquitous, any explicitjustification. in metaz'oan cladistics 79 uncompromisingapplication ofBoolean logic in character coding

■ Conclusions 83 is remarkable since several recent investigations have nomi- Acknowledgements 84 nated absence/presence coding as the most problematic coding References 84 method available for standard cladistic analysis. Moreover, the in Appendix: unspecified “absence” states metazoan prevalence ofunspecified “absence” character states in the pub- cladistics 87 lished data sets introduces a discrepancy between the theoreti-

cal foundations ofphylogenetic parsimony and current practices “For evolutionary biologists, characters transform from one in metazoan cladistics. Because phylogenetic parsimony assumes condition into another.” Kitching et at., 1998, p.25. transformation of character states, its effective operation breaks

down when not all character states are carefully delimited. Ex- amples ofresulting meaningless character state transformations Introduction are discussed in two categories: 1) when unspecified “absence”

states are plesiomorphic; and 2) when unspecified “absence”

states To facilitate are apomorphic (character reversals). future The self-evident fact that the structure of the data

progress in metazoan cladistics, the mandatory link between matrix determines the outcome of a cladistic analysis comparative morphology and character coding needs to be re- hardly needs mentioning. Data matrix construction established through a more explicit study ofmorphological vari- is also the difficult ofa cladistic ation arguably most step prior to character coding, and through a more explicitly and experimental approach to character coding. analysis, it is the only anchor that connects a

cladogram to the empirical world. However, a re-

markable paradox of cladistic practice in metazoan

Contents phylogenetics then becomes apparent. This most

important and difficult aspect of cladistic analyses

Introduction 67 has received surprisingly little explicit attention, ( Some fundamentals of phylogenetic parsimony: either theoretical or practical, since the first com- primary homology, transformational homology, and puter-assisted morphological cladistic analyses of character state identity 68 the animal kingdom were published over a decade the world Boolean the Seeing through eyes: prevalence ago. This observation becomes especially striking of binary character coding in metazoan cladistics 69 when the lack of attention A/p coding and metazoan cladistics: generalproblems 71 one compares explicit The failure of Boolean logic: character state identity directed towards construction of a robust morpho-

and character in unspecified “absence” states logical data set with the intensive efforts to extract

metazoan cladistics 73 phylogenetic signal from a given matrix.

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character in Several authors have noted a general trend in ing on coding the five most recently

of the Metazoa that: contemporary phylogenetic research where an in- published cladistic analyses

data set crease in the emphasis on the phylogenetic analy- 1) used a morphological (sometimes part

of total evidence and most sis of a given data set is paralleled by a decrease a analysis), 2) sampled Giribet al. in the explicit attention directed towards construct- of the major animal taxa: et (2000) (based Sorensen ing that morphological data set (Grande & Bemis, on the data set ofZrzavy et al., 1998), et

Peterson & 1998; Poe & Wiens, 2000; Rieppel & Kearney, al. (2000), Nielsen (2001), Eernisse

and et al. This for the 2002). This imbalance between two necessary as- (2001), Zrzavy (2001). paper

time the critical issue of whether pects ofcladistic analyses (character definition and first addresses of characters in phylogenetic analysis) is succinctly epitomized by current practice in the coding meta- theoretical the most recent comprehensive study of higher-level zoan cladistics is consistent with the

molecular of arthropod relationships based upon both underpinnings phylogenetic parsimony analysis.

and morphological data (Giribet et al., 2001). The

authors found it worth mentioning that they per-

formed 120 independent phylogenetic analyses by Some fundamentals of phylogenetic parsimony:

varying sets ofparameters and datapartitions, “exe- primary homology, transformational homology,

2 cuted in parallel in the 256 processors, totaling and character state identity

months of intense computation time using extremely

be charac- effective tree search algorithms and an aggressive First, some terms need to defined. By

42 I of search strategy, equivalent to years of comput- ter coding mean the definition (delimitation)

in sin- character its character the ing time if analyses had to be conducted a a and states, i.e., con-

in gle-processor machine.” Nevertheless, not a single struction of columns a data matrix. By character

cladistic character or character state transformation scoring I mean the assignment of different character

of the is mentioned in their paper! Instead, the characters states to the terminal taxa, the filling in

data matrix. authors are listed only in a supplementary appendix that columns of a Many designate

character Both can exclusively be accessed online. both these steps as coding. steps

be rather rooted in careful This imbalance may in some instances a should be morphological study.

limitations in the selection of characters be understood as harmless reflection of space me- The can

be character well Jenner dium chosen to report the results, as may ex- an aspect of coding as (see

pected for the comprehensive study of arthropod & Schram, 1999, and especially Jenner, submitted,

relationships of Giribet et al. (2001). However, in for discussions of character selection in metazoan

other cases, the imbalance may signal a problem cladistics).

in data it is to summarize the funda- the quality of the compiled morphological Second, necessary

the mental set. Serious concerns about quality of cladistic assumptions of phylogenetic parsimony anal-

data matrices traverse a broad spectrum of taxa; ysis in order to appreciate the merit of currently

these include parasitic flatworms (Rohde, 1996), adopted character coding schemes in metazoan cla-

hydrozoans (Marques, 1996), crustaceans (Watling, distics. At this point the reader should note that the

1999; Fryer, 1999, 2001; Olcsen, 2000), arthropods following selective references to the literature on

(Shultz & Regier, 2000; Schram & Jenner, 2001), the theoretical foundations of cladistics are not

reptiles (Lee, 1995; Rieppel & Reisz, 1999; Rieppel meant to be anything close to comprehensive, in-

& Zaher, 2000; Rieppel & Kearney, 2002), fishes stead I focus chiefly on the most recent discussions

(Patterson & Johnson, 1997; Grande & Bemis, and syntheses.

and Jenner & The first in cladistic 1998), metazoans (Nielsen, 1998; very step any morphological

in Schram, 1999; Jenner, 2001, submitted). This ar- analysis is a study of morphology/anatomy a

ticle addresses this problem in detail for cladistic comparative framework to identify comparable fea-

of the basis analyses Metazoa. tures in different taxa on the of conjectures

In the I will the following, critically review cur- of similarity (De Pinna, 1991; Brower & Scha-

rent practice of data matrix construction by focus- waroch, 1996; Hawkins et al., 1997; Rieppel &

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This establishes Kearney, 2002). study so-called treated as such hy- by computer-assisted cladistic analy-

potheses of that and primary homology are codified as ses, since cladograms are constructed and eval-

characters and character in a cladistic data states uatedon the basis of character state transformations,

matrix. The aim of character it coding is to represent is crucial to precisely delimit and definealternative

as as observed accurately possible organismic vari- character on states the basis of careful morphological

ation in a format to amenable cladistic analysis. This In other in to study. words, order represent mor- is the foundationofall computer-assisted cladistic phological variation as accurately as possible, and of analyses metazoan morphology to date in order to able to published be meaningfully interpret char- that employ phylogenetic parsimony analysis, also acter state transformations within the context of known variously as standard cladistic analysis or transformational it homology is crucial to properly phylogenetic systematics. In the context of phylo- establish character state identity (Brower & Scha-

genetic parsimony analysis, a character is defined waroch, 1996). Careful study of morphological

as a set of attributes or alternative conditions called similarity (Patterson, 1982; Hawkins et al., 1997;

character states that between vary taxa, are con- Hawkins, 2000; Rieppel & Kearney, 2002) is im- sidered as “the same but different” forms of the same for perative constructing character states that cor-

thing (character), and can evolve or transform into respond to precisely defined primary homology each other Brower & Schawaroch, Haw- (e.g., 1996; conjectures. The characters states of all characters

kins et al., 1997; Hawkins, 2000; Maddison & submitted to standard cladistic analysis need to be

Maddison, 2001). This establishes a framework of carefully delimited, irrespective of whether the that forms the transformational homology concep- coded characters are binary or multistate. tual basis ofall used widely phylogenetic so parsimony Having represented the universally accepted software, such as PAUP (Swofford, Hen- theoretical 2002), foundations of phylogenetic parsimony, and nig86 (Farris, 1988), MacClade (Maddison & it becomes ask whether necessary to current prac-

Maddison, 2002). All metazoan cladistic tices of character analyses coding in metazoan cladistics are

discussed herein employ these The consistent with the programs. pre- assumptions of cladistic parsi- sumed of cladistic characters independence (Emer- mony.

son & Hastings, 1998) therefore contrasts with the

potential of evolutionary transformation between

character within states a character. Accordingly, the world Seeing through Boolean eyes: the

phylogenetic parsimony is implemented by the character prevalence of binary coding in of character state counting transformations (steps) metazoan cladistics

on a cladogram aimed at minimizing ad hoc hy-

potheses of homoplasy (not the minimization of Coding morphological variation for use in a cla- natural such processes as evolutionary change, as distic of the analysis animal phyla [I use the term claimed by some; Kluge, 2001). “phylum” as a general descriptor of higher-level Out-group comparison is the accepted and uni- taxa without any Linnaean rank connotations] is used method for versally polarizing character state beset with difficulties, leading at least one author transformations, and it is employed in all analyses to exclaim in apparent desperation that the “choice of metazoan cladistics considered here. This logi- and i.e., of characters interpretation, coding, pose cally implies that prior to the phylogenetic analy- enormous problems”, and that the “the choice and sis, the plesiomorphic and apomorphic character definition of taxa and choice and coding of char- states remain unknown. Thus “all shared, identi- become acters a complete quagmire.” (Nielsen, cal character states represent conjectures ofpotential In 2001; 499). view of these despairing remarks, and homology, count as evidence in phylogenetic it is natural only to expect that cladistic data ma-

analysis, even if they are subsequently discovered trix has compilation received ample explicit at- to be symplesiomorphic” (Brower & Schawaroch, tention to ensure that the data maximally reflects

267-268). Since all identified character states variation observed in organisms. As will be dem- aie potentially phylogenetically informative and arc onstrated here, the reality is quite different.

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with variations Table 1 summarizes the character Typically we are presented upon adopted co- the minimally transparent statement that morpho- dings across the five studies considered here. One logical characters “were compiled from the phy- is immediately impressed by a strong predilection

is logenetic literature” (Zrzavy et ah, 1998: 251). A for Boolean logic. Boolean logic a useful tool

section of the discusses for the of and it is larger paper subsequently ordering diversity, widely ap- aspects of cladogram construction, and finally the plied in structuring a wide range of phenomena,

and items. Boolean is resulting topology is compared to topologies sup- including concepts logic a

of ported by other analyses. Strikingly, none of the symbolic logic system based on a form algebra five cladistic analyses of metazoan morpholo- in which values or statements are reduced to be-

in the millennium either true or and it functions means gy published new provided any ing false, by

the of which balanced justification for their choice of coding of Boolean operators, most familiar method. For example, Giribct et ah (2000) simply are AND, OR, and NOT. These operators are es-

the data of et ah sential for the of recycled set Zrzavy (1998), thereby proper operation digital comput- incorporating several important shortcomings of the ers, and they are habitually used, for example, to data matrix of the latter into a new phylogenetic structure the actions ofsearch engines on the inter- analysis (Jenner, 2001). At most, a statement was net. The simplest form of Boolean logic is a bi- offered that choice of method had in fact each of which have value a coding nary set, component can a been Nielsen but for the of “0” or “1.” The characteristics of Boolean made, e.g., (2001), most alge- part adopted character coding strategies are never bra that make it so useful for representing complex convincingly defended with explicit reference to command strings in computing, also make it suit- the known strengths and weaknesses of different able for representing the diversity of metazoan coding techniques. The most comprehensive and morphology in a manner amenable to computer detailed justification for the choice of a coding analysis. It is, therefore, perhaps not so surprising method is given in Peterson & Eemisse (2001: 173), to find that the great majority of characters employed who “acknowledge that these coding issues are in cladistic analyses of the animal phyla are coded

the contentious but feel that at moment this [binary according to simple Boolean logic, i.e., as binary absence/presence coding] is the most conservative characters (96.4% of the total number of charac- coding scheme available.” The reader, however, is ters), and 92.1% of these binary characters are coded left guessing as to why this should be so. This as absence/presence (a/p) characters. This contrasts relative of fundamental of with the of of the chief neglect a aspect meta- sharply statement one pro- zoan cladistics is unjustified in view of the insights ponents of a/p coding in cladistics: “Consistently yielded by more than a decade of theoretical and applied a/p coding is rarely seen” (Pleijel, 1995: experimental studies into the logic of character 313). coding (Pimentel & Riggins, 1987; Pogue & Micke- The percentage of characters coded as a/p in vich, 1990; Pleijel, 1995; Wilkinson, 1995; Hawkins, metazoan cladistics is also much higher than that et ah, 1997; Scotland & Pennington, 2000). observed for a variety of matrices published in

Table I. Character five since the 2000. The table absolute coding across morphological data matrices published year summarizes numbers of characters and their relative percentages coded by one of three methods: binary a/p =absence/presence; binary p.h. = binary with paired homologues; multistate. See text for discussion.

Studies Binary a/p Binary P.H. Multistate Total/study

Giribet et al. (2000) 223 (80.8%) 42 (15.2%) 11 (4.0%) 276

Sorensen et al. (2000) 64 (97.0%) - 2 (3%) 66

Nielsen (2001) 64 (100%) - - 64

Peterson & Eemisse (2001) 129 (93.4%) - 9 (6.6%) 138

Zrzavy et al. (2001) 56 (93.3%) 4 (6.7%) - 60

Total across studies 536 (88.7%) 46 (7.6%) 22 (3.6%) 604

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botanical journals (less than 1% of 1404 charac- of metazoans considered here necessarily operate ters in 34 matrices is coded strictly as a/p) as re- within a framework of transformational homology, viewed in Hawkins (2000). the distinction between a taxic and transformational

This for character preference binary coding, espe- approach to homology needs to be outlined in some

order cially a/p coding (non-additive binary coding), and detail in to unveil a number of serious short-

the seeming reluctance to code multistate charac- of comings character coding in theserecent analy-

ters to the represent diversity of metazoan morphol- ses of metazoan cladistics.

is typical for cladistic of the animal ogy analyses The logical justification for a/p coding in cla-

phyla in general, such as Schram distic (1991), Eernisse analysis is outlined in Patterson (1982), who

et al. (1992), Nielsen et al. (1996), and Wallace et advocated a taxic approach to homology with the

al. (1996). However, do exist. Hasz- of exceptions express purpose using homologies to find mono-

prunar (1996a), for example, coded 1 1 out of 40 phyletic groups. Patterson’s taxic approach to ho-

characters multistate and & Fau- (27.5%), Rouse mology should not be confused with the “taxic” chald (1995) coded 4 out of 13 characters to (30.8%) approach evolutionary theory as formulated earl- multistate. ier by Eldredge (1979), which marries the taxic and

Can we identify a general reason for this remark- transformational components of Patterson’s logic able preference for binary character in me- (Farris “Taxic” in this coding et ah, 2001). paper strictly tazoan cladistics? Is the universal preference for refers to Patterson’s conceptualization. Patterson

binary character in contrasted the coding, particular a/p coding, taxic approach with a transforma-

defensible within the of context standard parsimony tional approach to evolution, which is concerned

Is analysis? the choice of a particular method with of coding evolutionary change characters. Although

for the outcome of cladistic inconsequential a analy- Patterson (1982: 36) admitted that “the transfor-

sis? What is the effect of for mational employing a/p coding approach to homology may be more in-

the interpretation ofcharacter state transformations and formative a lot more interesting than the taxic in the of the evolution study ofanimal body plans? he nevertheless advocated the taxic approach,” per- The following to some answers because attempts provide spective “concentrating on transformations to these at the questions. expense of taxa is not fruitful” (p. 36). In-

terestingly, this led to Patterson’s explicit denial

of a between taxic relationship homology and evo- and cladistics: A/p coding metazoan general lutionary change: “If phylogeny has to be about problems evolution, homology has nothing to contribute to

it” (Patterson, 1982: 67). This is in stark contrast The five most cladistic to the of recently published analy- logic phylogenetic parsimony as outlined ses of the Metazoa three distinct kinds which is employ of above, concerned with nothing if not the character coding: recovery of the evolutionary history of life. 1) Under binary a/p coding (non-additive binary coding) the taxic perspective to homology a distinc-

(536 characters) tion can be made between the complement relation

2) binary coding with char- of the of paired homologues (46 homologues, i.e., presence a homologue

acters) its versus absence, and the presence of paired ho- 3) multistate (22 coding characters) mologues, i.e., homologues present in two or more

distinct forms (Patterson, 1982; Carine & Scotland, The distinction between binary a/p characters and 1999; Scotland, 2000a). The complement relation binary paired homologue characters is the basis (categories 1 of binary a/p coding, while the paired a 'id 2 is above) not important in the context of homologue relation underlies the logic of binary transformational in homology used standard cla- paired homologue coding, as well as multistate distic but it becomes crucial if analysis, a taxic view coding. The distinction between the complement of homology is adopted (Carine & Scotland, 1999; relation and the paired homologue relation is im- Scotland, 2000a). Although the cladistic analyses portant under a taxic approach to homology because

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of character carries cladistics indicates that than only presence a (state) poten- more 40% (see Ap- tial phylogenetic weight (Carine & Scotland, 1999; pendix) of the included a/p characters have prob-

Scotland, 2000a). This means that in a/p charac- lems with character state identity of“absence” states. ters the “absence” character state is empirically A/p coding is perfectly legitimate when the goal

and is defined is whether feature is absent empty, consequently not strictly as to express a simply or a character state, while in paired homologue char- present among the taxa of interest. However, when

all different fur- acters “presence” character states a feature shows morphological variation between nish potential phylogenetic evidence. terminal taxa a number of different coding deci-

of It The importance a distinction between taxic sions can be made. then becomes crucial to rec- and transformational approaches to homology was ognize that different coding methods have distinct recently debated in relation to the value of modi- strengths and weaknesses, and given a certain set fied three-taxon analysis (Carine & Scotland, 1999) of taxa and morphological features different cod-

alternative standard cladistic based methods different as an to analysis ing may yield phylogenetic re- upon phylogenetic parsimony for grouping taxa sults. This is amply illustrated by various detailed

(Carine & Scotland, 1999; Scotland, 2000a; Kluge studies for diverse taxa and characters where dis-

& Farris, 1999; Farris et ah, 2001; Kluge, 2001). tinctly different cladograms may emerge for the

While proponents of the taxic approach to homology same taxa under different character coding strate- consider it of that & a strength a/p coding no assump- gies (Rouse Fauchald, 1997; Rouse, 2001; Strong tions are made concerning the homology of char- & Lipscomb, 1999; Forey & Hitching, 2000; Haw- acters states within a character, and thus potential kins et ah, 1997; Hawkins, 2000). transformations between them (Pleijel, 1995; Carine Although all available coding methods have their

& Scotland, 1999; Scotland, 2000a, b), this inter- idiosyncrasies, a strong conclusion from recent pretation fundamentally contradicts the theoretical studies is that a/p coding of multistate variation foundations of as suffers from several flaws that phylogenetic parsimony analysis, strongly compro-

this implemented in programs such as PAUP, Hennig86, mise the value of coding method (Hawkins et and MacClade, where character state transforma- al., 1997; Strong & Lipscomb, 1999; Hawkins, tions central & assume a role. 2000; Forey Hitching, 2000). Among the ac-

the of in- Within framework transformational homol- knowledged weaknesses of a/p coding are the

the ogy the distinction between complement and troduction of: 1) redundant characters, 2) logical

relations is between different paired homologue insignificant because dependence characters, 3) group- phylogenetic parsimony operates by counting char- ing on the basis of non-homologous absences, and acter state transformations, be it between absence 4) the negation of the central role of comparative

in Wilkin- and presence of a feature (a/p characters), or alter- morphology cladistics (see Pleijel, 1995; native forms of a feature (binary paired homologue son, 1995; Hawkins et al., 1997; Strong & Lip- and multistate characters). This implies that all scomb, 1999; Hawkins, 2000; Forey & Hitching, character states within a character need to be ex- 2000 for detailed discussions). This study focuses

constructed plicitly on the basis of a careful study on the latter two categories, specifically discuss- of morphological similarity, or else character state ing difficulties introduced by a/p coding for the transformations may become meaningless. A spe- identity of character states, and the interpretation cial difficulty is thus introduced for “absence” cha- of character state transformations.

in racters states, particular when a feature is present In view of problems such as these with a/p coding, in various distinct forms, and is inapplicable for it is surprising to find that the bulk of characters certain taxa. The need to carefully delimit all char- (88.7%) coded in cladistic analyses of the Meta-

of acters states a character, including the “absence” zoa published during the last two years are a/p states, is one feature that distinguishes the trans- characters. If morphological variation within the formational from the taxic approach to homology. Metazoa is strictly dichotomous, with features ei-

As will be discussed below study of character state ther being absent or present, than the uniform adop- identity in the recent of most analyses metazoan tion of Boolean logic to represent this variation in

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a data matrix be may entirely justified. Obviously clearly delimited cannot be meaningfully analyzed that is not the case. The next section discusses the within the context of transformational homology.

of in This pitfalls a/p coding of multistate variation problem affects more than40% of all coded

metazoan cladistics. characters a/p (Appendix), and this is merely a

conservative estimate. For it example, appears to

be no code character for problem to a gap junc-

The failure of Boolean character tions for logic: state a/p metazoans, and to score all phyla as

and “absence” character identity unspecified either having or lacking them: characters 5 in Soren-

in states metazoan cladistics sen et al. (2000) and Nielsen (2001), and charac-

ter 4 in Peterson & Eernisse (2001). This character

Within the context of be phylogenetic parsimony and appears to applicable to all animal phyla. Simi-

transformational homology it is essential to perform larly, the adopted coding and scoring of chitinous

a detailed study of morphological similarity in order chaetae/setae in phyla such as Annelida and Bra-

to delimit properly all character states within a chiopoda is not considered as a problem here. How-

character “the but because as same different” (Hawkins et ever, chaetae/setae are modifications of

& ah, 1997; Rieppel Kearney, 2002). In the cases chitinous cuticles, strictly speaking this character

of with is in binary coding paired homologues and multi- only applicable taxa that possess cuticles with

state coding, it is obvious that a certain degree of chitin. Other phyla would then have to be scored

of for this character morphological study underlies the identification as “inapplicable”. Yet, one might

character states. Both conceive coding types try to accurately of ultrastructurally similar chaetae as being

observed character constructed from represent variation as separate a non-chitinous cuticle. The ex-

in expressly delimited character states within a single amples included the appendix are restricted to

character. In contrast, the Boolean reduction of those instances where the unspecified character

states scored morphological variation that defines a/p coding are obviously coded and as a default

the central role of whenever the slights comparative morphology “presence” state did not occur for a

in Such phylogenetics (Pogue & Mickevich, 1990; Haw- phylum. a procedure is compatible with a taxic kins et & to is ah, 1997; Hawkins, 2000; Forey Kitching, approach homology as implemented, for ex-

2000). This becomes especially clear in recent stud- ample, in modified three-taxon analysis, where the

ies of metazoan cladistics when the “absence” cha- “absence” states carry no empirical information

racter states are considered. (Carine & Scotland, 1999; Scotland, 2000a; Wil-

A is in the liams & striking asymmetry apparent care taken Siebert, 2000). Nonetheless, the coding and define to “presence” and “absence” character states. scoring of such “trash can” character states is in- The appendix summarizes examples of characters compatible with standard cladistic analysis based trom the five most recent cladistic studies of the upon phylogenetic parsimony. The character state

Metazoa that suffer from that the a specific character cod- transformations are at heart of such analy-

ing the “absence” character all problem: states are un- ses are only meaningful when states are care-

specified, and are scored for taxa with defined. they very fully

dissimilar This morphologies. fundamentally con- The lack of attention directed towards defining

tradicts the of standard cladistic the “absence” character assumption analysis states is particularly puz- outlined above that all character states should be zling in view of the obvious care taken to properly of code conjectures primary homology rooted in mor- and score subtle variations for some of the

phological similarity. As De Pinna (1991: 377) characters. For example, for at least 62 characters

in concluded, unspecified character states are empiri- the data set of Peterson & Eernisse (2001) it

cally all empty, “conjectures ofprimary homology that appears that care in character coding has been do not conform to the sim- criterion of similarity directed towards the “presence” states, while the

ply do not exist.” Because only cladogram rooting “absence” states are essentially unspecified. It is will determine what the and therefore that plesiomorphic apo- puzzling to find for some of their

morphic character that characters states are, states are not morphological study apparently did play

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role in and For be an important coding scoring. ex- mary homology have to based uponmorphologi-

ho- cal character that “the ample, their character 67 proposes a primary similarity leading to states are

but mology of different cell types that are thought to same different,” the only effect of lumping

be part of filtration nephridia (terminal cells, po- distinct morphologies under one state may be to

docytes, and nephrocytes, with terminal cells a obscure potentially useful variation. In the worst

of and character that not delim- component protonephridia, podocytes ne- case, states are properly

of ited and scored homol- phrocytes components metanephridial systems, actually propose primary

without and nephrocytes used to refer to nephridial systems ogy of dissimilar morphologies empirical

the central role present in arthropods and onychophorans). Phyla basis. That would negate of com-

in cladistics. The lacking any of these cell types are scored as “ab- parative anatomy unspecified

while of these cell “absence” discussed here fall into this sent,” phyla showing any types states cat-

is are scored as “present.” This scoring supported egory.

by data on the ontogenetic continuity of proto- Problems with unspecified “absence” states can

nephridia and metanephridia in certain polychaetes be of two types:

in and phoronids, and by a continuum cytological 1) taxa for which inapplicable character states are

differentiation and function between the different not recognized and are simply scored as “ab-

cell types involved (Ruppert & Smith, 1988; Smith sent”

multistate variation of character is & Ruppert, 1988; Bartolomaeus& Ax, 1992; Smith, 2) a not recog-

1992; Ruppert, 1994; Haszprunar, 1996b). A third nized and part of it is inappropriately forced

character state is erected and uniquely scored for into the “absence” state of a binary character

Nematoda, which possess no elements normally part

of filtration nephridia. Although Nematoda could A failure to recognize the hierarchical nature of

be scored “absent” for cell variation lead to simply as nephridial morphological may inappropriate

types, Peterson & Eernisse (2001) instead chose to character scorings (see Strong & Lipscomb, 1999,

because Lee & 1999 create a separate character state for them and Bryant, for recent reviews of the

they felt that “coding nematodes as equivalent to treatmentof inapplicable characters). For example,

is cnidarians, ctenophores et al. is not appropriate” when an attempt madeto code the morphological

in (p. 199). Irrespective of the justification of this variation of the lophophore present phoronids

decision, it clearly shows that for this character and brachiopods, these characters are logically in-

Peterson & Eernisse (2001) felt the need to more applicable for phyla lacking lophophores. Several

precisely code the morphological variation other- approaches have been proposed for coding inap-

wise subsumed within an unspecified “absence” plicable states in cladistic analyses. Although no

state. The coding and scoring of the remaining a/ method is entirely free of interpretational problems,

characters have benefited from similar the best code char- p could at- currently way to inapplicable

tention. This indicates that Peterson & Eernisse i acter states is to score them as “?s” or “-s” which

(2001) were to a certain extent arbitrary in the are treated the same (Hawkins et ah, 1997; Strong

amount of care they took to code and score differ- & Lipscomb, 1999).

ent characters within their data set. All authors of the cladistic data matrices con-

The general problem of unspecified character sidered here have properly applied inapplicability

states in phylogenetic parsimony is the incorrect scoring for some characters, but none of these stud-

suggestion ofsimilarity in morphologically dissimi- ies has done so accurately and consistently for all

lar taxa, and the unsupported assumption that the included data. The data set of Peterson & Eernisse

is It disparate morphologies united within a trash can (2001), however, an exception. is the clearest

character state represent a clear alternative to the illustration of consistently applied a/p coding with other coded character state. Pogue & Mickevich no attempt at all to correct for inapplicable char-

(1990: 353) qualify broad character states as a acter states. For example, seven synapomorphies

“common practice obscuring observed variation.” for the monophyly of brachiopods (characters 59-

As long as it is realized that propositions of pri- 65) code for morphological variation of the lo-

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For these with phophore. characters, taxa lacking this tion, the common result of creating default, variation are all scored of trash as “absent,” irrespective or can, character states that do not reflect whether they possess a lophophore, such as Pho- comparative morphology. Although such practice ronida, or not. This introduces character be dependence may defensiblewithin the non-evolutionary con- and into the cladistic redundancy analysis. Inap- text of taxic homology, it is incompatible with the and should be plicability coding scoring consistently purported goals of standard cladistic parsimony applied because different treatments of inapplicable analysis (Scotland, 2000a; Kluge, 2001). In order data the may differentially affect outcomes of an to remove this striking inconsistency between theory analysis. Waggoner’s (1996) analysis of arthropods and practice in metazoan cladistics, character cod- and fossil and and problematic taxa, Zrzavy et al.’s ing scoring should receive far more explicit

(2001) analysis of bilaterian phylogeny potently attention than is current practice. The following illustrate that different codings of inapplicable sections discuss several examples of the difficulty character states may produce substantially differ- to interpret character state transformations when ent results. phylogenetic “absence” character states are not defined.

“absence” also result from Unspecified states may not recognizing the multistate nature of variation.

In this variation coded the case, not by “presence” Reconstructing body plan evolution with state be united may inappropriately with unrelated Boolean logic: narrating history without

Such morphologies. a practice misrepresents avail- looking back able evidence and misses potentially useful phy- logenetic information. For character 29 The example, optimization of characters on cladograms is an in Peterson & Eernisse codes cleav- (2001) spiral essential source for insights into the evolution of

but the scored as “absent” for all age a/p, phyla spiral organismic complexity on taxonomic levels, cleavage exhibit a of great heterogeneity cleavage including the animal phyla (e.g., Valentine, 1997; types that cannot be subsumed within a cha- single Jenner, 1999, 2000). The morphological data sets racter state alternative The to spiral cleavage. scoring assembled for cladistic analyses of the Metazoa of the “absence” state assumes primary homology therefore seem to be an ideal source for insights of from cleavage ranging the lack of a ste- types into the origin and diversification of phylogene- such in Cnidaria reotypical cleavage pattern as tically significant parts of animal body plans. Pa-

(Davidson, 1991; Martindalc & Mar- Henry, 1998; radoxically, however, the widespread use of a/p tin, 1997), bilateral such as in Urochordata characters with cleavage unspecified “absence” states se- & (Jeffery Swalla, 1997) or even Deuterostomia the value of verely compromises current data ma- and forms with (Nielsen, 2001), unique or more trices for understanding the evolution of animal body difficult to interpret cleavage types such as Nema- plans. toda and et Acoela (Henry ah, 2000; Nielsen, 2001). Since most “absence” unspecified states are op- this character and does Obviously, coding scoring timized as plesiomorphies, the reconstructed ground not properly the of metazoan of represent diversity patterns stem species (nodes) on a cladogram cleavage types. Moreover, since Peterson & Eernisse for are many characters entirely ambiguous. For

(2001) do not include other character on cleav- any example, consider the scoring of character 54 in age geometry, phylogenetically significant varia- Peterson & Eernisse (2001), non-muscular perito- tion is not coded. The introduction of a multistate neal cells in lateral regions of coelom a/p, with character, or the of “?s” would be a more scoring Annelida, Echiura, and Sipuncula scored “present,” sensible of observed variation in way representing the remaining taxa as “absent.” The evolution of cleavage for the of phylogenetic types purposes this apparently complex character is optimized (am- parsimony. biguous) as a synapomorphy of a clade including Many included in the exhibit examples appendix these three phyla in addition to Mollusca (Neo- a mixture of problematic “inapplicability” scoring, trochozoa). According to this scoring all recon- and the improper binary of multistate varia- structed coding stem species up to the clade Neotrochozoa

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are and with to comparable plesiomorphic respect gram,” because “doing so can lead to nonsense all

this character as lack coeloms with they laterally zero reconstructed stem species that... have no state

located cells. this whatever” This is peritoneal Unfortunately, particu- (their italics). problem most po- lar coding and scoring obscures the most important tently illustrated by Zrzavy et al. (1998) who in-

that must have occurred the evolution cluded “all-zero” steps during an hypothetical outgroup to root of this character, i.e., the evolution of a coelom and their morphological cladogram (see also Zrzavy et

The sister to the Neotro- In this the is peritoneocytes. phylum ah, 2001). case, problem worsened

chozoa is which coelo- Nemertea, already possess by the inclusion of binary paired homologue char-

mic cavities, the rhynchocoel and vessels of the acters in et set. An Zrzavy al’s (1998) data attempt

circulatory system, as well as peritoneal cells that to interpret the paired homologue characters for this

line the & rhynchocoel (Turbeville Ruppert, 1985; “out-group” conjure up a grotesque organism with Turbeville, 1991). Thus, the most important com- a body plan composed of illusory, and in several

of this character ponents ostensibly complex already instances, contradictory features. These include a

evolved at the base of a larger clade that minimally schizocoel, an anterior/dorsal anus but also lack-

includes Nemerteaand Neotrochozoa. the an However, ing anus, a biphasic life cycle but at the same of these features remain origins unaddressed by the time lacking a primary larva, dominant asexual

of & analysis Peterson Eernisse (2001) because no reproduction, post-adult molting but also lacking

characters are included that code for the cuticular presence molting, hollow polyp tentacles, uniramous of either a coelom or peritoneocytes. limbs, and a non-centralized nervous system. Need- For a elucidation of character transfor- less proper to say, such a chimeric outgroup does not help mations that the evolution underlay of non-mus- to determine the polarity of character change. cular peritoneocytes additional characters need to The interpretation of character state transforma-

be included in the For the dis- tions analysis. example, (steps) on a cladogram breaks down when only

tribution of peritoneocytes within coeloms should “presence” character states are defined. A final

be either coded if the lateral location of these cells illustration of the problem is the introduction of

is the of this important part character, or when the circularity into cladistic analysis. In what must be relative prominence and function of the coeloms regarded as one of the most meticulously researched

is important, their multifarious differentiations th cladistic studies published during the 20 century, should be coded (a spacious hydrostatic body co- Grande & Bcmis (1998; ix) consider the “a priori elom or of eucoelom sensu Haszprunar (1996a) in assumption “primitiveness” for a character state” annelids, echiurans, and sipunculids, but more re- as a one of the diagnostic features of “authori- stricted and in in differently specialized molluscs and tarianism systematic biology” in generations past. This demonstrates that nemerteans). example clearly Strikingly, this problem is also prevalent in recent it is impossible to char- cladistic unambiguously interpret analyses of the Metazoa. Not specifying acter state for as hetero- the “absence” transformations, example \ state of a character can only be taken chronic shifts evolution of or as genuine novelties, to suggest that the phylogenetically informative when “absence” plesiomorphic states are unspeci- derived character states are already known before fied, as is the case for the of listed the majority examples congruence test. Optimizing characters on the in the the selec- appendix. Furthermore, arbitrary resulting cladograms indeed indicates that for most tion of data input may strongly impair the effec- a/p characters in studies of metazoan cladistics it tiveness of a cladistic as test ofalternative is the analysis a “presence” state which is the derived state. hypotheses 2001, (Jenner, 2002; submitted). Such a procedure logically foregoes the function Generally, the of problem reconstructing history of outgroup taxa to distinguish plesiomorphic and without specification ofantecedent is a character The states prob- apomorphic states. a priori assump- lem for all characters with “absence” as a character tion of the evolutionary polarity of a character state, whether these are unspecified or not. Accord- introduces unwarranted circularity into the cladis-

to ing Kluge & Farris (1999: is tic and it 209) a/p coding analysis, makes out-groups effectively non-

not used to normally as input a parsimony pro- functional.

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As illustrated in order above, to yield meaning- Ectoprocta, Annelida, and Arthropoda is uniquely

ful character the current state transformations, pen- homologous, and a proper alternative to archenteron-

chant for Boolean character with derived coding unspecified mesoderm. This interpretation is scarcely

“absence” states should be thoroughly reconsidered. For supported by morphological evidence. example, As will be discussed in the next section, this be- in addition to micromere-derived ecto-mesoderm,

comes especially clear when “absences” unspecified endo-mesoderm has been reported to arise from attain character 4d in phylogenetic significance through mesentoblast phyla such as Annelida. How- reversal. ever, even accepting spiral cleavage in the arthropod

the ground pattern (but see Scholtz, 1997), sources

of mesoderm are not in agreement with those in When becomes congruence meaningless: the trochozoans, i.e., mesoderm does not arise from

“absence” and unspecified states uninformative mesentoblast 4d (Anderson, 1973; Slewing, 1979;

character reversals Scholtz, 1997; Nielsen, 2001). Furthermore, nema-

todes lack any 4d-mesoderm, and according to their A cladistic analysis subjects primary homology cell lineage (see table 37.1 in Nielsen, 2001) it must

to a character in be concluded that propositions congruence test or- they possess only ecto-mesoderm.

der to corroborated Endo-mesoderm also be absent from separate secondary homologies appears to gas- from provisionally refuted homologies, i.e., ho- trotrichs (table 35.1 in Nielsen, 2001), although this is much moplasies (De Pinna, 1991). However, when the a more tentative conclusion based on studies

character older states are not based upon morphological than those for nematodes. Although an ar-

chenteric of similarity, secondary homologies supported by cha- origin mesoderm is so far unknown racter congruence become meaningless. As dis- for ectoprocts, the precise source of their larval,

cussed and above, unspecified “absences” are most often especially adult mesoderm, remains poorly resolved as the plesiomorphic character states, but known (Reed, 1991; Zimmer. 1997; Liiter, 2000;

the Haws logical of unspecified character states are Nielsen, 2001). Consequently, uniting all these phyla

most clearly expressed when unspecified states are on the basis of simply lacking archenteron derived

optimized as i.e. when attain mesoderm, while do show apomorphies, they they not any unique phylogenetic Several significance. examples illus- morphological similarity that could justify scoring

trate the fallacies of grouping phyla on the basis them for the same character state, fails to reflect of unsuppoitable homology of dissimilar morpholo- comparative morphology. Character 20 in Giribet

gies. All character transformations discussed et al. the data state (2000) (based on set of Zrzavy et

below are optimized on the morphological cla- ah, 1998, and optimized on the total evidence to-

of dograms their respective studies, except as noted pology), and character 36 in Peterson & Eernisse

otherwise. the (2001) also code for archenteric origin of meso-

Character 26 in Nielsen (2001) codes for the derm with a/p characters, and the same nonsensi-

absence cal or presence of mesoderm derived from transformations to an unspecified state are found the archenteron. Archenteron derived mesoderm is in their studies (ambiguous for Peterson & Eernisse,

scored for Ctenophora, Deuterostomia (Echinoder- 2001).

inata, Pterobranchia, Enteropneusta, Chordata, Bra- Moreover, the frequently adopted dichotomous

and chiopoda, and Phoronida), Chaetognatha, and coding of mesoderm source in the Metazoa (me- a reversal to “absence” of this source of mesoderm soderm from archenteron versus mesoderm from

supports the of a clade ofall monophyly protostomes 4d, blastopore rim, or ecto-mesoderm) is more re-

uiinus The flective of order created chaetognaths. phylogenetic significance by the very process of °1 this character transformation, however, is com- character coding than that it faithfully reflects ob- promised the by morphological disparity of the served organismic variation (Jenner, 2002). This

scored absences. The adopted scoring implies that problem principally results from the use of differ- the absence of mesoderm derived from the arch- ent criteria to diagnose the origin of mesoderm in enteron in phyla including Gastrotricha, Nematoda, protostomes and deutcrostomes. Whereas the ori-

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gin of mesoderm in protostome phyla such as nema- Zrzavy et al., 1998; Sorensen et al., 2000; Nielsen, todes and molluscs is determined by the onset of 2001; Peterson & Eemisse, 2001; characters 21, 144, mesodermal cell fate specification, which becomes 27, 19, and 45 respectively). This scoring is largely apparent during early cleavage, in deuterostome based upon the work of T. C. Lacalli, in particular phyla mesoderm origin is typically pinpointed by his proposed homology of the frontal eye complex the onset of morphological differentiation, prima- in “larval” amphioxus and the apical organs that

the differentiation of coelomic such in invertebrate larvae rily pouches are widespread (Lacalli, 1994, as in echinoderms. However, when initial meso- 1996). However, although this postulated homol- derm also criterion in into specification is used as a ogy has become widely incorporated cladistic deuterostomes, e.g., echinoderms, then it becomes data matrices, none of the cladistic studies carried clear that mesoderm specification is already estab- the character scoring to its logical conclusion. In lished during blastula stages, long before the first order to maintain logical consistency throughout signs of morphological differentiation of mesoderm the data matrix, the scoring of an apical organ in become apparent (Davidson et al., 1998; Davidson, Cephalochordata would have to be accompanied by

2001; Sweet ct al., 1999). This lowers the confi- the scoring of the adult brain being derived from dence have in of the characters that associated with the because the larval we might one or apical organ has been in of a be- central nervous the frontal regarded support dichotomy system, including eye tween protostomes and deuterostomes (see Nielsen complex, is retained in the adult. It must be con- et al., 1996; Nielsen, 2001; Sorensen et al., 2000; cluded that the reversal of character 45 in Nielsen

Zrzavy et al., 1998, 2001). (2001) to an unspecified character state in taxa with

45 Character in Nielsen (2001) codes for the very dissimilar nervous system ontogenies and mor- absence or of an adult brain derived be a reliable bilaterian presence from, phologies cannot synapo- or associated with, the larval apical organ. The morphy. reversal of this character at the base of the Bilateria Similarconclusions about the cladistic insignifi-

the is one of four unambiguous synapomorphies of cance of meaningless character state transforma-

Bilateria in Nielsen (2001). Comparison of the tions to unspecified states scored for phyla with nervous system morphologies of the bilaterian phyla dissimilar morphologies apply to other characters clearly reveals that there is no empirical basis for as well, such as characters 5 and 68 in Giribet et this transformation. Among the phyla scored as al. (2000) (optimized on the total evidence topol-

adult brain either derived with lacking an from, or as- ogy, mapping optimization criterion depen- sociated the larval A reversal the “absence” with, apical organ are: a) taxa dent). to unspecified state without adult brains but with larval apical organs, of character 5 (radial cleavage a/p) inappropriately such as Echinodermata; b) taxa with adult nerve unites phyla with distinct cleavage types, includ- concentrations that are formed separate from the ing phyla with spiral, e.g., Annelida, Mollusca, and larval such and Phoro- apical organ, as Entoprocta non-spiral types, e.g., Rotifera, Acanthocephala.

with clear adult brains but without Character 68 a/ nida; c) taxa any (tri-radial or star-shaped pharynx larval such as and Gna- unites with different apical organ, Chaetognatha p) phyla very organizations

and of anterior ends their thostomulida; d) taxa with a larval apical organ the of digestive systems on and a brain derived from it, such as Cephalochor- the basis of a reversal to the unspecified “absence” data. state. Here the morphologies incorrectly proposed

The condition in merits be from the cephalochordates some to uniquely homologous range com- clarification. lack of such in Although cephalochordates are usu- plete a pharynx, as is found some

not ally interpreted as possessing larvae comparable acoels (Rieger et al., 1991), to the presence of a

those found in other to invertebrates, e.g., Nielsen primarily non-muscular esophagus as observed for

(1998), all cladistic analyses published to date that Cycliophora (Punch & Kristensen, 1997), to the included a character for the of muscular coding presence or presence well-developed pharynges absence of an apical organ, have scored Cephalo- with cuticular hard parts characteristic of phyla such chordata as possessing one (Nielsen et al., 1996; as Gnathostomulida and Rotifera (Lammert, 1991;

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& Clement Wurdak, 1991). Thus in both these in of ly terms their topology. In contrast, the sole examples, the character state transformations merely empirical anchor of these studies receives surpris- supply spurious clade little support. ingly explicit attention, both before the analysis As discussed above, the problem is much more of character congruence (data matrix compilation),

widespread than these cases of character reversals. and especially after (dynamics of character state

For all 230 characters with “ab- a/p unspecified transformations). This unjustifiably cavalier attitude sence” states in the found five data sets studied here towards the data be considered may as a defining (Appendix), potential is weakness of phylogenetic significance contemporary morphological metazoan ascribed to unspecified character states This unsupported cladistics. problem manifests itself in various

by morphological evidence. Such cavalier treatment from guises, ranging uncritical character coding and of cladistic character coding diagnoses an impor- scoring (Jenner, 2001.2002; this paper), to the rather

tant weakness of current practice in metazoan cla- arbitrary selection of characters and taxa, thereby distics. Increased attention to the morphological the strongly impairing power of cladistic analyses

basis of our data sets and concomitant re-coding to test phylogenetic hypotheses (Jenner & Schram, of characters is needed to remedy these problems. 1999; and especially Jenner, submitted).

One important step in the right direction is the

explicit study oforganismic variationprior to cha-

Reasserting the central role of comparative racter coding and scoring. Increased attention to

morphology in metazoan cladistics comparative morphology, and more explicit atten- tion to character coding is needed to rebalance

The discrepancies between and in theory practice contemporary metazoan cladistics. The partition-

metazoan cladistics noted above are The of variation into discrete striking. ing states is often not of character predominance a/p coding, and the fre- straightforward, and each choice of character cod-

of quent coding unspecified “absence” character ing should therefore be explicitly defended. Instead states can be accommodated under an of only assump- bending nature’s variation to fit into ill-defined tion of taxic homology where only “presence” states character states, character coding should instead aim have potential phylogenetic significance. However, to accommodate variation. Of recognized course, all published morphological analyses of metazoan complex variation morphological may provide room cladistics operate by counting character state trans- for different coding strategies, the relative merits formations within the of context transformational of which can be debated. For example, authors may homology. This demands that all character states differ in the number of character states assigned delimited are clearly on the basis of a careful to a particular character the analysis depending upon termi- of “absence” nal included morphological similarity. Unspecified taxa in the analysis, or their individual states prevent any straightforward of interpretation of perception the potential phylogenetic significance character in than change more a third of the of the character states. In other a/p cases authors may characters included in the five in their analyses of meta- differ decisions to capture morphological zoan cladistics that the new millennium. variation either in inaugurated one multistate, or multiple bi- his dissociation between and I morphological study nary characters (see Jenner, 2002 for examples and character coding and scoring is worrying. The uni- references). versal of Boolean in adoption logic character coding Given the differential effects of different cod- has in cases resulted in the bending of mor- choices on outcome of many ing the cladistic analyses, phological variation to fit within the confines of a more explicitly experimental attitude towards data characters. binary matrix construction is imperative. In studies of

Contemporary of molecular morphological analyses meta- phylogenetics, experimental manipula- zoan cladistics arc heavily skewed. tions of are Typically, dis- data sets commonly employed to as- attention is proportionate given to the extraction sess the robustness of the outcomes of an analysis °1 phylogenetic signal from a given data set, and in terms of varying input parameters and assump- the resulting are discussed strict- tions. For it cladograms usually example, is commonplace to assess the

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effects of various weighting schemes for transitions/ are plesiomorphies inherited from the last common

translations, or insertions/deletions on the results ancestor of Gastrotricha plus Ecdysozoa, while a

the of analysis. Introduction of such an explicit chitinous endocuticle is the only uniquely derived

experimental approach would also be a valuable condition supporting ecdysozoan monophyly. Cod-

in cladistics facili- asset morphological as it would ing a single complex character removes potential

tate a better understanding of the robustness of phylogenetic evidence (trilaminate epicuticle and

phylogenetic conclusions both with regard to the proteinaceous basal layer) for uniting Gastrotricha data matrix used, and the results of other analy- either with Introverta alone (yielding a monophyl-

Two ses. examples from metazoan cladistics will etic Cycloneuralia sensu Nielsen, 2001) or Ecdyso-

illustrate the importance of an experimental ap- zoa, while subdivision of this cuticle character

proach to character coding. complex would reduce the empirical weight of the

it Recently has been debated how to code one ecdysozoan synapomorphies. The choice between

potential morphological synapomorphy of the Ec- these alternatives is not immediately obvious (partly

dysozoa. Schmidt-Rhaesa et al. (1998) discussed because Gastrotricha remain a perennial phyloge-

the cuticle structure characteristic of Ecdysozoa: netic problematicum), but different coding decisions

Panarthropoda and Introverta (sensu Nielsen, 2001: clearly embody differences in the phylogenetic

Nematoida and The of of varia- Scalidophora). complex ecdyso- significance a given range organismic

cuticle zoan was defined as tri-layered with a tri- tion, and consequently each decision has to be

laminate epicuticle, a proteinaceous exocuticle, and carefully justified. The practical significance of these

a chitinous endocuticle (Schmidt-Rhaesa et al., considerations will be illustrated by the following

1998: 274). Should this be coded as a single com- character coding experiment. character plex (Zrzavy, 2001), or should it be de- Zrzavy et al. (2001) coded the complex cuticle constructed into several features that may exhibit character (21) suggested as an ecdysozoan autapo- a less than total congruence (Wagele et ah, 1999; morphy by Schmidt-Rhaesa et al. (1998) as dis-

& This is trivial Wiigele Misof, 2001)? not a ques- cussed above (defined by Zrzavy et al. as molted tion. For Gastrotricha but cuticle with example, possess some epicuticle, exocuticle, and endocuticle,

all of the of charac- not components this complex with sclerotization). This complex character unam- ter. Although they are not included in Schmidt- biguously supported Ecdysozoa in the analysis of

Rhaesa et al.’s do al. Ecdysozoa clade, they possess a Zrzavy et (2001). However, Gastrotricha were tri-laminate epicuticle, but as part of a bi-layered united with Gnathostomulida at the base of the cuticle (Ruppert, 1991; Lemburg, 1998). Further- protostomes (see Jenner, 2002 for discussion of the

a basal fibrous characters more, they possess proteinaceous supporting this sister group relationship). or which be the granular layer, may comparable to I performed two coding experiments for cuticle

exocuticle of in proteinaceous (median layer) pa- structure based on the data presented Lemburg

and narthropods scalidophorans (Lemburg, 1998). \ (1998). In the first experiment, I added one char-

Chitin has so far been demon- the not convincingly acter to data set ofZzravy et al. (2001) to code strated in gastrotrich cuticles (Ncuhaus et ah, 1996). for a tri-laminate epicuticle with a proteinaceous So while it is true that a complex cuticle including layer as is shared between Gastrotricha and Intro- all be components may a unique synapomorphy of verta plus Panarthropoda, while character 21 in

Ecdysozoa (Schmidt-Rhaesa et ah, 1998; Zrzavy, Zrzavy et al. (2001) was retained to represent the

this of 2001), complex character appears in reality to new addition a chitinous endocuticle. In the be a character of different fea- second added characters complex comprised experiment, I two to sepa- tures with distinct evolutionary histories (Lemburg, rate the variation for the tri-laminate epicuticle and

1998). the proteinaceous layer, while again retaining char-

If the Gastrotricha 21. Both represents the sister taxon to acter alternatives were analyzed with a the Ecdysozoa, as maintained by Schmidt-Rhaesa heuristic search, 100 random addition replicates, et ah then the of tri- and (1998), at level Ecdysozoa a TBR branch swapping. laminate and a exocuticle epicuticle proteinaceous The first experiment yielded a strict consensus

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Fig. I. Strict consensus trees resulting from ananalysis of the data set of Zrzavy et al. (2001) with two modifications: 1) addition of character a coding for a tri-laminate epicuticle with a proteinaceous layer as found in gastrotrichs, introvertans and panarthropods,

2) addition oftwo characters to code the variation for the tri-laminate epicuticle and the proteinaceous layer separately, resulting in

the less resolved consensus tree. See text for discussion.

tree identical to that obtained for the unmodified Gastrotricha vis-a-vis the ecdysozoan phyla. data set (Fig. 1). The Ecdysozoa was supported, A final example illustrates the importance of cha- and Gastrotricha remained a sister groupto Gnathos- racter coding decisions for resolving the phylogen-

tomulida. However, in the second experiment, the etic placement of Gnathostomulida in the animal

clade of Gastrotricha and Gnathostomulida col- kingdom. The sister taxon to the gnathostomulids

lapsed, were removed as a sister remains uncertain 2002 for Chaetognatha group (see Jenner, a compre- of the Ecdysozoa (as supported in the first experi- hensive discussion of the phylogenetic position of

ment and with the unmodified data set), and the gnathostomulids within the Metazoa). The two most

positions of these phyla in addition to the clade important competing hypotheses for the placement

remained unresolved within the the Metazoa Ecdysozoa proto- of Gnathostomulida among based on stomes (Fig. 1). This indicates that the choice to morphological data are the Plathelminthomorpha code complex cuticle morphology in these phyla and Gnathifera hypotheses. Gnathostomulids are the

either as a or as several sister single a/p character, a/p group to a monophyletic Platyhelminthes

characters an may influence the results in impor- according to the Plathelminthomorpha hypothesis, tant way. and to the Syndermata (Rotifera, including Seison, of the effects of different inter- Being aware and Acanthocephala) according to the Gnathifera pretations of a certain complex of morphological hypothesis. In terms of the number of independent variation is thus essential when the aim is to test studies and synapomorphies, the Plathelmintho-

alternative such as for be phylogenetic hypotheses, morpha hypothesis appears to the best supported

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hypothesis (Jenner, 2002). However, the monophyly of Peterson& Eernisse (2001), which supported the of Gnathifera is supported by characters of a bet- Plathelminthomorpha hypothesis, with the same

ter quality than those supporting the Plathelmintho- analysis parameters as in the first experiment. Sub-

I morpha Hypothesis, principally because they are sequently introduced a new character into their

and muscle more detailed unique. The two most important matrix coding for the pharyngeal attachment

gnathiferan synapomorphies are: type found in gnathiferans and scored according-

ly. The first analysis yielded the 20 MPTs and

the of elements with tube-like well-resolved strict consensus found Peterson I) presence jaw by

support rods composed of electron lucent ma- & Eernisse (2001) (Fig. 2). In sharp contrast, the

terial surrounding an electron-dense core re-analysis with the second potential gnathiferan

the of cross-striated resulted in dramatic 2) presence pharyngeal mus- autapomorphy quite a collapse

cles that attach to the jaw elements through of the strict consensus tree, leaving one huge poly-

epithelial cells tomy for Bilateria (Fig. 2). The only clades that were

retained are Ecdysozoa, Eutrochozoa, Deuterosto-

included + Phoronida and Although the first character is in many mia, Brachiopoda Platyhelminthes.

cladistic analyses, the second character is restricted The relationships between these and all other bi-

to the analyses of Nielsen (2001) and Sorensen et laterian phyla remained unresolved. Furthermore, al. (2000). Despite the unique ultrastructural simi- monophyly ofPlathelminthomorpha was no longer

larities of gnathiferan jaw elements, the inclusion supported, and the position of Gnathostomulidaand of only the first character in a computer-assisted Rotifera remained entirely unresolved.

cladistic this it becomes an analysis does not guarantee a monophyl- In context, important ques- etic Gnathifera, as is illustrated by the studies of tion whether the separate coding of a character on

Wallace et al. (1996), Zrzavy et al. (1998, 2001), the attachment of muscles to pharyngeal hard parts

Giribet et al. (2000), and Peterson & Eernisse through epithelial cells is justified, as is done in

(2001). Interestingly, the only cladistic analyses with the matrices of Sorensen et al. (2000) and Nielsen

the in a sufficiently broad taxon sampling to test Pla- (2001), but not the other studies. Cross-striated

thelminthomorpha against the Gnathifera hypoth- pharynx muscles that attach to cuticular jaw ele-

in eses, and that supported the latter are Sorensen et ments are also found Micrognathozoa (Kristensen al. (2000) and Nielsen (2001). These studies are & Punch, 2000). Naturally, when comparable pha- also unique in including a separate character on the ryngeal hard parts are lacking in other taxa, they

of mode pharyngeal muscle attachment. It then should logically be scored as ‘inapplicable’ for mode becomes important to study the effect and justifi- of pharyngeal muscle attachment, but neither Soren-

cation of coding the jaws and their muscle attach- sen et al. (2000) nor Nielsen (2001) adopted this

I ment either as one or two separate characters. scoring. Sorensen et al. (2000) and Nielsen (2001)

performed two experiments. also score this feature as present in Annelida. How-

matrix of it is found in eunicid First, I re-analyzed the original data ever, only polychaetes, which

Nielsen (2001), which supported the Gnathifera are unlikely to be representative of the annelidan

with 100 hypothesis, a heuristic search, random ground pattern (Rouse & Fauchald, 1997). If we

addition replicates, TBR branch swapping (exclud- nevertheless choose to accept this scoring, we have

ing character 64 as Nielsen did for his strict consen- to confront an interesting issue. Cross-striated body

sus). Then I re-analyzed the matrix while excluding muscles (as opposed to cross-striated pharyngeal

the the in character (35) coding for mode of pharyn- muscles) taxa such as kinorhynchs, loriciferans,

geal muscle attachment. These two analyses yielded cycliophorans, and possibly nematodes (Wright,

exactly the same strict consensus of the same four 1991, fig. 28) also do not attach directly to the

MPTs with the intermediate a monophylctic Gnathifera, a situation cuticle, but rather through of an

identical to the analysis and results (fig. 56.1) of epidermal cell (Kristensen & Higgins, 1991; Punch

Nielsen (2001). & Kristensen, 1997; Neuhaus, Kristensen & Peters,

Secondly, I re-analyzed the original data matrix 1997b). Similarly, somatic muscles of Microgna-

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2. Strict Fig. consensus trees from an of; the unmodified resulting analysis 1) data set ofPeterson & Eernisse (2001); 2) the data set of Peterson & Eemisse with the of for (2001) addition a character coding cross-striated pharyngeal muscles that attach to jaw elements cells found through epithelial as in gnathiferans (less resolved consensus tree). See text for discussion,

thozoa attach cells to indicate always through epidermal the, may that muscle attachment to the cuticle in this case intracellular, skeletal that are cells be plates through epithelial may a plesiomorphy on located in the lateral and dorsal body regions (Kris- the level of Gnathifcra (to be tested in future cla- tensen & Punch, In a of muscle 2000). fact, survey distic analyses). This reasoning would lessen the attachment types throughout the Metazoa reveals probability that this type of muscle attachment is that the attachment of muscles to the cuticle through a novel autapomorphy of Gnathifera to be coded intermediate cells is much more wide- from epithelial independently the presence ofpharyngeal hard spread. It has, for example, been reported for ar- parts. thropod the beak muscles, tardigrade stylet muscles, These experiments illustrate that single changes muscles in in cephalopods (through beccublasts), gas- a data matrix can have profound effects on the trotrich muscles, muscles to of ectoproct (attachment outcome a cladistic analysis, and the same change

and head muscles for ectocyst), chaetognath (Ruppert, two taxa in two different matrices can have 1991; Mellon, 1992; Dewel, Nelson & Dewel, 1993; entirely different effects. This underlines the im-

Budelmann, & Mukai et Schipp Boletzky, 1997; portance of explicitly justifying character coding ah, 1997; Shinn, the an 1997). Recognizing widespread decisions, and experimental approach to char- distribution of this mode of muscle attachment is acter coding allows novel insights into the stabil- for "nportant properly evaluating the phylogenetic ity ofcladistic results that would otherwise remain

SI gnificance of cross-striated muscle attachment hidden. For example, Rouse & Fauchald (1997) and to pharyngeal hard in In Rouse parts gnathiferans. fact, it (2001) coded alternative data matrices with

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several authors only binary a/p or multistate characters to resolve conventional coding is favored by

polychaete and siboglinid (formerly the phyla Pogo- (Hawkins et ah, 1997; Strong & Lipscomb, 1999),

it introduce difficulties nophora and Vestimentifera) relationships, respec- can interpretational asso-

tively. These studies convincingly show that the ciated with inapplicable data when PAUP (Swof-

results derived from the a/p and multistate data sets ford, 2002) or Hennig86 (Farris, 1988) are used to

the NONA may differ substantially in both topology and reso- analyze the data. In contrast, program

lution (for further examples of the effects of dif- by P. Goloboff minimizes these problems (Strong

ferent coding methods in the context of animal & Lipscomb, 1999).

Jenner & this leaves the relationships see Schram, 1999; Jenner, Nevertheless, unexplained why

2001; Donoghue et ah, 2000). vast majority of characters is coded as absent/pre-

sent. At this point, only speculation can be offered

because explicit justification is never provided. One

Conclusions part of an explanation for our willingness to adopt

be Boolean logic in character coding may our un-

deniable for The current lack of explicitness in the construction preference ordering complexity by dichotomous division 1998: of our morphological data sets can only be labeled (Wilson, 169; Gould,

unscientific. data differ the roots of this can as Morphological sets pro- 2000). Interestingly, preference

be traced back to the of foundly between studies, which in itself is no rea- systematic biology pre- division son for despair. However, because they differ chiefly evolutionary times when dichotomous was method of classification 1982, in myriad details that are not made explicit, it be- the favored (Mayr, 1995). Dichotomous division ordered comes virtually impossible to make a reasoned organismic

choice between alternative hypotheses. This be- diversity by separating groups from each other on

the basis of a certain feature or not. The comes especially clear when the efficacy of different possessing is studies is evaluated with respect to hypothesis test- resemblance to binary a/p coding immediately

ing (Jenner, 2002; submitted). obvious. A second for the observed The universal preference for binary character partial explanation

for coding, in particular a/p coding, in metazoan cla- preference a/p coding may stem from the fact

that half the character distics cannot be explained by the superiority of only states (the “presence” need be delimited. the this coding method. In fact, within the context of states) to Taxa lacking “pres- then be default phylogenetic parsimony a/p coding is currently the ence” state can simply scored as a of their for most severely criticized coding method, as is dis- irrespective morphology. Although some characters is made differentiate cussed above. There are no indications that this an attempt to among

realization has permeated into the general conscious- the taxa lacking the “presence” state, for example

this ness of metazoan systematists yet. Alternative cod- through inapplicability scoring, typically is not

ing methods do exist, for example the conventional carried out consistently (if at all; see Peterson &

of This dissociation between coding Hawkins et al. (1997). The explicit con- Eernisse, 2001). compara-

nection of this coding method with comparative tive morphology and character coding and scoring

morphology is much better justified than for a/p fundamentally contradicts the premises of phylo-

coding (Hawkins et ah, 1997). Alternatively, other genetic parsimony. Clearly, we have to go back to authors have advised the use of different coding basics.

methods, such as step matrices that quantify char- acter state transformation costs (Maddison, 1993; Acknowledgements Forey & Kitching, 2000). However, current limi-

tations of phylogenetic software, and the acknowl- -P This work was supported by grant 805-33.431 from the Earth edged idiosyncrasies of different character coding and Life Sciences Foundation (ALW) of the Netherlands Or- methods prevent an easy solution. As a result the ganization for Scientific Research (NWO). I thank Alison Cole

merits of different re- coding strategies currently and Frederick Schram for their incisive comments.

main at the center of debate. For example, although

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Appendix 31: tentaculated mesosome: animals with and without meso-

some

33: mouth terminal, pharynx radial: animals with various mouth Unspecified “absence” states in metazoan cladis- positions and various pharynx constructions tics. of “absence” character Examples unspecified 35: pharynx with cross-striated muscles attached to jaws by

states for a/p characters selected from the most epithelial cells: taxa with and without muscles attached to epi-

thelial cells recently published cladistic analyses of the Meta- 37: introvert with teeth, spines and scalids: taxa with and with- Note that the zoa. precentages are ‘conservative’ out introvert estimates. Delimitation of “absence” states may be 38: non-eversible mouth conewith cuticular ridges and spines: for characters how problematic more depending on taxa with and without introvert

strictly one adopts to the similarity criterion for 39: pharyngeal gill slits: taxa with and without pharynges

41: notochord: taxa with and without chorda determining primary homologies. 44: limbs articulated with intrinsic muscles: taxa with and with- The appendix lists 230 a/p characters with un- out limbs “absence” % of all char- specified states (42.9 a/p brain 45: adult derived from or associated with larval apical

38% of all with and with without acters; characters). organ: taxa and without adult brains, or

apical organs

46: ventral longitudinalnerve cord, paired or secondarily fused;

taxa with and without centralized cords Absence unspecified in Nielsen (2001) nerve 48: brain collar shaped: taxa with brains of diverse construc- (33 characters: 51.6%): tion and without brains

49; deuto- and tritocerebrum: with brains of di- proto-, taxa

7: with taxa with and without synapses acetylcholine: nerve verse construction and without brains

cells 50: haemal system: taxa with and without coeloms

10: monociliateepithelia: taxa with unciliated and multiciliated 51: mixocoel: taxa with and without coeloms

epithelia 53: haemal system with axial complex: taxa with and without

11: multiciliateepithelia: taxa with unciliatedand monociliated coeloms

with coelomic epithelia 56: metanephridia compartment restricted to a

12: generalbody cuticle with collagen: taxa lacking cuticle and sacculus: taxa with and without metanephridia

with chitinous cuticle 58: cleavage bilateral: taxa with dissimilar cleavage types

13: general body cuticle with chitin: taxa lacking cuticle and

with collagenous cuticle

14: cuticle molted: cuticle and with non-molted taxa lacking a Absence unspecified in Zrzavý et al. (2001) cuticle (21 characters: 35%): 16: gonads with separate gonoducts: taxa lacking gonads and

with gonads without separate gonoducts

spiral quartet taxa with dissimilar 17; coelom with I: cleavage: cleavage types gametes pass through and metanephridia: taxa

2: 4d-mesoderm: taxa with dissimilarmesoderm sources or without coelom 7: archimeric architecture: taxa with and without coeloms 18: spiral cleavage with 4-d mesoderm: taxa with different cleav- 8: dimeric architecture: of dissimilar body taxa very body ar- age types chitecture 19: with ciliated larvae \ larvae apical sense organ: taxa lacking 10: mesoderm formed from archenteron: taxa with dissimilar and with without larvae apical sense organs

mesoderm sources 21: larvae or adults with downstream-collecting ciliary system: 15: epidermal locomotory ciliature highly reduced or absent: taxa lacking ciliary feeding systems and with upstream-collecting taxa with and without locomotory cilia systems 21: molted cuticle with epicuticle, exocuticle, and endocuticle, 22: larvae or adults with upstream-collecting ciliary system: with sclerotization: taxa without cuticle and with cuticle but taxa lacking ciliary feeding systems and with downstream-col- non-molting lecting systems 22: cuticle containinga-chitin: taxa with differentcuticle com- 27: with body segmented serially repeated organs developed cuticle positions and taxa lacking a from 4d-mesoderm: with 4d-mesoderm and unsegmented seg- 24: compoundcilia: taxa with and without multiciliateepider- mented animals lacking 4d-mesoderm mal cells 28: body with segments added successively from a teloblastic 28: terminal mouth with radial pharynx: taxa with and without growth zone: unsegmented and segmented animals terminal mouths and various pharynx architectures 29: of segmental longitudinal muscles developed from rows 42: sperm mitochondrial interpolation: taxa with and without mesodermal pockets from the archenteron; taxa with and with- sperm out archenteron derived mesoderm 43: male sex reduced or absent: hermaphroditic taxa without 30: body archimeric: coelomate and non-coelomate animals males and gonochoristic taxa with males

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44: retroperitoneal gonads with gonocoel: taxa with and with- 41: mouth terminal, pharynx radial: taxa with and without ter-

out coeloms and peritoneum minal mouths and with diverse pharynx constructions

45: adult brain derived with 43: with cross-striated attached from/associated apical organ: taxa pharynx muscles, to jaw ele-

with and without and adult brains ments with and without attached apical organs by epithelial cells: taxa muscles

46: dorsal nerve concentratibn/brain behind apical organ/api- to epithelial cells

cal with and without 45: with and pole: taxa apical organs and adult brains introvert spines, teeth, scalids: taxa with and with-

47: collar-shaped pharyngeal brain: taxa with brains of diverse out introverts

construction and lacking brains 46: non-inversible mouth cone with cuticular ridges and spines:

48: taxa with and without introverts orthogonal nervous system: taxa with and without central-

49: notochorda: with and without chorda ized nerve concentrations, cords or ganglia taxa

52: limbs articulated with 49: caudal and without intrinsic muscles: taxa with and with- gangliomtaxawith caudally located gan-

glia out limbs

from associated with and without 53; adult brain derived or with larval 51: protostome apical organ: taxa apical or- apical

organ/apical taxa with and without and adult gans pole: apical organs

brains 56: frontal gland system: taxa with and without frontally lo-

55: dorsal nerve concentration/brain behind cated glands apical organ/api-

cal taxa with and without 60: association with crustaceans: taxa in all pole: apical organs living places ex- 57: brain collar shaped: taxa with brains of diverse construc- cept in association with crustaceans tion and without brains

58: proto-, deuto- and tritocerebrum: taxa with brains of di-

verse construction and without brains Absence in Sørensen et al. (2000) unspecified 59: haemal system: taxa with and without coeloms

(31 characters: 47%): 60: mixoceel; taxa with and without coeloms

61: heart with coelomic pericardiuim: taxa with and without

coeloms 7: with and synapses with acetylcholine: taxa without nerve 62: haemal with axial with cells system complex: taxa and without

coeloms 14: cuticle with taxa general body collagen: with different cu- 66: with coelomic metanephridia restricted to a ticle composition and without cuticle compartment sacculus: taxa with and without metanephridia 15: general body cuticle with chitin: taxa with different cuticle

composition and without cuticle

17; cuticle molted: taxa with and without cuticle

18: trunk without cuticle: taxa with and without cuticle Absence unspecified in Peterson & Eernisse with 21: gonads separate gonoductsL taxa with differentgonad (2001) (71 characters: 51.4%): and organizations gamete outlets

coelom 22: gametes pass through and metanephridia: taxa with The ofcharacters shows different majority inapplicability problems with gamete outlets and with or without coeloms the with respect to outgroups (Fungi, Choanoflagellata). from 25: sperm anteriorly inserted flagellum: taxa with aflagellar Apart those there within the Metazoa and are problems for many charac- sperm flagellum attached in position other than anteriorly

ters as well: 26: spiral cleavage with 4d-mesoderm: taxa with and without 7: water-canal system: taxa with and without choanocytes mesoderm and with different cleavage types 10: of 29: larva “acoelomorph” type ciliary rootlet: taxa with and with- or adult with downstream-collecting ciliary bands of out cross-striated rootlets compound cilia on multiciliate cells: taxa without epidermal ciliary 14; cilia densely multiciliatedepidermis; taxa without ciliated epi- or monociliatedepidermal cells dermis and with 30: monociliate epidermis larva or adult with upstream-collecting ciliary bands with 15: distinct in cilia: with and cilia “step” taxa without locomotory single on monociliate cells: taxa without epidermal cilia cilia or multiciliated epidermal cells

19: centriole: with 35: with spermatozoa without accessory taxa and body segmented serially repeated organs developed without trom 4d-mesoderm (or ectomesoderm);'taxa with and without sperm

4d-mesoderm 21: perforatorium: taxa with and without acrosomes

23: with 36: with gonads present gametes passing through coelom and body successively added segments developed from a teloblastic metanephridia: taxa with and without gonadsand diverse gamete growth zone: segmented taxa without teloblastic release mechanisms growth and unsegmented taxa 37: 29: spiral cleavage: taxa with distinct cleavage body with segmented longitudinal musculature developed types

from 30: annelid cross: taxa with and without spiral cleavage rows ofmesodermal pockets from the archenteron: taxa

molluscan with and without with and without archenteron-derived mesoderm 31; cross: taxa spiral cleavage

38: 36: endomesoderm derived from gut: taxa with and without body archimeric: taxa with and without coeloms

39: with endomesoderm tentaculated mesosome: taxa with and withoutmesosome

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38: 4d endomesoderm: taxa with endomesoderm from diverse 101: nerve cells organized into distinct ganglia: taxa with and

without cells sources nerve

39: from 4d: and 102: brain with anterior and mesodermal germ bands derived taxa with circumpharyngeal posterior rings without 4d-derived mesoderm ofperikarya separated by a ring of neuropil: taxa with brains of

40: lateral coelom derived from mesodermal bands: taxa with different constructions and without brains

103: ventral with and without centralized and without mesodermal bands (irrespective ofsource) and lateral nervous system: taxa coeloms nervous concentrations

104: taxa with and without 43: somatoblast: taxa with and without spiral cleavage circumesophageal nerve ring: cen-

46: with muscles the tralized nervous concentrations apical organ extending to hyposphere: taxa

106: dorsal associated with the with nervous cord/ganglion mesosome: and without apical organ

taxa with and without 47: pretrochal anlagen: taxa with and without trochophorelarvae mesosomes 109; tanycytes: taxa with and without introverts 48: prototroch: taxa with and without larvae 114: closed system with dorsal and ventral blood 49: metatroch: taxa with and without trochophore larvae circulatory vessels: taxa with and without hemal systems 50: adoral ciliary band: taxa with and without trochophorelarvae 128-136: characters for differentiations of Hox 51: telotroch: taxa with and without larvae coding genes and clusters: with without Hox taxa ans genes 52: neurotroch: taxa with and without trochophore larvae

53: neotroch: taxa with and without larvae

54: nonmuscularperitoneal cells in lateral regions of coelom: taxa with and without coeloms and peritoneum Absence unspecified in Giribet et al. (2000) (data

55: trimery: taxa with and without coeloms set from Zrzavý et al., 1998) (74 characters:

56: mesocoelomic ducts and taxa with and without meso- pores: 26.8%): coels

57: ciliated extensions ofthe mesocoel: taxa with and without

5: radial cleavage: taxa with distinct cleavage mesocoels types

6: spiral cleavage: taxa with distinct cleavage types 58: lophophore: taxa with and without mesocoels 7: spiral-quartet cleavage: taxa with distinct cleavage types 59,61 -65: characters codingfor variationin lophophoremorpho- 14: blastopore forming mouth and anus by fusion oflateral lips: logy: taxa with and without lophophore taxa with different blastopore fates 68: protonephridia with channel cell completely surrounding 15: blastopore forming anus: taxa with distinct blastopore fates lumen: taxa with and without protonephridia 18: with body segmented serially repeated organs developed 69: axial complex: taxa with and without coeloms and hemal

from 4d-mesoderm or ectomesoderm: taxa with and without systems segments and different mesoderm sources 70: hydropore: taxa with and without protocoel 19: entomesoblast (4d/2d): taxa with and without spiral cleavage 71: paired hydropores; taxa with and withoutprotocoel 20; mesoderm formed from archenteron: taxa with distinct cleav- 72: with with- metanephridia open through metacoel: taxa and

age types out metanephridia and metacoels 23: metameric coelomic cavities; taxa with and without coeloms 73: metanephridiawith coelomic compartmentrestricted to sac- 24: teloblastic segment-forming zone: taxa with and without culus: taxa with and without metanephridia segments 75: mantle sinuses with gonads: taxa with and without mantles 26; segmented longitudinal musculature developedfrom archen- 76; innerepithelium secreting periostracum: taxa with and with- teric mesodermal pouches: taxa with and without archenteron- out mantles derived mesoderm 77: calcareous valves, which rotate about a hinge axis: taxa 30: coelom: taxa with and without mesoderm with and without mantles

gonocoel:taxa with disparate gonadconstructions and lacking 78: cuticle with chitin: taxa without cuticles and with different 31: gonads cuticle compositions 32: eucoelomatic condition: taxa with and without coeloms 79: trilaminate epicuticle: taxa with and without cuticles 33: coeiomocytes: taxa with and without coeloms 80: trilayered epicuticle: taxa with and without cuticles 35: haemal system: taxa with and without coeloms 81: collagenous basal layer: taxa with and without cuticles

36: mixocoei: taxa with and without coeloms 83: eedysis: taxa with and without cuticles 37: bilaterally paired coelomic primordia: taxa with and with- 86: head divided into three segments: taxa with and without

out coeloms segments and heads

87: 38: heart with coelomic taxa with and without terminal mouth: taxa with and without terminal mouths pericardium:

89: oral cone: taxa with and without introvert coeloms

42: haemal with axial complex: taxa with and without 93: digestive gut without cilia: taxa with and without digestive system

hemal and coeloms gut systems

94: anus: taxa with and without digestive tract 50: metanephridia with coelomic compartments restricted to

97: synapticules: taxa with and without pharyngeal gill bars sacculus: taxa with and without metanephridia 100: with and without acetylcholine used as a neurotransmitter: taxa with and 51: serially repeated nephridiopores: taxa ne- without nerve cells phridia

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57; ultrafiltration with and without through podocytes: taxa 157: endodermal ring canal in medusa: taxa with and without podocytes medusae

65: mouth/esophagus with cuticle of spiny/toothed consisting 161: podocysts: taxa with and without polyps

chitin: taxa with crystalline and without cuticle 162: pedalia; taxa with and without medusae 75: with and without introvert tanycytes: taxa 186; compound cilia: taxa without epidermal cilia and with

86: bipartite body: taxa with distinct body architectures monociliate cells

88: with intovert scalids: taxa with and without introverts 193: cuticle taxa simple or two-layered: with and without cu-

89: non-inversible mouth taxa with cone: and without introvert ticle scored for simple cuticle 93: tripartite body and coelom; taxa with and without coeloms 194: cuticle: taxa with collagenous differently constructed cu- 94: taxa with and without lophophore: mesocoels ticle and lacking cuticle

99: articulated and limbs: with and segmented taxa without limbs 195: chitinous cuticle: taxa with differently constructed cuticle

108: gonadswith separate gonoducts: taxa with distinct gonad and lacking cuticle architectures and outlets gamete 196: articular molting: taxa with and without cuticle

109: coelom and with gametes poas through metanephridia: taxa 199: dorsal cuticle with aragonite spicules: taxa with and with-

and without coeloms and metanephridia out cuticle

112: taxa with and without permanent gonopore: gonads 202: cuticular sclerite formation: taxa with and without cuticle

113: taxa with and without coelomic gonopericardial system: 203: sclerotization of cuticle with tannin proteins: taxa with pericardium and without cuticle

117: filiform taxa with diverse forms of 204: cuticle: sperm: sperm myelinic taxa with and without cuticle

118: acanthocephalan of taxa with diverse forms characters type sperm: 214-216,219: coding for nematocystdifferentiations:

of with sperm taxa and without nematocysts

119: of clitellate type sperm: taxa with diverse forms of 230-231: characters for with sperm coding synapses different neuro-

127: males: taxa with males and taxa without with hermaphroditic transmitters: taxa and without nerve cells

males (present state) 235: single pair ofventral cords: taxa with and without ventral

134: taxa with and planula larva: without larvae nerve cords

136: larvae/adultswith cilia: 237: cerebral taxa downstream-collecting compound ganglion: with and without centralized nerve

taxa with monociliate epidermal cells and with nonciliate epi- concentrations

dermal cells 239: dorsal neural tube: taxa with ventral nerve cords and with-

137: larvae/adults with upstream-collecting single cilia taxa out nerve concentrations

lacking ciliated cells and with 240: brain: with epidermal multiciliatedepider- collar-shaped taxa diverse brain constructions

mal cells 241: proto-, deuto- and tritocerebrum: taxa with diverse brain

138: trochophora: taxa with and without larvae constructions

143: larva: with dipleurula taxa and without larvae 244: caudal ganglion; taxa with and without caudally located 145: adult brain derived from/associated withlarvalapical organ/ ganglia

taxa apical pole: with and without adult brains and 248: lateral taxa with apical organs nerve cords: and without nerve cords

146: larval apical into with and 252: number of organ incorporated brain: taxa statoliths: taxa with and without statoliths without adult brains and apical organs 253; number of statocyst parietal cells: taxa with and without

153; with and without polyp pharynx: taxa polyps statocysts

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