Table Of ContentBijdragentot deDierkunde, 64(2)65-74 (1994)
SPB Academie Publishingbv, The Hague
Owen revisited: a reappraisal of morphology in evolutionary biology
Alessandro Minelli& Frederick R. Schram
1Department ofBiology, University ofPadua, Via Trieste 75, 1-35121 Padua, Italy; 2lnstituteof
Systematics and Population Biology, University ofAmsterdam, Box 94766, NL-1090GTAmsterdam,
TheNetherlands
Keywords: homology, phylotype, macroevolution, morphogenesis
Abstract sameorganindifferentanimalspecies underevery
variety of form and function"] and analogy ["A
Anew analysiswithin theframeworkofdevelopmentalgenetics part or organ inone animalspecies which has the
provides both raw data and theoretical support to the “old” samefunctionas anotherpart ororganina differ-
morphologyand suggests anew,morepredictive,approach to
ent species"] that formalizedthe approach of suc-
the concept ofhomology.We distinguishbetween “positional
homologues” and “structural homologues” as independent ceeding generations to comparative anatomy. At
componentsofthe moregeneralconceptofhomology.Wedis- that time,analysis of form,theso-calledBaupläne,
cusssomegeneralpatterns seenin the anatomyofanimals and already hada centralroleinthestudiesand discus-
in their morphogenesis. Slack et al. (1993) advanced the con-
sions of animalrelationships that had prevailed in
cepts ofthe “zootype”,aparticularspatialpatternofgeneex-
pression, and the “phylotype”,aparticularstage ofembryonic biology since thelast few decades oftheeighteenth
developmentthatexpresses the zootype. Webuild upon these century (e.g., see Russell, 1916).
conceptsand expandthem.This allowsustopropose someaddi- Nevertheless,thismethodofanalysis placed con-
tionalphylotypes(arthrotype,cyclotype,platytype,malacotype,
straintson makingdirectcomparisons betweentaxa
trimerotype) that may guide future investigations towards
understandingthe genesisofmetazoan form. that researchers didnot perceive as closerelatives.
Wemightevensuggestthattheverynotionofphyla
directlyaroseas taxonomieexpressions ofthemajor
Zusammenfassung difficulties encountered in assessing homologies.
The conceptual source of our current practice of
Eine neue Analyse im Rahmen der Entwicklungsmechanik subdividing theanimalkingdom intomajor groups
liefert sowohl empirischeEvidenz und theoretische Unterstüt-
(viz., what we currently call phyla) arises, in fact,
zungfür die “alte” Morphologieals auch ein Homologiekon-
zeptmitmehrAussagekraft.Wir unterscheiden Lagehomologie fromCuvier's (1817) establishmentofhis fourem-
und strukturelle Homologieim Sinne zweier grundsätzlichver- branchements (Vertebrata, Articulata, Mollusca,
schiedener Teile eines allgemeinenHomologiekonzeptes. Wir and Radiata). Cuvierregarded these body plans as
besprechen einigeverallgemeinerteMuster der tierischen Mor-
not comparable witheach other, andso theunique
phologie and Morphogenese.Wir erweitern die Konzeptedes
Zootypusund des Phylotypus(Slacketal., 1993)auchdadurch, and separate status of "phyla" becameensconced
daß wir einige weitere Phylotypi (Arthrotypus, Cyclotypus, in our tradition.In contrast to this, Geoffroy St.-
Platytypus, Malacotypus,Trimerotypus) in schematischen Zü- Hilaire(1818-22) kept extending comparisons be-
genvorschlagen. tween animals. He eventually moved to a position
wherein a single type-plan relatedall animals, an
approach that hadwidesignificance atthetimebut
Introduction
which eventually went into eclipse.
Just over 150 years ago, Owen (1843) introduced Only recently hasthe scienceofsystematics made
definitions of the concepts of homology ["The more rigorous, cladisticsattempts to dealwithani-
66 A. Minelli& F.R. Schram - Owen revisited
malphyla inawaythatwouldallowformulationof These gradients determinetheprimary polarity of
testable hypotheses concerning evolutionary rela- thezygote. Withoutthispolarity thegrossarchitec-
tionships. The first such attempt to deal cladisti- turalorientationofthe embryo andthe capacity to
cally withallanimalphyla withasingle datamatrix develop more specific structures withinit wouldbe
(Schram, 1991; Meglitsch &Schram, 1991) hastrig- impossible. Slack etal. regard theevolutionofthis
gered furthereffortsto expand thedatabaseand to controlas the necessary first step that allowedthe
evaluate alternativeexplanations (Eernisse et al., evolutionofmetazoans to begin. Theythenextend
1992;Conway Morris, 1993). this concept further to postulatethe "phylotype",
i.e.,aparticular stageinembryonic development at
whichthe zootype becomes manifest.
Morphology and developmental genetics This hypothesis in fact parallels concepts that
havebegun to appearin print, derivedfrompurely
The intellectual viewpoint developed from the comparative morphological research (Emerson &
French savants forthestudy of morphology origi- Scharm, 1990; Schram &Emerson, 1991; Minelli,
nally occurred without any understanding of the 1992). These latter authors have tried to build
genetic mechanisms thatunderliethegeneration of on other, broader generalizations concerning the
anatomical form.Revealing these mechanismshas ontogenyof shape as applicable to understanding
not come easily. In fact, discerning the exact role major shifts in animal form in the evolution of
thatgenesplay inthecontrolofformhas presented animalBaupläne, both for metazoans as a whole
problems. Nevertheless, throughout thelast decade (Gould, 1977; Alberchetal., 1979)andcrustaceans
we havemadequantum leaps in our knowledge of specifically (Schram, 1986). Together these genetic
the genetics of development (e.g., see Lawrence, and morphologic advances constitute a break-
1992), which has lead to a heightened level of through that can now allow us to move towards
sophistication in understanding thegenetic control some general theory of morphology within the
of animal architecture. Jacobs (1990), from the framework ofanimalmacroevolution. Wesuggest
viewpoint of paleontology, and Averof& Akam that rather than one single phylotype we must
(1993) and Slack et al. (1993), from theviewpoint speak of aseries of phylotypes that correspond to
of developmental genetics, now suggest that this othercomplexes of genes, inconcert withtheHox
growing understanding offers theprospect ofrede- complex and their expression, that control more
fining the concept of "Metazoa" and, as a result, specific aspects of metazoan body architecture.
reconceptualize what it means to be a particular Itnow seems clearthatthediagnostic featuresof
kind ortypeofanimal.Slack etal. (p. 490) suggest adult structure, i.e., characters that we have tra-
"thatananimalis anorganism thatdisplays a par- ditionally usedto definephyla, appear "relatively
ticular spatial pattern of geneexpression", apat- late" in ontogeny as well as phylogeny, and that
tern whichthey term the "zootype". By this they these featuresdo not revealthemost fundamental
mean thatthe process ofontogenetic development characteristics of a phylum's architecture. As an
comes under a specific manner of maternal and example, we have traditionally diagnosed Arthro-
zygotic genetic controlthatdefinesaspecifiedsetof poda as those animals that possess a segmented
polaritiesofa developing animalembryo. Thiscon- body, bearing jointed appendages, andenclosedin
trol serves to effectively define not so much the achitinized cuticle. However,seriousproblems de-
specificstructures astheoverallarchitecturalframe- velop whenconsidering anatomyatthislevel.Many
workoftheadultanimalbody, i.e.,anterior/poste- highly respected authorities (e.g., D.T. Anderson,
rior, left/right, dorsal/ventral. 1973; Mantón, 1977), focusing strictly on matters
We can conceive oftheirzootype as astate that of ontogeny, function, and the structural differ-
contains a specific array of genes, which generate ences betweenmajor arthropod types, donotagree
chemical lineargradients extending throughout the withtheeffectiveness ofsuch adiagnosis andchal-
zygote, collectively termed the "Hox cluster". lenge the idea of arthropod monophyly. Many
Bijdragen tot deDierkunde, 64 (2) - 1994 67
otherauthorities,focusing onthesimilaritiesamong ogy ofposition. In otherwords, wecan homologize
major arthropodtypes, ofcourse dispute this(e.g., places orpositions along abody, e.g.,inarthropods
see Gupta, 1979;Wheeler et al., 1993). linking nodes or hot spots across species groups.
A different approach to arthropod phylogeny If we can entertain this possibility, then we can
hasemerged recently that dealswithbroadpatterns also homologize theevents or structures located at
seeninarthropodBaupläne ratherthanspecific ele- thosehotspots even though they mayappearquite
ments of form. Schram & Emerson (1991) recog- dissimilarinform orfunction.For example,inmil-
nizedafundamentalorganization ofthearthropod lipedes (Diplopoda), thegonoporeoccurs on what
body inwhichregional markers along thelengthof canberegarded asthefifthsegmental unitposterior
thebody, which they termed"nodes", serveas foci to the head(i.e., intheposterior partofthe second
for structural events, and thesenodes occur across double segment following the collum). In male
all major groups of arthropods. The analysis of dragonflies, asecondary penis orclasper occurs on
Schram& Emerson implied that factorsotherthan the second abdominalsegment. Gonopores are in
just the traditional "diagnostic features" of seg- nowayastructuralhomologue ofsecondary penes.
ments, jointed limbs, and chitin serve as the most However (Fig. 1), we can perceive the fifthpost-
important aspectsto defininganarthropod. Rather, collumsegmentofdiplopods as apositional homo-
theorganization ofthearthropod bodyintodistinct logue ofthesecond abdominalsegment ofinsects.
regions marked by specific "hot spots", around Furthermore, ArthropodPattern Theory (Schram
which "segmental" events take place, determines &Emerson, 1991) postulates thatthis very hot spot
with greater certainty an organism's status as an in"myriapods" andinsects corresponds to aniden-
arthropod. Thus, arthropods evolvednot so much tical position in the Bauplan of the crustaceans
by the process of imposing a pattern on the seg- wherea maxillipede can occur. Therefore, because
ments as they didby segmenting (or breaking up) of this homology of location, we can extend the
themorefundamentalpatternsofthebody regions. comparison between diplopod gonopores,dragon-
They concludethat the ancestor ofthearthropods fly secondary penes, andcrustacean maxillipedes as
possessed a body broken into a series of body positional homologues. In the phylogenetic se-
regions, with borders demarcatedby "hot spots" quenceof unfolding genetic constraintson arthro-
whoselocationswere genetically determined(prob- pod development, thecontrolofposition, i.e., pat-
ably by overlapping gradients), rather than a uni- tern and place, through theaction of some combi-
form, long body composed of iterativesegments. nation of gap, pair rule, and homoeotic genes
preceeds the genetic and/or epigenetic control of
specific structures. On the other hand, we can
Positionalversus structural homology recognize special homologues ifthey occur in dif-
ferent positions without the need to imply some-
Theapproachoutlinedaboveallowsareadjustment thing like genetic piracy (Roth, 1988).
of our understanding of homology in animals.
Traditionally, comparative anatomists have inter-
preted a specific structure ataspecific position on Some general principles in animal morphology
thebody ofa species as a homologue ifit matched
an identical or similarly developed structure at a Indeed, we nowcan set down some general prin-
corresponding place inanotherspecies. However,if ciples derivedfrom thediscoveriesof developmen-
genescontrolthe expression of not only structure, talgenetics aswellas fromtheworkofcomparative
but also position (e.g., ifin arthropods thecontrol morphologists. Laying downthesepoints maycon-
ofspecific structures, such as segments proper or tributetowards a general theory of morphology, if
appendages, is differentfrom the control ofposi- you will,atheory of macroevolutionby pattern as
tion, or body pattern), then we can distinguish be- anadjunct to the more traditionaltheory ofmicro-
tween the homology of structures and the homol- evolutionby process.
68 A. Minelli& F.R. Schram Owen revisited
Fig. 1.Bodyfeatures asdifferent asthepenisofamaledragonfly(A,X)and the genitalopeningofamillipede(B,X) canberegarded
aspositionalhomologues,inspiteofthelack ofstructural homologybetweenthem.This homologypossiblyextendstoapairofmaxilli-
pedes ofmany crustaceans (C, X).Another exampleofpositionalhomologyispossibly givenin the sameanimals,i.e.,the gonopods
ofmalejuliformmillipedesandthe genitalopeningsofdragonfliesandcrustaceans (Yin the figuresonthe left,f(femaleopening)and
m (maleopening) in the sketch drawingson theright).Vertical bars indicate approximatelevels ofthe nodes ofArthropodPattern
Theory(Schram& Emerson, 1991).
(1) Cellularorganization is ofsecondary impor- system in the zebrafish (Kimmel, 1993). Further-
tanceinestablishing thezootype. Forexample, one more, Weygoldt (1979) even questioned D.T.
candirectly comparetheprocessofsegmentation in Anderson's (1973) contentionthat blastodermfate
Drosophila, whichoccurs inasyncytial blastoderm maps had any relevance to discerning germ layer
witharapid diffusionofmorphogens, tothatin the derivation, although Wheeleretal. (1993) believed
flourbeetle Tribolium,even though partof thelat- Anderson's ontogenetic datahad validity but only
ter's development occurs in acellular,rather than as asinglemultivariatefeatureamongmany others.
syncytial, context (Sommer & Tautz, 1993). (3) Theformationofbodysegmentsis not ofpri-
(2) Specific celllineage is often irrelevant. For mary importance. This has been examined above
example, one can see this in the segmental repat- forarthropods (Jacobs, 1990; Schram&Emerson,
terning of post-naupliar material (both ecto- and 1991). These authors contended that in phyloge-
mesodermal) in peracarid crustaceans aftera very netic as well as in developmental terms the heter-
regular unfolding of cell lineage up to that point onomously segmented animalsare formedthrough
(Dohle &Scholz, 1988). Celllineage is also scarcely the segmentation or the breakup of an earlier
relevant for the patterning of the central nervous evolved body pattern, ratherthanapatterning or a
Bijdragen tot deDierkunde, 64 (2) - 1994 69
regionalization of a previously segmented body. mouth, or genital openings, or both can appear.
However, some steps in segmentation are some- Second, in nematodes, the subterminal hot spot
times anticipated during ontogeny, e.g., in the marks cloacal openings in malesbut an anus only
parasegments of Drosophila (Martinez Arias & infemales, the female genitalporebeing borne on
Lawrence, 1985) and corresponding units inchilo- anadditionalmid-body hotspot. Third, in trache-
pod centipedes (Minelli &Bortoletto, 1988). More- ate arthropods(millipedesandinsects) thesamehot
over, secondary patterning is sometimes superim- spot maybe the site of eithergonoporeor secon-
posed at later developmental stages. dary penis, as mentionedabove. Fourth, an ante-
(4) Mostanimalsare moreextensively patterned rior mid-ventralhot spot apparently contrains the
ventrally than dorsally. The functionalmeaning of locationof nephridiopores in echiurans as well as
thisis not difficultto understandgiven the sensory theanus in sipunculans.
interactions with the substrate to achieve feeding (9) Terminal(apical) controlhassomething to do
andlocomotion, butthemorphogenetic controlof withindividuality. In formsthat webelievelackef-
thisneedscloserinvestigation. However,thereexist fective terminalcontrol, individuality is softened.
severalpossible mechanismsto explain this,as seen Twoexamples can illustratethis. First, in scypho-
in the complexity of thegenetic controlof dorso- zoans, annular constrictions (types of hot spots)
ventral polarity as known in Drosophila (K.V. leadto strobilization.Second, in polypoid cnidari-
Anderson, 1989), as well as theoreticalmodels to ans, bryozoans, and certain protochordates, bud-
explainthis,asseeninexplanations oftheevolution ding leads to colony formation. The manner of
of invertebrateform(Nielsen, 1985). genetic control, or lack thereof, ofthesephenome-
(5) Maternalcontrolnever extends over thefull na needs examinationin detail.
deploymentofthezootype(Slacketal., 1993; Buss, (10) Thereis aminimumsizeforpatternexpres-
1988;Lawrence, 1992).Thematernalgenesserveto sion. Thissize, however, depends onthepatterning
determinezygote polarities, but specific controlof mechanism.Forexample, subcellularkinetiesactas
individual form falls largely to zygotic gene com- templates to determinetheciliary structures incili-
plexes. ate protistans (Frankel, 1989). However, for the
(6) Body regions arealmost alwaysfew in num- kind of patterns we concern ourselves with here,
ber.Whythis is soremainsobscure, butthefactre- some animals appear too small to get more than
mains that numbers of body regions seem to fall antero/posterior polarity, e.g., dicyemid meso-
mostly between2and 4. zoans. Others seem too smallto develop segmenta-
(7) Thereis astabilizing effect derivedfrom the tion, e.g., eriophyid mites (ca. 50 um).
establishmentof controlover theposterior endof (11) Thefunction of specific anatomicalstruc-
the body. The overlapping fields of control that turesstabilizes (reinforces)pattern.This seems true
radiatefrom theopposite ends,anteriorandposte- both for the anterior-posterior and dorsal-ventral
rior, exist as a valuable pre-condition for the de- polarities as well as for the positioning of land-
velopment ofsize-invariantpatterns(cf. theFrench marks (hot spots) along the main body axis.
flag model of positional information developed
by Wolpert, 1969; also, see below concerning the
malacotype). Selected phylotypes
(8) Body landmarks(hotspots) havepriority. By
this we mean that the hot spot has multi-poten- Giventhe aboveprinciples, and in thelight ofthe
tialities in phylogeny and ontogeny. Once estab- phylotype concept(Slack etal., 1993; Seidel, 1960),
lished, the spotsconstrainthesiteofappearanceof we can suggest some specific phylotypes for which
subsequent morphological events, whatever they developmental geneticists need to search for the
might be. Four examples can illustratethis point. underlying genetic controls. We do not intendhere
First, in planarians and digenean trematodes we to put forth a detailed analysis of all metazoans.
can recognize a mid-body hot spot whereeither a However, we can indicate a few obvious types
70 A. Minelli& F.R. Schram - Owen revisited
Bijdragen tot deDierkunde, 64 (2) - 1994 71
(Fig. 2). Furthermore, we do not expect that each scutigeromorph centipede antennae and tarsi, and
phylum corresponds to aphylotype. Phylotypes are amblypygid chelicerate "pedipalps". Study ofar-
really better equated with levels or degrees of or- thropods certainly will continueto play an impor-
ganization withinthezygoteandearly developmen- tantroleingeneratingraw datarelevantto ageneral
tal stages, and wewouldexpect our phylotypes in theory of morphology.
some cases to correspond to grades rather than to Otherphylotypes canbesuggested. TheCnidaria
clades. and Ctenophora appearto possess theclassic zoo-
Wehavealreadyalludedto thecontrolofarthro- type as defined by Slack et al. (1993). However,
pod body patternpostulated bySchram &Emerson given that the zootype specifies a dorso/ventral-
(1991). This pattern appears related to the opera- anterior/posteriororientation, theradiateBauplan,
tionof gapand homoeoticgenecomplexes (Averof or "cyclotype", ofthesephyla is somewhatatodds
& Akam, 1993). Genetic specification of an "ar- with the supposed underlying control that Slack
throtype" shouldcomewhendevelopmental genet- et al. postulate. There is an implicit longitudinal
ic studies expand beyond insects to include myria- orientation to their body plan with incipient hot
pods, crustaceans, andcheliceriforms. Somethings spots that may correspond to sites of budding (al-
to lookforinthisregard mightincludegenetic mar- readyalludedto above). However, therealso seems
kers of positional homology as well as terminal to beanadditionalpolar coordinate referencesys-
markers. This latter kind of marker should have tem established inthese animalsthat facilitatesin-
significance for limb formationas well as for the tercalary growth and structural development. This
main body. There appears to be an element of a suppression oflinearity may belinkedwith theab-
polar coordinate reference system (Bryant, 1993) senceofany strong terminalcontrolofthe body in
that operatesinthedevelopment ofarthropod ap- these "lower"radiate forms.
pendages (perhaps only analogous to consideration A"platytype",aroundwhichflatwormsevolved,
of similar polar axis issues in the body of cnida- clearly expresses the underlying zootype with dis-
rians). This polar system is coupled with a "seg- tinct anterior-posterior, dorsal-ventral, and left-
mentation" process similar to that of the main rightorientation. Whilebodyregionalization seems
body axis ofarthropods whereinprotein markersof incipient, theseanimals evidently lack awell-devel-
annulinmarkthe limbarticle boundaries(Bastiani oped posteriorcontroller.A mid-bodyhotspot, for
et al., 1992; Steiner& Keil, 1993). Limb develop- which geneticists might seek amarker, acts as the
ment with clear limitsto segment numbers on the locusofmouthand/orgenital structures. Informs
limb seems tobe generally coupled withstrongapi- in whichthesefeatures shift anteriorly, such as the
cal or terminal control. Limb termini are often catenulids, secondary events of constriction and
clearly demarcatedbystructuralevents(e.g., dacty- budding take place at the mid-body hot spot.
lar claws, terminal sensilla). When these terminal Moreover, the lack ofeffective posterior terminal
controls seem lacking, often segmental controls control may allow the "paracolonial" strobiliza-
soften and flagellar ("ultra-segmented") limbs tion of cestodes.
appear,e.g. malacostracancrustacean antennules, A"malacotype" affordsanexcellentexample of
Fig. 2. Some tentativelypostulatedadditional phylotypesasderivedfrom the ideas ofSlack et al. (1993).Their zootypeconsists ofa
distinct geneticcomponent (theHox complex)thatdefines thebasic polarityofthe metazoanzygote.Subsequentlyevolveddiagnostic
features aresketchedintermsofelements ofdevelopmentalcontrol givingriseto“hot spots”locatedat differentplacesalongthe main
body axis.Somereal animalsare figuredforreference: Hydra(Cnidaria)forthe cyclotype;agenerictrematode (left)andthetapeworm
Echinococcus (Cestoda)—thisonewith thebody articulatedinto ashortchainofunits byaprocess ofstrobilization—for theplatytype;
Sepia(Mollusca) for the malacotype,Zorotypus (Insecta)for thearthrotype, and the polyp-likeCephalodiscusand the worm-like
Balanoglossus(both Hemichordata)for the trimerotype.Abbreviations: otd-orthodenticle,ems-empty spiracles, lab-labial,pb-
proboscipedia,Dfd-deformed,Scr-sexcombsreduced,Ubx-antennapedia/ultrabithorax/abdominaAl group,AbdB-abdominal B,
eve-even-skipped.
72 A. Minelli&F.R. Schram - Owen revisited
what an effective posterior terminal controller thehotspotsbetweenthem, are undergeneticand/
produces, for this appears as the hallmarkof the or somedegree ofepigenetic control.However, the
nemertineand molluscanBaupläne. Thisposterior development ofspecific structuresprobably retains
controllerexpresses itselfinitiallywiththedevelop- alarge degree ofepigenetic autonomy. Theappear-
ment ofananus, asinnemertines, andlateronwith ance of anatomicalfeatures becomes functionally
thebody terminusservingasthefocusofexcretory, integratedintotheanimalbodyas awhole, but cen-
respiratory, reproductive, and circulatory struc- tral controlover theirdevelopment persists mainly
tures as in molluscs. Indeed, the structural con- as a controlof timing rather thanas a controlof
straint of a strong posterior controllermay have specific form, e.g. endocrine involvement in the
provedtoostrict forthemolluscs, intermsoffunc- form ofappendages developing from insectimagi-
tion, since subsequent evolutionary events within nai discs (Couso et al., 1993). We can now speak
themolluscs seemtofocuson mitigating theeffects (indeed, wemustspeak, seeYoung, 1993)ofanimal
of the posterior controller (and the concomitant "types" not withreferencetoabstract "paper ani-
lack of intermediatehotspots wherenewfeatures mals", but rather with reference to specific gene
couldattach). Severalalternativeplans derivefrom complexes and timing sequences.
this: 1) developing secondary hot spots, thus Thescience of morphology has comefullcircle.
achieving "soft segmentation," as in polyplaco- Thegreat morphologists ofthe late 18thandearly
phorans and monoplacophorans; 2) becoming 19thcenturysuch asCuvier,GeoffroySaint-Hilaire,
stronglyasymmetrical, asingastropods; 3) shorten- Goethe, and Owen, studied thebroad patterns of
ing (monoplacophorans) andbending thebodyaxis animalstructure and strove for generalizations as
(cephalopods). tothemeanings ofobservedsimilarityinformand
Finally, a "trimerotype" mayhave significance function.The typological concepts ofthisphiloso-
for several phyla. This plan focuses around a phie anatomique, especially thoseof Geoffroy St.-
manifestationof two strong hot spots betweenthe Hilaire,provided aneffectivetoolwithinatheoreti-
anteriorandposterior controllers.Withinthecon- cal framework for directing morphological re-
fines of this constraint, great variationexists with search (Russell, 1916). The great body of knowl-
theexpression oflophophorate, deuterostome,and edgethesescientists uncoveredatteststo thesuccess
certain aspects of trochophorate body plans. It is of their method, knowledge that has effectively
possible that certainaspects of this phylotype ap- burrowedandcementeditselfintotheveryfounda-
peared independently withinthe higher phyla, but tions of modernbiology. The perspective of that
itseems clearthatit isoftensubjected to somepro- time viewed science and philosophy as parts of a
foundmodifications.Forexample, we can note the continuum of human thought. Although western
effectsoftheimposition ofasecondary polar coor- science came to reject the platonic philosophic
dinatesystem over thetrimeryofechinoderms, and aspects, the Naturphilosophie, of many of these
themodificationofortotallack ofterminalcontrol early workers, it could not reject the discoveries
seeninthecoloniallophophorates, hemichordates, they made(Young, 1993). These early morpholo-
and chordates. gists worked in a time when "philosophical sys-
tems"determinedthata majorefforttoestablish a
coherentbody oftheory shoulddirectthecourse of
Conclusions future empirical investigations. The subsequent
period, thatwhichbegan withtheeffortsofDarwin
The overall, most important featurein all of the and Wallace to establish a causal evolutionary
above-mentionedphylotypes is the importance of theory, directedthe attentionofscienceawayfrom
thegenetic controloftimingofontogenetic events, a consideration of pattern and eventually com-
which reflects the phyletic evolutionof metazoan pelled investigations of process that were much
body plans. Thebroadfeaturesofanimalarchitec- moreexperimentally oriented(Lenoir, 1982). These
ture,such astheanteriorandposterior termini,and laterdayempiricists rejected theoldermorphologi-
Bijdragen tot deDierkunde, 64 (2) - 1994 73
cal theory on grounds spurious to its proven effi- and Arthropodaarenotsister taxa: Aphylogeneticanalysis
cacy, and as aresult morphological investigations ofspiralianmetazoanmorphology.Syst. Biol.,41: 305-330.
passed intoeclipse. Eventoday, investigators often Emerson,M.J.&F.R. Schram, 1990.Theoriginofcrustacean
biramous appendages and the evolution of Arthropoda.
view analyses of pattern as somehow less impor-
Science, 250: 667-669.
tant, even less "scientific", thanthose ofprocess. Frankel, J., 1989. Pattern formation. Ciliate studies and
With the150thanniversary ofOwen's definitionof models: 1-314 (Oxford Univ. Press, New York).
homology, webelievethe timehas come to redress GeoffroySaint-Hilaire,É., 1818-22. Philosophieanatomique:
this imbalance. 1-517 (J.B. Baillière,Paris).
Gould, S.J., 1977. Ontogenyand phylogeny: 1-501 (Belknap
Press, Cambridge,Mass.).
Gupta,A.P. (ed.), 1979. Arthropodphylogeny: 1-762 (Van
Acknowledgements Nostrand Reinhold,New York).
Holland, P., 1992. Homeobox genes in vertebrate evolution.
This research has obtained partial support from BioEssays, 14: 267-273.
grants fromthe ItalianNationalResearch Council Jacobs,D.K., 1990.Selector genesand the Cambrian radiation
ofBilateria. Proc.natl. Acad. Sei., 87: 4406-4410.
(C.N.R.) and the Italian Ministry of the Univer- Kimmel,Ch.B.,1993.Patterningthe brainofzebrafishembryo.
sity and Scientific and Technological Research Ann. Rev. Neurosciences, 16: 707—732.
(MURST) toA.M. Lawrence,P.A., 1992.Themakingofafly: 1-228 (Blackwell,
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