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Macroevolution of Animal Body plans

Jenner, R.A.

Publication date 2002

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Citation for published version (APA): Jenner, R. A. (2002). Macroevolution of Animal Body plans. Grafische Producties, UvA.

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Download date:30 Sep 2021 Chapterr 7

Bilateriann Phylogeny and Uncritical Recyclingg of Morphological Data Sets s

Ronaldd A. Jenner

Publishedd in Systematic Biology 50: 730-742 (2001)

141 1 142 2 SjB-f.. BW. 5«5>:73O-7«.20Ol

Bilateriann Phylogeny and Uncritical Recycling of Morphological Dataa Sets

RONALDD A. JENNER InstituteInstitute for Biodiversity and Ecosystem Dynamics, University of Amsterdam. P.O. Box 94766,1090GT, Amsterdam, TheThe Netlierlands; E-mail: jcnner9science.uva.nl

DATAA QUALITY, DATA RECYCLING, AND clusivelyy based on the morphological data of DATAA MATRIX COMPILATION Zrzavyy et al. (1998); and Sorensen et al. (2000),, adopting a modified version of the Thee vitality of systematic biology as a sci- dataa set of Nielsen et al. (1996). Indeed, encee depends on our invested efforts to en- observingg that previously compiled data suree the quality of the input data of our anal- setss are recognized as valuable sources of yses.. When insufficient attention is directed phylogeneticc information is encouraging towardss the construction of the data matrix, andd could signify the continual refinement properr interpretation of the results of cladis- andd consolidation of an increasingly ma- ticc analyses becomes impossible. Neverthe- turingg morphological data set. However, less,, some systematists have argued that severall critical comments are in order. modemm systematics is increasingly charac- Inevitably,, any morphological phyloge- terizedd by a shift of emphasis from observa- neticc analysis of higher-level animal taxa tionn as the source of the data matrix to what hass to rely largely on information assembled cann be inferred from the data matrix after its fromm the published literature. One should be constructionn (e.g., see Patterson and Johnson, cautious,, however, in extracting character in- 1997;; Grande and Bemis, 1998; Rieppel and formationn from the literature, especially from Zaher,, 2000). The current availability of an dataa sets previously compiled by different unprecedentedd amount of comparative data authors.. Yet, the recent phylogenetic analy- andd ever-increasing computing powers may sess listed above did not always attempt to havee largely fostered such a shift. explicitlyy and critically evaluate or reevalu- Itt may therefore not be unexpected to atee the recycled data matrices. Of course, a discernn a tendency among recent phylo- practicall problem is apparent. The vastness geneticc studies of higher-level animal re- off the ever-expanding field of invertebrate lationshipss (both morphological and total zoologyy makes it increasingly difficult and evidencee approaches) to use morphologi- timee consuming to obtain a complete first- call characters garnered from character lists handd overview and appreciation of compar- previouslyy compiled by different authors as ativee data for higher-level phylogenetic stud- raww data for new phylogenetic studies. A iess of the Metazoa. Nevertheless, insufficient partiall list might include Eemisse et al. attentionn to the quality of the data set may (1992),, strongly relying on Brusca and Brusca stronglyy impair the quality of the resulting (1990)) and Meglitsch and Schram (1991); phylogenies. . Kimm et al. (1996), relying principally on Thee morphological matrix of Zrzavy et al. dataa from Brusca and Brusca (1990), Eemisse (1998;; ZEA) is especially important, compris- ett al. (1992), and Wheeler et al. (1993); Sund- ingg 276 characters and representing the most bergg et al. (1998), relying on Brusca and comprehensivee morphological data matrix Bruscaa (1990); Zrzav^ et al. (1998), chiefly forr the Metazoa compiled to date. Their mor- relyingg on data derived from Meglitsch phologicall data set has been incorporated andd Schram (1991), Schram (1991), Eemisse intoo several new phylogenetic studies of the ett al. (1992), Backeljau et al. (1993), Schram Metazoaa (Giribet, 1999; Giribet et al. 2000), andd Ellis (1994), Nielsen (1995), Rouse and andd the phylogenetic results of this latter Fauchaldd (1995), Nielsen et al. (1996), Ax often-citedd study have already been used as (1996),, Haszprunar (1996a, b), Wallace et al. aa framework for interpreting different as- (1996),, and Gilbert and Raunio (1997); Giribet pectss of animal evolution (de Queiroz, 1999; (1999)) and Giribet et al. (2000), which are ex- Vermeijj and Lindberg, 2000). Determining

143 3 thee quality of this matrix thus becomes criti- att integration or quality assessment of pri- cal.. Below I will demonstrate legitimate rea- maryy homologies hinders the discrimina- sonss for questioning the quality of this ma- tionn of valuable and problematic data. The trixx and show that its uncritical recycling se- matrixx is chiefly based on syntheses, espe- riouslyy compromises several important re- ciallyy other phylogenetic analyses and text- sultss from the latest phylogenetic analysis of bookss (see listing above). It is impossible to bilateriann relationships (Giribet et al., 2000; tracee the exact source of character informa- GEA),, recently published in this journal. I tionn in the matrix, and none of the charac- willl refer to particular characters from the terr definitions are discussed. ZEA (p. 251) matrixx of ZEA as ZX, where X is the number write,, "The original data were not reanalyzed off the character in the matrix of ZEA. priorr to analysis...." This is a problem be- Insufficientt attention to data matrix con- causee various authors have shown that sev- structionn and uncritical use of data matrices sera ll of the sources of the matrix suffer from off other authors is especially problematic for aa range of difficulties (e.g., see Rouse and phylogeneticc analyses of higher-level taxa. Fauchald,, 1995; Nielsen et al., 1996; Jenner Browerr (2000:15) writes about "characters as andd Schram, 1999). Nevertheless, ZEA's ma- observations"" to highlight the link between trixx was adopted without change by Giribet dataa matrix entry and its empirical support in (1999)) and GEA. phylogeneticc analyses. However, for phylo- Givenn the impossibility of assessing the geneticc studies of higher-level taxa, to equate qualityy of a morphological matrix by ap- characterss with observations is an oversim- pealingg to general principles, I will offer a plification.. Observations on characters are fil- broadd range of examples for diverse taxa and teredd through multiple layers, often implicit, characters.. Nevertheless, I will propose sev- off interpretation in their transformation to a erall general and related categories of prob- definitivee data matrix entry. The scoring of lemss associated with this large morpholog- aa single 0 or 1 for a given supraspecific ter- icall data matrix, the recognition of which minall taxon in the matrix may encapsulate willl be essential for a proper evaluation of aa variety of information and interpretation, thee phylogenetic results of ZEA and GEA. includingg synopses of the extent and impor- II will specifically illustrate the problems in- tancee of character variation within terminal volvedd by briefly discussing several of the taxa,, the internal phylogenetic relationships majorr conclusions from the recent study withinn the terminals along with their bearing off GEA. onn the reconstructed ground patterns that are scoredd in the matrix, the density and relia- bilityy of original observations for the termi- Theory-DrivenTheory-Driven Scoring Without nall units (e.g., recent or old literature), the EmpiricalEmpirical Support adoptedd strategy for character selection, and Thesee problems refer to data matrix en- thee many difficult decisions of character cod- triess that are largely or wholly determined ingg of complex features that may be function- byy a priori assumptions of character evolu- allyy and structurally linked. Recycling of any tion.. For example, among the taxa scored morphologicall data matrix for use in a new presentt for Z93 (tripartite body and coelom) studyy would supposedly logically imply a aree the chordates. The trimeric, archimeric, fulll agreement with all the decisions that fed orr oligomeric organization of the ances- intoo construction of the matrix. When these trall deuterostome has played an important issuess are not explicitly confronted, however, rolee in hypotheses about the evolution of thee data matrix is reduced to a black box. If thee chordate body plan (e.g., Nielsen, 1995; ourr goal is to deepen our understanding of Presleyy et al., 1996). However, the scoring thee evolution of metazoan morphology and off chordates for possession of a trimeric phytogeny,, we need to scrutinize the many organizationn is not rooted in observations, facetss of data matrix construction (Jenner and butt represents an evolutionary inference Schram,, 1999). contingentt upon the nesting of chordates withinn a dade of arguably trimeric nonchor- PROBLEMSS WITH THE MORPHOLOGICAL datee invertebrates: Brachiopoda, Phoronida, DATAA MATRIX OF ZEA Pterobranchia,, Enteropneusta, and Echin- Althoughh ZEA's data matrix unites dis- odermata.. Neither ontogeny nor morpho- paratee information, the lack of any attempt logyy illustrates the trimeric nature of the

144 4 bodyy in Urochordata, Cephalochordata, and thesee three taxa. However, when we con- Vertebrata.. Rather, cephalochordates and siderr the scoring of Z38, a striking incon- vertebratess elaborate a metamericbody plan, gruencee is revealed. The broad scoring of whereass even the presence of coeloms in uro- Z388 in ZEA across Protostomia (molluscs, chordatess awaits confirmation (Welsch, 1995; annelids,, onychophorans, arthropods) and Presleyy et al., 1996; Burighel and Cloney, Deuterostomiaa (urochordates, vertebrates) 1997).. The scoring of trimery in the matrix of justifiess a broad character definition— ZEAA in these taxa is therefore without any aa definition that would encompass both empiricall support. Consequently, the opti- anatomicallyy restricted hearts with a special- mizationn of this character as the only po- izedd pericardium, such as in molluscs, and tentiallyy unique synapomorphy for a clade muscularr longitudinal blood vessels referred off (Phoronida Brachiopoda Hemichordata too as hearts with a relatively nonspecialized Echinodermataa Chordata) (Bryozoa is scored "pericardium,''' that is, composed of the lin- "?")) in the morphological and total evidence ingg of the body coelom, such as found in analysess of ZEA should be reevaluated. polychaetes.. In view of this broad definition, Otherr recent studies exemplify similar errors. thee scoring for various other taxa remains Thee characters are often easily diagnosed by unexplained,, especially echinoderms, ptero- thee adjective "modified," or something simi- branchs,, and enteropneusts, which are incor- lar,, and such identifying statements of "mod- rectlyy scored in ZEA as lacking a heart with ifiedd spiral cleavage" for crustaceans (Valen- aa coelomk pericardium. tine,, 1997:8001), cleavage of the "distorted AA second instance of data matrix incon- spirall type" in acanthocephalans (Cromp- sistencyy concerns characters Z43 (podocytes) ton,, 1989:254), or "modified enterocoely" in andd Z57 (ultrafiltration through podocytes), phoronidss (Williams et al., 1996) should in- incidentallyy involving the same terminal stilll caution in the interpretation of the evo- taxa.. Pterobranchs and echinoderms are both lutionaryy significance of these features. scoredd as possessing ultrafiltration through podocytess and also as lacking podocytes. Third,, urochordates are scored as possess- DataData Matrix Inconsistency ingg longitudinal muscles along the chorda Morphologicall data matrices may include andd undulatory movement of the finned tail conflictingg characters for two distinct rea- (Z83),, but scored as "?" for a chorda (Z78). sons:: (1) homoplasy, that is, meaningful andd properly scored potential synapomor- phiess refuted by character congruence, and ImpreciseImprecise Character Definitions and (2)) poorly identified and scored characters. InsufficientInsufficient Attention to Primary Homology Therefore,, the most potent method for iden- Ann important flaw of the morphological tifyingg careless data matrix construction is to matrixx of ZEA is the absence of explicit char- scann it for characters that actively contradict acterr definitions. The only information is eachh other. Here I discuss three examples of thee name given to the character. This makes this. . itt virtually impossible to assess the merit Thee first involves two characters and at off the primary homology assessments that leastt three independently incorrectly scored constitutee the data matrix. Although some taxa.. Z38 codes the presence of a heart with characterss are not a problem, for example, aa coelomk pericardium, and Z42 codes the protonephridiaa (Z48), the precise meaning presencee of a hemal system with an ax- off many other characters cannot be eval- iall complex. A hemal system with an axial uated.. Two particularly clear examples of complexx refers to a blood vascular system lackk of attention to primary homology are as thatt is structurally and functionally linked to follows. . aa set of coelomk spaces, together termed Evenn the scoring of a character with an os- thee axial complex (Nielsen, 1995). One of tensiblyy straightforward definition such as thee fundamental components of this com- positionn of the anus as anterior/dorsal or plexx structure is a heart surrounded by a posteriorr (Z73) can mask many difficulties coelomk:: pericardium, and the axial complex off interpretation. Although explicit specifi- iss uniquely present in enteropneusts, pter- cationn is lacking, the scoring indicates that obranchs,, and echinoderms. ZEA correctly thee character refers to adult morphology. scoree this complex character as present in Suchh broad-scale comparison of adult anus

145 5 positionn across the Bilateria is complicated Becausee the analysis of GEA is specifically byy the changing body axis orientation during aimedd at resolving the phylogenetic place- thee ontogeny of many of the scored taxa (or mentt of acoelomates and aschelminth taxa, evenn the complete loss of the larval anus dur- includingg the recently discovered phylum ingg metamorphosis). This can be illustrated Cycliophora,, the exertion of special care in byy addressing the difficulty of substantiat- thee scoring of characters for these taxa is ingg the primary homology of an anterior/ critical,, especially those features pertaining dorsall anus even for the most closely related too body cavity organization. Yet, a pseudo- taxaa that share this feature, the two sister coelomm (Z34) is still coded as a diagnosable groupp pairings in the morphological anal- character.. The definitional problems associ- ysiss of ZEA: (Brachiopoda Phoronida) and atedd with this character do not justify its (Cycliophoraa Entoprocta). codingg as a separate character (see discus- Nielsenn (1991) drew attention to the sionss in Ruppert, 1991a; Ahlrichs, 1995; Ax, factt that the anterior/dorsal anuses of Bra- 1995).. Ultrastructurally, there is no sharp dis- chiopodaa (Inarticulata) and Phoronida arrive tinctionn between the acoelomate and pseu- att their adult position through very different docoelomatee organizations, which constitute ontogeneticc pathways, providing little basis differentt points along a continuum of non- forr proposing primary homology of adult coelomatee organization. Both can be desig- anuss position. Brachiopod metamorphosis natedd as primary body cavities lined by ex- (exemplifiedd by Crania anomala) involves thtracellulae rr matrix. A primary body cavity shorteningg of the ventral side of the body, mayy range from a virtual absence of any whereass in phoronids the dorsal side is ex- cavityy (so-called acoelomate organization), tremelyy shortened. The scoring in ZEA to- suchh as the very narrow interstitial spaces tallyy ignores the change in position of the inn gnathostomulids, to a more spacious cav- anuss with respect to the larval body axes in ityy such as found in priapulids (pseudo- phoronidss and brachiopods. Second, scoring coelom).. Even according to these graded dis- off the sister taxa Cycliophora and Entoprocta tinctions,, cycliophorans and kinorhynchs are forr anterior/dorsal anus may seem at first misscoredd in ZEA as possessing a pseudo- glancee more defensible, based on the super- coell (see Kristensen and Higgins [1991] for ficiall morphologies of the adults, but com- kinorhynchs;; Funch and Kristensen [1995, plexx problems remain. The anterior/dorsal 1997]] for cycliophorans). These consider- anuss of the entoproct adult directly corre- ationss necessitate the rescoring of other spondss to the posterior position of the anus noncoelomatess in the matrix of ZEA; more- inn the larva before metamorphosis (Nielsen, over,, in view of larval body cavities in coelo- 1971),, but the anteroposterior axis of the cy- matess (see below) and the presence of a spa- cliophorann feeding stage (adult) is developed ciouss primary body cavity in various adult diametricallyy opposite to the anteroposterior coelomatess such as the molluscan hemocoel axiss of the pandora larva in which it devel- (Salvini-Plawenn and Bartolomaeus, 1995), opss in the asexual part of the life cycle (Funch mostt of the Bilateria would have to be andd Kristensen, 1997). Any relationship of rescored. . bodyy axes between the adult feeding stage Otherr characters with very unclear defi- andd the chordoid larva from which it devel- nitionss include terminal differentiation, Z2; opss in the sexual part of the life cycle is ob- regularr metagenesis, Z130 (coding urochor- scuredd by the degeneration of the chordoid datess and cycliophorans despite the lack of larvaa after it settles on a host Moreover, none anyy developmental and morphological sim- off the cycliophoran free-living stages devel- ilarities);; prevalence of the left body side, opss a digestive system. A meaningful com- Z84;; specific type of cnidocyte morphogene- parisonn of adult anus position without at- sis,, Z213; eutely, Z10 (organs or organisms?); tentionn to ontogenetic changes is obviously bipartitee body, Z86 (scored for such dis- nott straightforward. Furthermore, relating tinctlyy differently organized animals as the thee presence of broadly U-shaped guts with noncoelomatee kinorhynchs and coelomate considerationss of ecology and functional chaetognaths);; mono- and biphasic life cy- morphologyy in different taxa would only cles,, Z131 (character states in the literature lessenn the probability for scoring anterior/ havee been variously defined on the basis dorsall anus as a primary homology across off ecological, morphological, or functional Bilateria. . criteria,, creating substantial confusion in

146 6 studiess of metazoan life cycle evolution differentt effects on the outcome of a phy- [McEdwardd and Janies, 1993]); primary logeneticc analysis. The prevailing tendency larvaee Z133 (see Jenner, 2000; and be- iss to score adults and larvae as separate low);; and dipleurula larvae, Z143 (known lifee cycle stages. When no life cycle stage is ass a hypothetical ancestral deuterostome specified,, one has to guess from the charac- larvall type that is misscored for Ptero- terr scoring what life cycle stages are being branchiaa if an explicit character definition compared. . iss adopted [Nielsen, 1995; Salvini-Plawen, Forr example, some characters apparently 1998J). . codee only the adult stage. Z270 codes the life habitt (free-living or ecto- or endoparasitic) off the taxa, scoring exclusively ectopara- LifeLife Cycle Stages and Character Codingsitis mm for Myzostomida, which nevertheless Thiss subject deserves more attention by possesss free swimming larvae. Z247 scores workerss on metazoan phylogeny. It relates thee presence of a basi-epithelial nervous too how the phylogenetic significance of mor- system,, mainly for deuterostomes and phologicall characters depends on which part lophophorates.. First, there are misscorings off the life cycle is used for comparison. An off the adult stage, such as Chaetognatha ingrainedd concept of phylogenetic systemat- (Salvini-Plawen,, 1988; Shinn, 1997), icss is that only "comparable semaphoronts" Loriciferaa (Kristensen, 1991), and Priapulida (definingg a semaphoront as an organism at (Storch,, 1991). Moreover, the scoring of aa particular stage in the life cycle) should Z2477 ignores the observations of the basi- bee compared (Wiley, 1981:119). Although epitheliall position of many regions of the thiss idea has a pedigree going back to centrall nervous system in many proto- Hennig'ss original conceptualizations of phy- stomes,, particularly during earlier stages logeneticc systematics, that does not make off ontogeny (Nielsen, 1995). Z34 codes the itt well-founded, at least not for all phylo- presencee of a pseudocoel and scores a geneticc levels. A consideration of the em- restrictedd set of noncoelomate taxa such piricall evidence marshalled in support of ass kinorhynchs, loriciferans, and rotifers. thiss premise by Hennig (1966) makes strik- Ignoringg the problems of definition of inglyy clear that the relevance of this con- thiss character for the moment (see above), ceptt for higher-level animal phylogenetics whenn entire life cycles are being consid- iss far from obvious. The concept is usu- ered,, this feature should also be scored as allyy illustrated by examples from animals presentt in coelomates, where it is observed withh relatively simple life cycles (tradition- inn the larvae before they develop their allyy characterized as direct development), es- coeloms. . peciallyy arthropods (insects) and vertebrates Forr these three characters the implicit as- (Hennig,, 1966). These examples deal with sumptionn is to score adults only, although relativelyy closely related species in which aa viable alternative would call for scoring thee correspondence of life cycle stages (lar- acrosss the entire life cycle. The choice should vae,, juveniles, adults) is relatively clear-cut. bee explicitly justified, because it directly de- Thee situation is much more complicated for terminess the phylogenetic significance of the higher-levell animal taxa, there being no gen- characterss involved: Scoring the character erallyy accepted theory of life cycle evolution. acrosss all life cycle stages would result in po- Suchh a theory is necessary for a proper un- tentiall synapomorphies for a more encom- derstandingg of the correspondence of life cy- passingg set of taxa man that obtained when clee stages across the Metazoa. Until we de- onlyy adults are scored. Other characters ap- velopp such a theory, evaluating the value of parentlyy do score across the entire life cy- thee prescription that "larvae can only be com- cle,, such as Z48, which records the pres- paredd with larvae and adults with adults" encee of protonephridia. The current scoring (Bartolomaeuss and Ruhberg, 1999:172) will recordss both taxa where protonephridia can remainn very difficult when comparing ani- bee argued to be present in the adult ground malss with diverse life cycles, such as the di- patternn (e.g., Priapulida, Kinorhyncha, En- rectlyy developing arthropods and the indi- toprocta)) and taxa where published reports rectlyy developing polychaetes. What is clear, providee support only for their presence in however,, is that different decisions about thee larval ground pattern (e.g., actinotro- comparabilityy of life cycle stages will have chh larva of phoronida, trochophora of

147 7 Molluscaa and Echiura, and chordoid larva of ZEAA scored Nemertea for two charac- Cycliophora). . terss associated with the presence of stato- AA satisfactory hypothesis of the relation- cystss (Z252, Z253). This necessarily implies shipp between the nature of metazoan life thee presence of statocysts in the ground cycless and cladistic character coding for patternn of Nemertea, which proves to be higher-levell phylogenetic analyses has not aa very questionable assumption. Tradition- yett been developed. Such a hypothesis, ally,, Nemertea is divided into two groups, however,, is necessary to justify our choice thee Anopla and Enopla. However, we cur- off semaphoronts for coding characters for rentlyy lack a cladistically framed phytogeny cladisticc analyses. For example, if we fol- off trie Nemertea, which makes it very dif- loww the recent hypothesis that all ecdyso- ficultt to deduce the presence of statocysts zoanss (moulting protostomes) have secon- inn the nemertean ground pattern from their darilyy lost their larval forms (Peterson et al., occurrencee in only two interstitial genera 2000),, than the recent claim justifying the off hoplonemerteans (Enopla) (Otonemertes comparisonn of "larval" arthropods and an- andd Ototyphhnemertes) (Turbeville, 1996). Al- nelidd larvae (Bartolomaeus and Ruhberg, thoughh it is not uncommon to extrapolate 1999)) has to be questioned. Therefore, it characterss present in any of the members of a wouldd be instructive to study whether the higherr taxon to be part of the ground pattern choicee of semaphoronts in recent phyloge- off that higher taxon, that strategy can be jus- neticc analyses of the Metazoa is consistent tifiedd only in the absence of conflicting data. withh our current understanding off metazoan Here,, the choice for two hoplonemerteans as lifee cycles. representativess of the nemertean ground patternn is at the very least completely arbitrary. Scoringg nemerteans as absent (accepting the GroundGround Patterns o/Higlter Taxaevolutio and nn of statocysts within the Nemertea) CharacterCharacter Variation orr polymorphic (reflecting absence of stato- Onee of the most important but difficult as- cystss in virtually all nemerteans) are viable pectss of using higher-level taxa as terminals alternativee character scorings. inn a phylogenetic analysis is related to decid- Inn contrast, the scoring of various lar- ingg to code either ground patterns or exem- vall characters for nemerteans such as pro- plarr species (e.g., seee Yeates, 1995; Bininda-totrochh developed as ciliated lobes (Z139) is Emondss et ah, 1998; Wiens, 2000; see also basedd on controversial information from het- Dayratt and Tillier, 2000, for an especially eronemerteann pilidium larvae (Anopla; see, strikingg case study). The ground pattern is e.g.,, Nielsen, 1998; Rouse, 1999). Another thee set of characters primitively present in a examplee is the scoring of compound cilia clade,, irrespective of its phylogenetic level. forr Nemertea (Z186). So far, compound cilia Thesee characters may include both ances- havee been described only from pilidium lar- trallyy inherited plesiomorphies and newly vaee (Nielsen, 1987), which are not considered evolvedd apomorphies for that clade. When too be present in the nemertean ground pat- codingg ground patterns, these have to be ternn (Ax, 1995; Nielsen, 1995). deducedd or assumed for all characters for AA final illustration of arbitrary character alll terminals before performing phylogenetic scoringg relates to the cytology of muscles, analysis.. Interestingly, inattention to meth- eitherr smooth or striated (Z261). This is a odss of ground pattern reconstruction may highlyy variable character both within and liee at the heart of conflicting phylogenetic betweenn higher-level taxa and is difficult to hypothesess (Jenner and Schram, 1999). The scoree this character without polymorphisms matrixx of ZEA exhibits strictly unambigu- inn the absence of explicit justification. For ouss data entries, that is, no scored poly- example,, the unambiguous scoring of stri- morphismss (distinct from the ?'s), and ZEA atedd muscle for polychaetes in the matrix of (p.. 252) explain that character information ZEAA ignores the common presence of smooth iss extrapolated to "whole 'phyla' if counter- muscless in polychaetes (Gardiner, 1992). evidencee is absent." However, using the un- ambiguouss scorings to instill confidence in thee robustness of the data entries would be MiscellaneousMiscellaneous Misscorings misleading.. A few examples will illustrate Althoughh a variety of dubious or incor- this. . rectt data matrix entries can be understood

148 8 ass manifestations of a few general classes of terpretationss in recent phylogenetic studies problems,, a hotchpotch of problematic char- off the Metazoa (Jenner and Schram, 1999; acterr codings and scorings remains. A selec- andd in prep.). Many of these issues are not tionn of examples from diverse taxa and char- uniquee to the matrix of ZEA, but it is es- acterss will provide final illustrations of the sentiall to make them explicit if we want to manyy pitfalls involved. usee morphological data to produce robust Radiall cleavage in ctenophores, Z5 (cteno- andd reliable phylogenetic analyses. Admit- phoree cleavage is very distinct from radial tedly,, publishing a matrix that is completely cleavagee [Martindale and Henry, 1997]); freee of accidental mistakes seems hardly pos- presencee of a mixocoel in molluscs, Z36 sible;; however, the above discussion shows (duringg mollusc ontogeny there is no conflu- thatt the information in the data matrix of encee of coelomic and primary body cavity ZEAA should be treated with appropriate spacess [Raven, 1966; Salvini-Plawen and caution. . Bartolomaeus,, 1995]); presence of a postanal taill in enteropneusts, Z85 (the anus is located att the posterior tip of the body [Benito and MORPHOLOGYY AND TOTAL EVIDENCE Pardos,, 1997]); gametes passing through INGEA A coelomm and metanephridia in gastrotrichs Althoughh the study of GEA is a total evi- andd Lobatocerebromorpha, Z109 (both taxa dencee approach to determining bilaterian re- lackk coeloms and metanephridia [Rieger, lationships,, the treatment of morphological 1980;; Ruppert, 1991b]); lack of podocytes dataa is rather limited and minimally trans- inn various taxa such as onychophorans, parent.. It provides neither an explicit list of arthropods,, echinoderms, pterobranchs, includedd characters nor a data matrix illus- andd vertebrates, Z43 (Ruppert and Smith, tratingg the distribution of characters among 1988;; Storch and Ruhberg, 1993; Hessler and taxaa (although a reference to the paper of Elofsson,, 1995; Nielsen, 1995; Benito and Par- ZEAA is included). This makes it virtually dos,, 1997); serially repeated nephridiopores impossiblee to evaluate GEA's morphologi- inn kinorhynchs, Z51 (kinorhynchs possess call and total evidence trees. Although GEA aa single pair of protonephridia [Kristensen claimm to use 276 morphological characters andd Higgins, 1991]); larval planktotrophy in forr their analysis, 69 characters are uniform cycliophorans,, Z135 (cycliophoran chordoid forr Bilateria and therefore uninformative for larvaee completely lack endodermal cells, sortingg their relationships (this excludes vari- lett alone a mouth and anus [Funch, 1996; ablee characters that are autapomorphies, at Funchh and Kristensen, 1997]); absence of leastt in the morphological analysis, for sin- epidermall microvilli in bryozoans and "?" glee terminals), and 27 of these are exclu- inn entoprocts and cycliophorans, Z184 (these sivelyy scored for cnidarians, which were not taxaa do possess epidermal microvilli, and includedd in the analysis. In addition to un- ZEAA do not address why taxa such as arthro-criticallyy recycling the problematic matrix of pods,, onychophorans, and chaetognaths are ZEA,, the phylogenetic significance of none scoredd as lacking epidermal microvilli; the off the morphological characters is discussed microvillii are present and play an important explicitly.. GEA merely provided a few sim- rolee during cuticle formation [Minelli, plee lists of synapomorphies for some of the 1993;; Storch and Ruhberg, 1993; Funch and majorr clades found by their analysis. Nev- Kristensen,, 1997; Mukai et al„ 1997; Nielsen ertheless,, we may still be tempted to con- andd Jespersen, 1997; Shinn, 1997; Schmidt- cludee that the poor quality of the morpho- Rhaesaa et al., 1998]); presence of epidermis logicall matrix did not directly affect the main withh intracellular skeletal lamina in urochor- phylogeneticc conclusions of GEA's total ev- dates,, Z189 (Burighel and Cloney, 1997); and idencee analysis. Unfortunately, ZEA's prob- locomotionn in adult ctenophores muscular lemss are directly manifested in scoring er- ratherr than ciliary, Z258 (Hernandez-Nicaise, rorss for the morphological synapomorphies 1991). . proposedd to support the major bilaterian Thee above examples reveal only part of cladess in GEA. I will illustrate this for the thee problems inherent in the morphological cladess Trochozoa and Platyzoa, for which matrixx of ZEA. More generally, the above nonee of the proposed synapomorphies of listingg presents a cross-section of the intri- GEAA is free of flaws of character coding and catee difficulties associated with character in- scoring. .

149 9 Thee total evidence analysis of GEA found iss understandable as a method to avoid po- (largelyy molecular) support for a mono- tentiall problems of rooting with distant out- phyleticc Platyzoa, a clade of noncoelomates groups,, including the noncoelomate nonbila- definedd by Cavalier-Smith (1998) on the ba- terianss into the analysis would be necessary sissis of a largely intuitive narrative assessmentfo rr a proper optimization of coelom charac- off phylogenetic data. GEA write (p. 551), terss (and other characters that can in princi- "Thee absence of coelom (as defined histo- plee be scored for nonbilaterians) at the base logically)) is the only morphological syrtapo- off the Bilateria. morphyy that might define Platyzoa, although Thee scoring of all three proposed synapo- itss optimization is ambiguous (this character morphiess for Trochozoa (respiratory pig- statee is also present in Entoprocta, Nemer- ments,, hemal system, and primary larvae) todermatida,, Kinorhyncha, Nematoda, and inn GEA is likewise fraught with problems. Nematomorpha;; it is coded as unknown for First,, Z44 codes for the presence of res- Syndermata)."" Three problems are apparent piratoryy pigments. The broad scoring of withh this. taxaa indicates that this character at least First,, ZEA scored the presence of a coelom unitess hemoglobins and hemerythrins. How- inn Priapulida. Although the nature of the ever,, that does not explain the scoring priapulidd body cavity has been the subject notedd for several taxa, such as echinoderms, off some debate over the past few decades, gastrotrichs,, and entoprocts. Hemoglobin applicationn of electron microscopy indicates hass been found in some echinoderms and thatt a spacious primary body cavity rep- gastrotrichss (Ruppert, 1991b; Byrne, 1994; resentss the likely priapulid ground pattern Smiley,, 1994; Terwilliger, 1998), but respi- (Storch,, 1991; Neuhaus, 1994; Ahlrichs, 1995; ratoryy pigments have not been found in Schmidt-Rhaesa,, 1996) and GEA claim to anyy entoprocts (Terwilliger, 1998; C Nielsen, scoree ground pattern features for the mor- pers.. comm.). More importantly, there is no phologicall terminals. A genuine coelomic molecularr support for the purported ho- cavityy that answers to a histological defini- mologyy of the different types of respiratory tionn occurs in only 1 of the 18 currently de- proteins,, hemoglobins, hemerythrins, and scribedd extant species of priapulids (Shirley hemocyaninss that would validate their inclu- andd Storch, 1999). The small coelomic cav- sionn within a single character. itiess surrounding the mouth cone (in addi- Second,, five taxa are misscored for the tionn to the spacious noncoelomic major body hemall system (Z35: circulatory system), and cavity)) of the meiobenthic priapulid Meiopri- thee scoring of one taxon should have been (ipuhtsfijiensis(ipuhtsfijiensis represent a peculiaritexplicitly withiyy justifien d in view of a viable alter- priapulidss (Storch, 1991). In addition, Meio- nativee interpretation. Outside the Trochozoa priapuluspriapulus may be one of the mostevolutionarthee hema- l system is scored as present in ilyy derived extant priapulids (Adrianov and deuterostomess and panarthropods and as re- Malakhov,, 1996;but see also Wills, 1998). This ducedd in nemerteans. However, ZEA incor- suggestss the absence of a coelom is likely to rectlyy scored hemal system in vertebrates bee primitive for Priapulida, which would ne- ass "unknown." The vertebrate hemal sys- cessitatee rescoring this feature. temm is directly comparable to that of other Second,, the scoring of syndermates (Ro- coelomates,, apart from the secondarily at- tifera,, Acanthocephala, and Seison) as "un- tainedd (both ontogenetically and phyloge- known"" for presence of a coelom is inaccu- netically)) endothelium (Ruppert and Carle, rate.. All syndermates unambiguously lack a 1983).. Furthermore, chaetognaths also pos- histologicallyy defined coelom (Clément and sesss a hemal system (Shinn, 1997). The cor- Wurdak,, 1991; Dunagan and Miller, 1991; rectt scoring of this information is essential Ahlrichs,, 1995). forr the proper phylogenetic placement of Third,, on a more interpretational level, the chaetognaths.. For example, when chaetog- absencee of a coelom would be applicable for nathss are rescored for presence of a hemal aa much broader range of bilaterians if entire systemm in the original matrix of Nielsen lifee cycles, including larvae, were considered ett al. (1996), they shift from within the pro- (seee discussion above). This would mean that tostomess to a sister group position to the absencee of a coelom is a symplesiomorphy deuterostomes.. This illustrates that chang- ratherr than a synapomorphy in GEA's analy- ingg only a tiny fraction of a data matrix sis.sis. Although the exclusion of nonbilaterians(0.05 %% of the total information content in this

150 0 case)) may have nontrivial consequences for representationn of all pertinent information. thee results. Because GEA identified chaetog- Includingg all applicable data would be espe- nathss as one of the most phylogenetically ciallyy relevant tor the highly unstable taxa problematicc bilaterians that group among inn the analyses, for which variable analysis protostomess in their morphological analysis, parameterss yield inconsistent phylogenetic thiss crucial information could bear on their placements.. For example, GEA cannot confi- conclusions.. Further notable misscorings are dentlyy place the Nemertodermatida. In their sipunculidss and entoprocts, which both lack summaryy dadogram, GEA place nemerto- aa hemal system (Ruppert and Carle, 1983; dermatidss (together with chaetognaths) at Nielsen,, 1995), and nemerteans, which do thee base of the Protostomia, far removed nott possess a reduced hemal system. Struc- fromm the other platyhelminths. The difficulty turall and developmental data (Turbeville, off placing the nemertodermatids in the to- 1986)) indicate that the nemertean circula- tall evidence analysis may be largely caused toryy system is coelomic and not homolo- byy GEA's recognition of the sequence of Ne- gouss to the hemal system of other bilateri- mertinoidesmertinoides elongates as a sequence artifact. anss (in contrast to the claim by GEA, the However,, equally important, ZEA's morpho- morphologicall matrix of ZEA simply scores logicall matrix did not include all pertinent absencee of hemal system for nemerteans). characters.. The complex pattern of inter- Finally,, the scoring of Bryozoa (Ectoprocta) connectingg epidermal ciliary rootlets (dis- ass lacking a hemal system clearly should tinctt from the terminal axoneme structure) bee defended, because available morpho- inn acoelomorph (Acoela and Nemertoder- logicall data allows the alternative scor- matida)) platyhelminths is not included in ingg based on the proposed homology of thee matrix, although this distinctive char- thee bryozoan funiculus and hemal system acterr has been widely regarded as one of (Carlee and Ruppert, 1983; Ruppert and Carle, thee few synapomorphies of Acoelomorpha 1983). . (e.g.,, Smith et al., 1986; Ax, 1995; Haszprunar, Third,, the scoring of primary larvae (Z133) 1996b;; Rieger, 1996; Littlewood et al., 1999). iss even more problematic because no clear Similarly,, although ZEA's and GEA's anal- morphologicall definition is at present avail- ysess found no support for a close relation- able.. Primary larvae commonly appear to be shipp between annelids and arthropods, they interpretedd as ciliated (free swimming) lar- didd not include one potentially important vae,, a rather imprecise definition. Adopt- synapomorphyy that yielded a close relation- ingg such a definition leaves unexplained shipp between these taxa in previous stud- why,, for example, catenulid platyhelminths ies:: longitudinal body musculature orga- aree not scored as possessing primary lar- nizedd into bands (Rouse and Fauchald, 1995, vae.. Catenulids do possess a ciliated larva 1997).. Thus, despite the comprehensiveness knownn as a Luther's larva (Ruppert, 1978), off the morphological data matrix, the ob- whichh has been considered as a primary larva jectivityy of the analyses could be enhanced (Gallenii and Gremigni, 1989). Lack of a pre- byy including an explicit character selection cisee morphological definition might also ex- protocol,, which is conspicuously lacking in plainn the apparent conflict between the scor- manyy phylogenetic analyses (Poe and Wiens, ingg of some taxa for the presence of a primary 2000).. Notably, explicating unacknowledged larvaa and for the presence of a monophasic or differencess in character selection plays a piv- biphasicc life cycle (Z131). Abiphasiclife cycle otall role in understanding current conflicting iss commonly defined as including a primary phylogeneticc hypotheses of the animal king- larva,, while a monophasic life cycle is said domm (Jenner and Schram, 1999, and in prep). too lack a primary larva. However, urochor- datess are scored as possessing a biphasic life cyclee but lacking a primary larva. Currently, MORPHOLOGYY AND METAZOAN thee concept of primary larvae must be re- PHYLOGENETICS S gardedd as being largely phylogenetic rather GEA'ss study is impressive in its scope, its thann structural (Jenner, 2000). Obviously, that incorporationn of newly sequenced taxa, and makess meaningful discussions on character itss use of sensitivity analyses and charac- scoringg very problematic at this time. terr congruence tests to yield the most ro- AA final comment concerns the reliability bustlyy supported and maximally congru- off GEA's (and ZEA's) results as a balanced entt phylogenetic hypothesis. Unfortunately,

151 1 GEAA also inherited the greatest weakness of andd classification. KMK Scientific Press, Moscow, ZEA:: an uncritically assembled morpholog- Russia.. [In Russian with English summary.] AHLRICHS,, W. H. 1995. Uhrastruktur und Phylogenie icall data matrix. Introducing a poorly con- vonn Seison nébdiac (Grube 1889) und Seism mnula- structedd morphological matrix into a total ev- tustus (Claus 1876). Hypothesen zu phylogenetischen idencee approach of the Bilateria can scarcely Verwandtschaftsverhaltnisseninnerhalbderr Bilateria. bee expected to add weight to the analy- Cuvillierr Verlag, Gotongen, Germany. sissis or to infuse confidence in the espoused Ax,, P. 1995. Das System der Metazoa L Ein Lehrbuchder phylogenetJschenn Systematic Gustav Fischer Verlag, clades. . Stuttgart,, Germany. Naturally,, the performance of a new anal- Ax,, P. 1996. Multicellular animals: A new approach to ysiss with a properly adjusted morphological thee phylogenetic order in nature, volume 1. Springer- matrixx will be imperative to ascertain the full Verlag,, Berlin, Germany. BACKELJAU,, T., B. WtNNEPENNlNOCX , AND L. DE BRUYN. effectss of the many problems involved (a vo- 1993.. Cladistic analysis of metazoan relationships: A luminouss task that lies outside the scope of reappraisal.. CUdistics 9:167-181. thiss paper). Moreover, the analysis will have BARTOLOMAEUS,, T., AND H. RUHBERG. 1999. infrastruc- too take place in the context of a detailed dis- turee of the body cavity lining in embryos of Epiperipc- cussionn of the results of other phylogenetic tustus bMIeyi (Onychophora, Peripatidae)—A comparisonn with annelid larvae. Invert Biol. 118:165-174. studies.. In their concluding paragraph, GEA BENITO,, J., AND F. PARDOS. 1997. Hemkhordata. pointt out that their results may be subject to Pagess 15-101 in Microscopic anatomy of inverte- revisionn on the basis of increased taxon sam- brates.. Hemichordata, Chaetognatha, and the in- plingg and the inclusion of diploblast taxa. Al- vertebratee chordates (F. W*. Harrison and E. E thoughh these recommendations are certainly Ruppert,, eds.). Wiley-Liss, New York. BININDA-EDMONDS,, O. R. P., H. N. BRYANT, AND A. valuable,, the above discussion shows there is P.. RUSSELL. 1998. Suprasperific taxa as terminals in ann even more urgent need for improving the cladisticc analysis: Implicit assumptions of monophyry qualityy of the morphological data set used in andd a comparison of methods. BioL ƒ. Linn. Soc. ZEAA and GEA. 64:101-133. . BROWER,, A. V. Z. 2000. Homology and the inference of Thee phylogenetic data sets assembled in systematicc relationships: Some historical and philo- previouss studies provide a valuable foun- sophicall perspectives. Pages 10-21 m Homology and dationn available for further refinement and systematics.. Coding characters for phylogenetic anal- extension.. The continual evaluation and ysiss (R. Scotland and R. T. Pennington, eds.). Taylor & revaluationn of pertinent phylogenetic data Francis,, London. BRUSCA,, R. C, AND G. J. BRUSCA. 1990. Invertebrates. willl have to play a central role in fu- Sinauerr Associates, Sunderland, Massachusetts. turee studies. Although molecular data are BURICHEL,, P., AND R. A. CLONEY. 1997. Urochordata: playingg an increasingly important role in Ascidiacea.. Pages 221-347 in Microscopic anatomy metazoann phylogenetics, our understand- off invertebrates. Hemichordata, Chaetognatha, and thee invertebrate chordates (F. W. Harrison and E E ingg of animal evolution is, and always will Ruppert,, eds.). Wiley-Liss, New York. be,, critically dependent on morphological BYRNE,, M. 1994. Ophiuroidea. Pages 247-343 in Micro- dataa as well, including total evidence anal- scopicc anatomy of invertebrates. Echinodermata (F. W. yses.. Therefore, molecular and morpholog- Harrisonn and F.-S. Chia, eds.). Wiley-Liss, New York. icall data deserve to be treated with equal CARLE,, K. J., AND E. E. RUPPERT. 1983. Comparative ul- rrastructuree of the bryozoan funiculus: A blood vessel care. . homologue.. Z. Zool. Syst EvoL-Forsch. 21:181-193. CAVAUER-SMITH,, T. 1998. A revised six-kingdom sys- ACKNOWLEDGMENTS S temm of life. Biol. Rev. 73:203-266. CLEMENT,, P., AND E. WURDAK. 1991. Rotifera. Pages II thank Ame Mooers, Ronald Sluys, Sven Lange, 219-2977 in Microscopic anatomy of invertebrates. As- Frederickk Schram, Claus Nielsen, Gonzalo Giribet, and chetminthess (F. W. Harrison and E E Ruppert, eds.). twoo anonymous reviewers for their incisive comments, Wiley-Liss,, New York. andd Ame Mooers for his encouragement to write this CROMPTON,, D. W. T. 1989. Acanthocephala. Pages 251- paper.. My work is supported by grant 805-33.431-P 2622 in Reproductive biology of invertebrates, volume fromm the Earth and Life Sciences Foundation (ALW), IV,, part A (K. G. Adiyodi and R. G. 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