EVOLUTION & DEVELOPMENT

4:4, 243–246 (2002)

©

BLACKWELL PUBLISHING, INC.

243

One small step for worms, one giant leap for “Bauplan?”*

David H. A. Fitch

a,†

and Walter Sudhaus

b

a

Department of Biology, New York University, New York, NY 10003, USA;

b

Institut für Biologie/Zoologie, Freie Universität Berlin, Berlin 14195, Germany

†

Correspondence (email: david.fitch@nyu.edu)

A popular hypothesis about animal diversification is thatunique changes occurred in the Precambrian or Cambrian(ca. 700–500 millions of years [Myr] ago) to produce the dis-tinctive features of all animal “Baupläne” (”body plans”) andthat such changes have not occurred since (Gould 1989:47).In contrast, we suggest that changes similar to the key inno-vations initiating the appearance of these distinctive featuresoccur repeatedly during evolution. A major example is the“inversion” of the dorsoventral axis in the evolution of chor-dates (Arendt and Nübler-Jung 1994), initiated by a switchin mouth position from the neural to the abneural side. Herewe note that similar changes in mouth position evolved

�

50Myr ago at least twice in a group of nematodes related to

Caenorhabditis elegans.

Because this means that suchchanges were not unique to the Cambrian, they can be stud-ied by experimental approaches in closely related extant or-ganisms. A direct consequence of this focus on studying el-emental key changes is that “Bauplan” becomes a less usefulconcept for understanding

how

animal diversity evolved.As a practical approach to understand the origin of differ-

ences between currently disparate forms, we can analyze thesedifferences in terms of the suites of apomorphic (derived)evolutionary changes that made one form different from an-other. Such disparity resulted from many accumulated alter-ations, novelties, and reductions and the extinction of ani-mals from side lineages with intermediate forms (Sudhausand Rehfeld 1992:185–188). Retrospectively, some of thesechanges (which we call “key” changes) might be consideredmore important than others in initiating a major difference.Even slight changes could provide the important first step(retrospectively recognized as key) in an evolutionary seriesof events resulting in a major difference between taxa. Thisapproach of identifying key changes relieves us from dealingwith Bauplan (body plan), which is typological and has un-certain ontology. (Bauplan has been defined as a “phylo-typic” organization or archetypal pattern shared by species ina supraspecific taxon and that is distinguishable from othersuch patterns; e.g., it is unclear how many differences of what

grade distinguish Baupläne [Gerhart and Kirschner 1997:296;Raff 1996:33; Sudhaus and Rehfeld 1992:185].) In fact, a breakwith such typology was the foundation for Darwin’s revolu-tionary conceptual framework (Mayr 1979). Epistemologically,identifying key changes is more likely to give us a practicalunderstanding of the origins of morphological disparity thantrying to fit variation into typological concepts like Bauplan.

An important key change that led to one of the major dif-ferences between extant chordates and protostome inverte-brates was most likely a simple change in mouth position(mouth heterotopy) from the neural toward the abneural sideof the body. This follows from recent observations support-ing homology (shared ancestry) of the dorsoventral (

�

neu-ral–abneural) axis and mouth–foregut primordia among allbilaterian animals.

Recently, Geoffroy Saint-Hilaire’s original 1822 obser-vation of similar but inverted patterns along the dorsoventralaxis in arthropods and vertebrates has been extended by evi-dence for the remarkable conservation of several underlyingpatterning mechanisms (Arendt and Nübler-Jung 1994,1996, 1997; De Robertis and Sasai 1996; Holley et al. 1995,1996; Schmidt et al. 1995). For example, the sequence ofgerm layers in the blastula fate map is conserved along thisaxis, as is the morphogen mechanism (reviewed in Arendtand Nübler-Jung 1997). The concurrence of all these pat-terns and mechanisms strongly supports homology of thecorresponding neural–abneural axis in these and other bilat-erian taxa (Arendt and Nübler-Jung 1997). Consequently,the neural midline cells in these taxa are homologous(Arendt and Nübler-Jung 1996, 1997). That is, the “dorso-ventral” axis can be regarded as a “neural–abneural” axisthat is homologous in these animals. The position of the neu-ral midline is labeled “dorsal” in chordates and “ventral” inarthropods, annelids, and nematodes because “ventral” isgenerally defined by the side on which the mouth opens(Arendt and Nübler-Jung 1997; Wolpert 1998:454).

Recent evidence also supports homology between pro-tostome and deuterostome (e.g., chordate and hemichordate)foregut and mouth primordia:

brachyury

,

goosecoid

, and

forkhead

are expressed in mouth and foregut regions and

otx

in the pre- and postoral ciliated bands of representative cili-

*A metaphor by which we mean that even a tiny change for an insignificant creature may provide a good model for understanding the evolution of form.

244 EVOLUTION & DEVELOPMENT

Vol. 4, No. 4, July–August 2002

ary larvae of both protostomes and deuterostomes (Arendt etal. 2001; Tagawa et al. 2001). In particular, the splitting of

brachyury

expression from a contiguous area around theclosing blastopore into separate regions fated to produce thedistal foregut and hindgut is remarkably similar betweenprotostome and deuterostome ciliary larvae (Fig. 2d ofArendt et al. 2001; Fig. 3 of Tagawa et al. 2001).

By far the simplest explanation for all these patterns isthat in the bilaterian ancestor (before the divergence of chor-dates from protostomes), (1) the mouth and anus originatedat opposite ends of the blastopore, as observed in extant am-phistome annelids and onychophorans, and (2) a complexneural–abneural axial pattern was already in place (Arendtand Nübler-Jung 1997). If so, the key change that gave riseto the “inverted” Bauplan of chordates was most likely justa change in the position of the mouth (from an ancestral po-sition on the neural side) to the abneural side (Wolpert1998:454).

Alternative scenarios have been proposed to explain howthe same neural–abneural (dorsoventral) axial pattern couldhave evolved independently in different lineages, for exam-ple, by independent co-option of the same neural–abneuralpatterning mechanism from a different role in a “less com-plex” bilaterally or even radially symmetric ancestor alongwith independent origins of a mouth (Gerhart 2000). How-ever, these alternative hypotheses require several more

adhoc

explanations than the hypothesis in which the neural–abneural axis was conserved and in which one simple type ofchange (mouth heterotopy) explains the dorsoventral “inver-sion.” Even the hypothesis proposed by Nübler-Jung andArendt (1996), that the chordate mouth arose as a novel fea-ture on the abneural side (concomitant with obliteration of anancestral mouth on the neural side), is less parsimonious.Therefore, these alternative hypotheses bear the burden ofproof.

Thus, the key change that initiated the evolution of one ofthe most distinctive features of chordates was not a bigchange. Was such mouth heterotopy unique to the Cam-brian? In nematodes, the mouth was ancestrally situated ter-minally, as in extant rhabditids, a group that includes themodel system,

C. elegans

(Fig. 1). An inclination in mouthposition to the abneural side evolved in the Ancylostoma-tidae (strongylid parasites of placental mammals), as ob-served in

Gaigeria pachyscelis

(Fig. 1A). Independently,mouth position shifted toward the neural side in

Hypodontusmacropi

, a strongylid marsupial parasite (Fig. 1A). Thus,mouth heterotopy has occurred recently and has occurred asa key change in the lineage leading to chordates; mouth het-erotopy relative to the neural–abneural axis was not uniqueto the Cambrian or Precambrian.

Similar heterotopy has occurred in the evolution of anus/cloaca position. In rotifers and leeches, a foot or posteriorsucker, respectively, originated on the neural side anterior to

the anus/cloaca (for fastening onto the substrate and for al-lowing specialized locomotion), pushing the anal opening tothe abneural side. The terminal anus of hemichordate en-teropneusts presumably evolved or has been maintained forefficient ejection of waste from the burrow. In irregular seaurchins, the anus shifted from the aboral toward the oral side(Brusca and Brusca 1990). These examples provide prece-dents for dorsoventral heterotopy of another important fea-ture originating from the blastopore occurring at varioustimes in different evolutionary lineages.

Why is it not recognized more widely that many of thekinds of changes ultimately leading to disparate forms werenot unique to the Precambrian/Cambrian? One reason maybe that the human mind is so impressed with large differ-ences that it cannot easily conceive origins of such differ-ences in small steps (see Darwin 1859:29). Perhaps focusingon typological Baupläne exacerbates this difficulty? But amore important reason is the common misconception (alsosustained by typological terms like “phylum-level bodyplan,” “phylotypic stage,” and “phylotypic process”) that thetaxonomic level of Phylum is primarily determined by Bau-plan (or developmental stage or spatial pattern of develop-mental regulatory mechanisms). First, it is tautological to useBauplan to define a particular taxonomic level if a Bauplanis itself defined as the set of features characteristic of a par-ticular taxon. Second, it has been considered “paradoxical”that “all phyla are old” despite “repeated opportunities forthe appearance of new phyla” (Raff 1996:174). This paradoxis resolved by noting that the different hierarchical levels ofthe taxonomic system (Phylum, Class, Order, etc.) are ap-plied

arbitrarily.

These taxonomic levels reflect

relative

di-vergence points in time, as Darwin (1859:420) famously rec-ognized, not particular differences in Bauplan. That is, thegroups-within-groups hierarchy of taxonomy simply derivesfrom common ancestry at more and more ancient times (Fig.1B). Phylum divisions represent divergences that occurredearlier than Class or Order divisions within the Phylum,

re-gardless of the grade of difference in Bauplan

(Darwin1859). Even if an

identical

key innovation as that character-izing a “phylum-level body plan” arose recently from withinan Order, a new Phylum could not be erected for it withoutupsetting the entire taxonomic hierarchy,

no matter how dis-tinct the new Bauplan

(Fig. 1B). Thus, “all phyla are old”simply because of the hierarchical restrictions of taxonomy,not because fundamental key changes to body plans have notarisen more recently. A paucity of Phyla more recentlyemerged than the Cambrian is therefore

not

evidence for lackof recent innovative changes in Bauplan.

Large differences between animals as disparate as extantchordates and arthropods originally began as small (retro-spectively key) changes between closely related taxa likethose appearing as differences between species today. ThePrecambrian and Cambrian were no more unique in produc-

Fitch and Sudhaus

Small steps to “Bauplan”

245

Fig. 1. Evolution of “key” changes. (A) Phylogenetic hypothesis for relationships of representative strongylid and rhabditid nematodesbased on ribosomal RNA gene sequences (Sudhaus and Fitch 2001). Note that strongylids are derived from rhabditids. Schematics at thebranch termini depict sagittal views showing mouth position (the indentation in the black outline of the anterior portion of the body)relative to the nerve ring and neural cord (red ring and line inside each schematic). Scanning electron micrographs show the anteriorends of Oscheius sp., strain DF5000 (photos by Can Nguyen), with a terminal mouth (lateral view and terminal view, inset), the primitivestate for these nematodes; Gaigeria pachyscelis, with a mouth on the abneural body side (photo by Marion Link); and Hypodontus mac-ropi, with a mouth on the neural body side (from Beveridge 1979). Scale bars, 10 �m (Oscheius sp. inset, 1 �m). Terminal mouth positionwas ancestral (blue lineages); mouth heterotopy (red lineages) occurred independently in at least two strongylid lineages. Because ofsome unique features and parasitic lifestyles, strongylids have been classified traditionally at a higher level than the free-living rhabditids.Because strongylids are derived from paraphyletic rhabditids, however, the hierarchical constraints of the taxonomic system require thatthe taxonomic level for strongylids is demoted below that of the rhabditids (or the level for the rhabditids is promoted above that of thestrongylids), because taxonomic level is not determined by Bauplan. (B) A Phylum encompasses groups at lower taxonomic levels (e.g.,classes, orders) because the members of lower taxonomic groups are descendants of stem-species that are themselves descendants of thestem-species from which all members of the Phylum are derived. Even if a distinctive feature that was identical to that of a “phylum-levelBauplan” (red lineages) evolved recently (here within an order), it could never be called “phylum-level” because of its origin at a lowertaxonomic level, not because of the morphology.

246 EVOLUTION & DEVELOPMENT

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ing these changes than were recent periods. It is just that dis-parity between clades increases over time (with or withoutselection), not only because of the accumulation of change,but also because the opportunity for extinctions of interme-diate forms increases with elapsed time since common an-cestry. As we accumulate data on phylogeny and comparedevelopmental mechanisms at different levels of morpho-logical disparity, we predict we will find more cases inwhich ancient changes will have recent analogues that can bestudied experimentally with closely related extant taxa.

An important consequence of this approach directed to-ward understanding key

changes

is that Bauplan becomes aless useful concept. We cannot understand evolutionary de-velopmental mechanisms by being awestruck at the disparityof typologically conceived Baupläne associated with arbi-trarily applied taxonomic levels. “Bauplan” and even “Phy-lum” are concepts left over from a preevolutionary era thathave little or no relevance to the objectives of modern evo-devo (see Williams 1992:87). A practical understanding ofthe

evolution

that resulted in today’s forms requires that weinstead direct our attention to the more immediately relevantand approachable activity of elucidating the branching pat-terns of the tree of life and reconstructing the key

changes

that initiated the evolution of these forms. Kuhn (1970) ob-served that scientific revolutions are often characterized bythe shedding of outmoded concepts and changing the ques-tion altogether. Whatever you wish to call it, evo-devo couldbecome one such revolution.

Acknowledgments

We thank K. Kiontke, C. Desplan, R. Strathmann, F. Piano, J. Hub-bard, R. Raff, and members of the Fitch laboratory for critical com-ments and lively discussion; the NSF for supporting work in theFitch laboratory; and the Fulbright Commission for supporting in-ternational exchange between W. S. and D. F.

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