Aplacophora as Progenetic Aculiferans and the Coelomate Origin of Mollusks as the Sister Taxon of Sipuncula

22 Pages·1993·9.9 MB·English

by  A H Scheltema

Reference: Bin/. Bull 184: 57-78. (February, 1993)
Aplacophora as Progenetic Aculiferans
and the Coelomate Origin of Mollusks
as the Sister Taxon of Sipuncula1
AMELIE H. SCHELTEMA
\Vootls Hole Oceanographic Institution, Woods Hole, Massachusetts 02543
Abstract. Evidence is presented in support of the fol- several internal structures that, although they appear to
lowingphylogenetic hypotheses: (1)Sipunculaarethesis- be in a primiDtive state, areactually secondarily derived as
ter taxon of Mollusca; (2) the two aplacophoran taxa, is quadrant specification during early cleavage.
Neomeniomorpha (= neomenioids) and Chaetodermo-
morpha (= chaetoderms), are monophyletic with a com- Introduction
mon neomenioid-like ancestor, and of the two taxa, The uniqueness ofAplacophora among Mollusca lies
Chaetodermomorpha are more derived; (3) Aplacophora in theirderived vermiform body in combination with an
and Polyplacophoraaresistertaxaand formaclade, Acu- internal organization that appears to reflect a primitive
lifera; (4) Aculifera are the sister group ofthe remaining molluscan state, especially the simple ladderlike nervous
extant mollusks, Conchifera; and (5) Aplacophora are system, serial musculature, distichous radula (two teeth
progenetic Aculifera. per row) in its plesiomorphic aplacophoran state, simple
The evidence is based on homologies ofearly and late digestive system, and epidermis that produces an aculif-
emhryological development, adult morphologies, and erous cuticle. Their evolutionary significance to the phy-
molecular analyses. Embryological development in si- lum has longbeen a matterforconjecture. Firstcamethe
punculans and mollusks shows a close relationship be- question ofwhether Aplacophora wereeven mollusks, as
tween them, and embryological development ofthe shell theylackanumberof"typical" characterssuchasashell,
separates Aculifera and Conchifera. Adult morphologies mantle, and kidneys (e.g., Thiele, 1902; H. Hoffmann,
indicate: (1) monophyly ofAplacophora; (2) sister-group 1929-30), but they have more usually been considered to
relationship between Aplacophora and Polyplacophora; belongwithin thephylum becauseofsimilaritiestochitons
(3) a molluscan plesiomorphy of nonsegmented serial in theirnervoussystem (Amphineura) and spicules(Acu-
replication oforgans; and (4) progenesis in Aplacophora. lifera) (e.g., Spengel. 1881; Heath, 1911). Further discus-
Molecularevidencesupportstheembryological and mor- sions were concerned with whether aplacophorans were
phological relationshipsbetween Sipunculaand Mollusca. "degraded" or truly "primitive" mollusks (see Hyman,
Mollusca are thus hypothesized to be coelomate Eu- 1967, pp. 68-70 for a historical account).
trochozoa, which share an ancestor that probably had se- There have been no current arguments which separate
rialreplication oforgans. Differencesinsizeandstructure Aplacophora from Mollusca since evidence for a close
of the coelom among Eutrochozoa are hypothesized to relationship between Aplacophora and Polyplacophora
have been brought about by changes in the timing and was published by S. Hoffman (1949), but under present
the process ofcavitation of the mesodermal bands that discussion is their origin and position within the phylum
arise from cell 4d. Through the process of progenesis (Salvini-Plawen, 1972. 1981a, 1985; Scheltema, 1978,
Aplacophora retained an ovoid embryological shape and 1988), as well as the origin ofthe phylum Mollusca itself.
Mollusca have been argued eithertohaveanoncoelomate
R'eCcoenitvreidbut1i9oAnugNuoss.t 81929025;farcocmepttehde W25ooNdosveHmobleerOc19e9a2n.ographic In- onreilgiian-Eacnhdiutroa-bSeiptuhencsuilsater(Staalxvoinnio-Pfltahweene,uc1o9e7l2,om1a9t8e5Afnig-.
stitution, and 314 from theSmithsonian MarineStation at Link Port. 42), or to be eucoelomates with an ancestor in common
57
58 A. H. SCHELTEMA
with other coelomates (Wingstrand, 1985; Scheltema. be a molluscan apomorphy. not homologouswith annelid
1988). In either argument, Aplacophora have been con- or sipunculan coelom. Alternatively, the molluscan peri-
sidered stem formsand therefore preceded the Monopla- cardium can be considered as reduced from a large coe-
cophora with serial replication oforgans. lomic space homologous to that in other eutrochozoa.
Hypotheses for a noncoelomate origin rest on the ar- The involvement ofthe pericardial coelom in excretion
gument that the worm-like Aplacophora with replicated is unique to mollusks. Ultranltration of blood occurs
lateroventral musculature evolved from a turbellario- through podocytes that are present in most molluscan
morph ancestor, and that consequently the molluscan classesincludingAplacophora(Andrews, 1988; Reynolds
coelom is not homologous to that in the Eutrochozoa. A and Morse, 1991).
coelomate origin has been hypothesized from annelid- Five independent lines of evidence indicate that re-
mollusk relationships, including the presence ofa cell 4d duction ofcoelom is the case, and that Mollusca are eu-
that gives rise to mesoblasts and consequently a homol- trochozoan coelomates: (1) presence of the molluscan
ogous coelom, the presence ofa trochophore larva, and cross in mollusks and sipunculans and (2) homology of
serial repetition of body parts. Because the molluscan certain characters in larvae ofmollusks and sipunculans
coelom is small and unsegmented, the idea that annelids indicate that mollusksand sipunculans are sistertaxa; (3)
and mollusks form a clade with a common segmented a large pericardium among"primitive" mollusks indicates
ancestor is poorly accepted. The dichotomous choice be- thatit isa molluscan plesiomorphy; (4)theembryological
tween eitheraturbellariomorph oran annelid-like ances- development ofmesoderm in annelids, mollusks, sipun-
tor for mollusks has dominated recent thinking about culans, and nemertines is similar, and the coelom in the
molluscan evolution (e.g., Hyman, 1967; Haszprunar, fourgroups is homologous; and (5) moleculardatagroups
1992), and the relationship of mollusks to other Eutro- mollusks with other eutrochozoans.
chozoa has not been examined. However, recent molec-
ular data discussed below urge reconsideration of mol- Sipunculans as sister taxon ofthe mollusks
luscan relationships to other phyla.
Evidence is presented here to support the hypotheses An evolutionary relationship between sipunculansand
that(1) Molluscaareeucoelomateswith theirclosest living mollusks lies in their early embryological development
relatives in Sipuncula, theirsistergroup; (2) Aplacophora and in morphological features ofsipunculan pelagosphera
and Polyplacophora are sister groups in the subphylum and molluscan larvae.
Aculifera(contradictingScheltema, 1978, 1988);(3)Acu- Molluscan cross. The molluscan cross is found in the
liferaare thesistergroup ofthe remainingliving mollusks, embryological development of Gastropoda, Polyplaco-
Conchifera; (4) the aplacophoran taxa Chaetodermo- phora, Scaphopoda, and Aplacophora by the end ofthe
morpha (= Caudofoveata, here also called chaetoderms) 64-cell stage (Verdonk and van den Biggelaar, 1983;
and Neomeniomorpha (= Solenogastres sensu nomine Heath, 1899; van Dongen and Geilenkirchen. 1974; Baba,
Salvini-Plawen, here also called neomenioids) are mono- 1951). It is formed by la'2-ld12 cells and their descen-
phyletic, sharing a neomenioid-like ancestor; and (5) dents, with cells la"2-ld"2, called peripheral rosette cells,
aplacophoransare progenetic Aculifera. Considered in the formingthe angle between the armsofthecross(Fig. 1A,
discussion is the homology ofthe eutrochozoan coelom B, D, peripheral cells solid black). In Annelida, however,
and the evolutionary difference between metamerism, or it is cells la"2-Id"2 that form the cross (Fig. IE, cross
segmentation as it occurs in the annelids, and serial rep- cells solid black) (Wilson, 1892). In the 64-cell stage of
lication of organs, as found in Neopilina and Vema the neomenioid aplacophoran Epimenia vermcosa figured
(Wingstrand, 1985). The term "metamerism" is used here by Baba (1951), a molluscan cross seems apparent from
only to denote a segmented coelom; "serial replication" Baba'sshading(Fig. ID), although Salvini-Plawen (1985)
isused todenotethe moregeneral caseofserial repetition found "no definite cross formation" in the same source.
oforgans, whether or not by metameres. Manuscript drawings by G. Gustafson of developing
Chaetoderma nitidulum eggs likewise show a molluscan
Evidence that Mollusca are Descended cross. In contrast to most mollusks, early cleavage in Pe-
from Coelomates lecypoda is asynchronous and bilateral, and no cross is
Mollusca have acoelom consisting ofgonadal lumina, formed; its absence would seem to be an apomorphy.
pericardium, and kidneys, as well as part ofthe gameto- Likewise, development in Cephalopoda seems an apo-
ducts in Aplacophora. A noncoelomate ancestry calls for morphy ofthat group, which has telolecithal eggs, early
thewidening ofa pericardial space lined by mesoderm as bilateral cleavage, and no molluscan cross.
protection for a heart (Salvini-Plawen, 1968a, 1972; not In Sipuncula, a molluscan not an annelid cross is
discussed 1985, 1990) and for gonads separate from the formed, as Rice ( 1975, 1985) has emphasized and refig-
pericardium. This development ofcoelomic spaces would ured from Gerould ( 1906), who firstdescribed itspresence
APLACOPHORA: PROGENETIC COELOMATES 59
that metamorphoses from a trochophore stage (Rice,
1975, 1985). Gerould noted the resemblance ofthe pela-
gosphera lip glands to chiton larval pedal glands, and of
the pelagosphera buccal organ to the radula sac in chiton
larvae (Figs. 2, 3, 4). Pelagosphera larvae can eitherswim
upright with the large metatroch or creep, head-down,
along a solid surface. These activities are lost along with
the larval head at metamorphosis. Jagersten (1963) first
described creeping in living pelagosphera, and he related
it to a creeping gastropod. He also noted that the buccal
organ (= pharyngeal bulb, Schlundkopf) was used in
feeding. Later Jagersten (1972) proposed a possible, but
not certain, homology of the pelagosphera lip, which is
the creeping surface posterior to the mouth, and the
creeping lobe, or foot, between mouth and anus ofmol-
luscan larvae.
Rice (1975, pp. 120-121) described the creeping lo-
comotion ofpelagosphera as follows: "The larva is able
to ... glide along with . . . [the] head flattened against
the bottom. Frequently the larvae . . . may crawl in the
manner ofan inchworm. presumably scraping material
from the bottom. The continual eversion of the buccal
Figure 1. (A-D) The molluscan cross. (A) Gastropoda (Lyniiiucu organ duringfeedingprobablyaidsintheremoval offood
(siBa)gnPaolliys.plaafctoeprhVoreard(oSntkenoapnldaxvahneatdheinanBai.ggaefltaearr.Hea19t8h3,,1p8.991.1p1i.fi3g2.,3fbi)g;. from the substratum. Thistough muscular organ [covered
23);(C)Sipuncula(Golfingiavulgaris. afterGerould, 1906.p.99,fig. D, by cuticle. Rice, 1973] isbelieved to function in breaking
aspublished in Rice, 1975, p. 99. fig. 17); (D) Aplacophora (Epimenia up material intosmall panicles forfeeding. . ." A mucus-
verrucosa.afterBaba, 1951.p.46,fig. 18).Theapical rosette la'"-ld'" likesubstancefrom the lipglandsissecretedastheanimal
csisehlslohswonawrneinisnchoofaiwrnens,ecislntoisfpeipnlsei,tnigpo;pplepienngr;isptahirepmrplasilnogfr;otshteeitptcercoeclselslslsloaf'l:ac-"rIo2ds-'sl2d2a"an:d"-adr2aedu"gsohltaierdre; cmoomvme.s).aloMnyg aonwanturraelcesnutbsotbrsaetruvmat(iRoincse,o1n98l1ivainngd ppeelras.-
and trochoblast cells Ia2-Id2 are clear. In Epimenia (D), the cleavage gosphera corroborate many ofRice's.
stageappearstobe earlierthan shown in A-C, asthe tipcells have not Precise descriptions ofthe protrusible buccal organ and
yet separated from 2a' and 2c' (indicated by question marks), and the lip gland have been given by Rice (1973). The buccal
arms ofthe cross are not quite straight, similar to an earlier stage in organ isa muscularsac, ventral and posteriortoacuticle-
dPioslcyeprlnaibcloephionrHae(aHteha'tshi.ll1u8s9tr9a.tipoin.,3a2,ndfigi.n1C7).tiIpncBe,llsonwleyreonneottipincdeillcawtaesd lined invagination calledthebuccalgroovethatliesbelow
inGerould'soriginalfigure.(E)Annelidcross,Polychaeta(Nereis)(after the esophagus. The epithelium of the buccal organ is
Wilson, 1892,p.396.diagramII).Theapicalrosette la1"-Id"'isshown overlain by the cuticle ofthe ventral side of the buccal
infine,closestippling;peripheralcells la'2-ld12areshowninfine,open groove and is the area first protruded (Fig. 2). Although
stippling;and thearmsofthe crossfrom la"2-ld"2 aresolid. the precise innervation ofthe buccal organ was not dem-
onstrated, thecircumesophageal connectives, which arise
from the dorsal cerebral ganglion, are closely associated
in sipunculan development (Fig. 1C). The presence ofa with the organ. Both the topography and function ofthe
molluscan cross during embryological development is buccal organ and groove are remarkably similar to those
understood here to be of phylogenetic importance, and ofthe radularapparatus in mollusks: ventral odontophore
sipunculans and mollusks share a character not found in = buccal organ; ventral radula sac = buccal groove; and
either annelids or flatworms (Freeman and Lundelius, ventral cuticular radula = ventral portion ofthecuticular
1992). Its presence can be considered apomorphic to the buccal groove. Furthermore, the odontophore and prob-
embryonic morphology of turbellarians, which lack a ablythebuccal organ are innervated through connectives
cross. united with the cerebral ganglion. The homology would
Similarities between sipunculan andmolluscan lan'ae. be more certain ifitwere known whetherthebuccal organ
Gerould (1906) noticed certain other resemblances to musculature is formed from mesoderm, as is the odon-
mollusks besides the molluscan cross in thedevelopment tophore ofmollusks (Raven, 1966), or whetherit is myo-
ofsipunculans. In particular, he found similaritybetween epithelial asinarchiannelids(Jagersten, 1947; Rice, 1973).
sipunculan pelagosphera and molluscan larvae. The pela- The lip gland takes several forms in various pelago-
gosphera is uniqueto sipunculans. It isaswimming larva sphera, from a bilobed to a paired or four-lobed body
A. H. SCHELTEMA
which opens either directly, or by way ofa ciliated duct
or ducts, into the lip pore. In comparison, the anterior
pedal gland in larval chitons and in Aplacophora isduct-
less (cf.. Figs. 2A, 4B, 6C). Aplacophora, but not chitons,
have a central ciliated pit.
Similarities in form and function in these three struc-
tures lip and foot, lipglandsand pedal glands, and buc-
cal organ and radula with its sac are striking. Their
morphologies are particularly clear in sagittal sections of
a pelagosphera and a chiton larva (Figs. 3, 4). There are
also similarities in their development, as they all arise
from posttrochal ectoderm, with these differences: in si-
punculans, the origin ofall three structures isstomodeal,
whereas in mollusks, the ventral somatic plate, usually
from cell 2d, gives riseto the foot and itsglands, and only
the radula sac is stomodeal (Raven, 1966). In Sipuncula
aswell, cell 2dgivesrisetothesomatic plate, which forms
theectoderm ofthetrunk(Rice, 1976). In mollusks, how-
ever, the proximity and functional interdependence of
thesomaticand stomodeal structuresare indicated bythe
pedalcontribution tofeedingin veligerlarvae. Ananterior,
medialciliarytractisformedon thefootbywhich particles
unsuitable for ingestion are rejected (Moor, 1983).
Onlythe head region ofthe pelagosphera, which israd-
ically altered during metamorphosis to ajuvenile sipun-
culan. can be compared to the Mollusca. The posterior
part of the body with its large coelomic sac, nephridia,
mid-dorsal anus, and ventral nerve cord, are already de-
finitive adult structures.
Evidence from the presence ofthe molluscan crossand
from locomotary and feeding structures that are similar
in mollusks and larval sipunculans is sufficiently strong
that the two phylacan beconsidered as sistergroups, and
mollusks, therefore, as eucoelomates. Of course, if the
primitive mode ofsipunculan development should prove
to be by way ofa nonfeeding, lecithotrophic larva, then
the similarities between planktotrophic pelagosphera and
molluscan larvae would be convergent. However, Rice
(1985) most recently considered evolutionary questions
ofsipunculan larval development and concluded that a
yolkyeggand short-lived planktotrophic pelagospherawas
the primitive mode ofdevelopment.
Otherconsiderations. Two further observations can be
made to support arguments for a sipunculan-molluscan
sister relationship, one embryological, the other paleon-
tological. The first is the embryological development of
Echiura (Newby, 1940) compared to that of the sipun-
culans. Echiurans have traditionally been linked with si-
punculans, both having worm- or sac-like, unsegmented
coelomate bodies, but echiurans afford a contrast to si-
Figure2. PeiagospheralarvaeofSipuncula.(A)Frontalviewofhead.
Siinmailu*sp. (from Rice, 1981, fig. 4). (B) Entirelarva.Aspidosiphon punculans in their closer relationship to annelids. They
sp. (from Rice, 1981, fig. 6). Numbers as in Figure 3: I huccal gland, haveanannelidcrossratherthana molluscan crossduring
3 poreoflipgland,4 mouth, 5 lip. early cleavage, and as in annelids, the major ciliary band
API ACOPHORA: PROGENETIC COELOMATES 61
metazoans. One pieceofevidence foran earlysipunculan
history is the mid-Cambrian genus Ottoia from the Bur-
gess Shale. Considered priapulids by Conway Morris
(Whittington, 1985)and close to priapulids by Banta and
Rice (1976), the genus indicates great diversity of spe-
cialized sacciform, coelomate orpseudocoelomate, worm-
like animals already in the early Paleozoic. Sipunculans
therefore could have a very long, but unobservable and
unverified, geologic history. A second piece ofevidence
isthatsipunculanscontain hemerythrins, found alsoonly
in priapulids, lingulid brachiopods, and some annelids
(Curryand Runnegar, 1990). Because lingulidsand prob-
ably priapulids and annelids are known from the early
Cambrian, the presence ofhemerythrins indicates a very
long history for all forms having these oxygen transport
molecules.
Si:e ofthepericardium in "primitive" mollusks
The pericardium is larger relative to the heart in Apla-
cophora, Monoplacophora, and Polyplacophora than it
is in Gastropoda, Pelecypoda, and Cephalopoda (Schel-
tema, 1973, 1988; Scheltema and Kuzirian, 1991) (Figs.
5, 6A). Ontogenetically, the pericardium is already large
before the heart develops from pericardia! epithelium in
Aplacophora (Baba, 1938), and in Polyplacophora de-
velopment ofthe pericardium precedes development of
the gonad (Hammersten and Runnstrom, 1925). Thus
the polarity of pericardia! size is from large to small in
Mollusca, and thecontinued reduction within the phylum
is considered to be a derived condition ofthe Mollusca.
Figure3. Midsagittalsectionofthepelagospheralarva,Phascolosoma
agassi:ii(from Rice, 1973, pi. 5). 1 buccalorgan, 2 lipgland, 3poreof
lipgland, 4 mouth, 5 lip, 6 stomach, 7 coelom, 8 esophagus.
ofolder echiuran larvae is the prototroch anterior to the B
mouth. In sipunculan pelagosphera. the metatroch below
the mouth, not the prototroch, is the major swimming secFtiigonuroef4A.cantNheowclhyitsoenttdliesdcrleapravnaes(oafftPerolHyapmlamcaorpshtorean.a(nAd)RMuindnssagtirtotma,l
organ. Indeed, the region in pelagosphera that forms the 1925, fig. E, figure reversed). (B) Ventral view ofStetwplax hcalhiana
head with its locomotory lip, lipgland, and buccal organ, justaftermetamorphosis(afterHeath. 1899,fig. 59).Theopeningofthe
is represented in echiuran larvae by only a few rows of pedalgland(3) liesposteriortothe mouth (4); theglandopensthrough
cellsbetweentheprototrochand metatroch, and nolarval "aseriesof. . .intercellularchannels"ratherthanaduct(Heath, 1899,
organs are present. p3.o6p3e1n)i;ncgoomfppaerdealwgiltahndF,ig4urmeou6tCh.,15rfaodoutl,a6slaacr,va2laenytee.rSitorrucpteudraelsgnluanmd-,
If sipunculans are sister taxon of the Mollusca, they bered 1-5 are homologoustostructureswith thesamenumbersin Figs.
must have arisen, like mollusks, early in the evolution of 2 3.
62
A 9
9 9
Figure 5. Large pericardia! space and heart in primitive molluscs. (A) Aplacophoran, Chaetaderma
nitidulum, sagittal section. Gametes pass from the gonads through the pericardium with its large, paired,
lateral extensions ("horns") and thence into gametoducts leading to the mantle cavity (from Scheltema.
1973,fig. 2,andScheltema, 1988,fig. 13).(B)Polyplacophoran, Chitonsine/am, crosssection(afterWissel,
1904, pi. 24, fig. 49). (C) Monoplacophoran. Neopilinagalathea. dorsal view, with paired pericardia! sacs,
paired ventricles,andtwopairsofauricles(afterLemcheandWingstrand, 1959,fromScheltema, 1988, fig.
13).(D)Polyplacophoran,Acanlhopleiiraechinata, dorsalview,withtwopairsofopeningsbetweenauricles
and ventricle (after Plate, 1898. from Scheltema, 1988. fig. 13). 1 pericardium, 2 ventricle, 3 auricle,
4openingbetween auricleand ventricle, 5 auriculoventricularvalve, 6aortal bulb, 7 gonopericardial duct,
8 lateral extension ofpericardium, 9gametoduct.
Development ofmesoderm from mesoderm that originates from embryonic cell 4d.
This cell gives rise to a pair of mesodermal teloblasts,
The interpretation that the coelom is reduced in Mol- which migrate inward to a ventrolateral position, one on
lusca assumes that the molluscan pericardium is homol- each sideofthe midline (Verdonk and van den Biggelaar,
ogoustothecoelom in otherspiralian coelomates, namely 1983;Anderson, 1973;Rice, 1975)andproliferate forward
Annelidaand Sipuncula. In all three,thecoelom isformed into two lateral mesodermal bands. Mesodermal bands
APLACOPHORA: PROGENETIC COELOMATES 63
Figure6. (A)Cross-section through the pericardium ofa neomenioid aplacophoran, Helicoradomenia
juani (from Scheltema and Kuzirian. 1991, fig. 5C). (B) Cross-section through the pedal gland and pedal
pit ofa neomenioid aplacophoran, Ocheyoherpia sp. The voluminous pedal gland occupies most ofthe
headregion;thelobesoftheglandarein varyingstagesofsecretion.(C)Ciliatedpedal pitofHelicoradomenia
juani. The pedal gland discharges into the pedal pit, not through distinct ducts, but through numerous
channelsasdescribedforchitons(Fig.4B).(D)Secretoryepidermalpapillaeoftheneomenioidaplacophoran,
Helicoradomeniajuani (from Scheltema and Kuzirian, 1991, fig. 2C). (E) Secretory epidermal papillae of
thepolyplacophoran.Acanthochitonfascicularis(from Fischerelai, 1980, fig. 3). 1 pedal gland, 2 ciliated
pedal pit, 3dorsal blood sinus, 4dorsalcecum ofmidgut, 5 cerebralganglion, 6oralcavity, 7 pericardium,
8 auricle, 9 ventricle, 10 ovum. 11 U-shaped gametoduct, 12 copulatory spicule pocket, 13 foot. Asterisks
in Dand E, cavitiesofdissolved spicules.
64 A. H. SCHELTEMA
are present as well in Nemertini (Turbeville, 1986). In cussthe presence orabsenceofacoelom. Ghiselin (1988)
annelids, sipunculans, and nemertines, the coelom is considered the evolution ofMollusca in light ofthe mo-
formed bycavitation (schizocoely) ofthe bands. Thecoe- lecular evidence given in Field et al. (1988), amplifying
lom constitutes the major body cavity in annelids and the data with an analysis of specific nucleotides and a
sipunculans, but in nemertines it forms only vessels for useful history of molluscan phylogenetic hypotheses.
bloodcirculation (Turbeville, 1986). In mollusks, theme- Ghiselin favored a segmented, coelomate eutrochozoan
sodermal bands break up into masses of coelenchyme, ancestor, with loss or reduction of segmentation in the
from which is formed a solid anlage or pair ofanlagen Mollusca. Salvini-Plawen (1990), however, retained a
that cavitate to form the pericardium, heart and kidneys preference fora turbellariomorph molluscan ancestry and
(Raven, 1966; Moor, 1983). In some molluskswith paired refuted the validity ofthe sequencingby Field et al. (1988)
anlagen, the pericardium begins as paired cavities before and Ghiselin (1988), because "for some selected, tradi-
becoming united (Raven, 1966). In Neopilina the peri- tionally monophyletic groups [including mollusks] eu-
cardium is still paired (Fig. 5C), and the large pericardia! phemistic premises are made" by eliminating some data
"horns" in some Aplacophora (Fig. 5A) may reflect an as convergences. Willmer and Holland (1991) also con-
ancestral paired condition. sidered that mollusks had a flatworm origin and suggested
The coelom amongthe spiralian protostomes described that RNAanalysisofseveral Platyhelminthes might show
here is interpreted as being homologous because ofsim- them to be poly- or paraphyletic, but the work ofTurbe-
ilarities in early embryological development. Differences ville et al. (1992) indicates that they are monophyletic.
in coelom formation among the four phyla apparently
arise from variations in the timing ofcavitation after the Monophyly ofAplacophora
mesodermal bands have formed; but the differences in
process are not considered sufficient to deny homology A proposed homology of the chaetoderm oral shield
ofthe coelom. A single pericardium formed by fusion in with the creeping sole ofthe archimollusk was the basis
mollusks other than Neopilina is thus an apomorphy. forseparatingthe two aplacophoran taxa into two classes
(Fig. 7B, C; Fig. 8A) (Salvini-Plawen, 1972, 1985, 1990).
This homology was based on the innervation ofthe oral
Molecular evidence
shield (Salvini-Plawen, 1972), the character of the epi-
Recent sequencing of 18S ribosomal RNA among 22 dermis, and the presumed homology ofcuticular struc-
classes (not including Aplacophora), in 10 animal phyla, tures (Fig. 8C, arrowhead) (S. Hoffman, 1949), but it is
split offacoelomate Platyhelminthesassistergroupofthe not upheld either by light or transmission electron mi-
remaining bilaterian taxa, the eucoelomates, which fall croscopy (Scheltema et al., in press, fig. 9; Tscherkassky.
into four closely rooted groups (Field ct ai, 1988). The 1989). The oral shield cuticle is continuous with that of
group termed Eutrochozoa (Ghiselin, 1988) includes five the pharynx and isa lip. and the innervation ofthe shield
analyzed phyla: Mollusca, Annelida. Brachiopoda, Po- is cerebral, lying anterior to that part ofthe anterior ner-
gonophora, and Sipuncula. More recently Turbeville el voussystem considered "tentacular," and thuspart ofthe
al. (1992) haveadded Nemertini tothe Eutrochozoa,bas- head region, by Ivanov (1991). Accordingly thetwo apla-
ing their results on 18S rRNA and analyzing two Platy- cophoran taxa cannot be separated on the basis of the
helminthes, in addition to the single flatworm analyzed chaetoderm oral shield, although Salvini-Plawen (1990)
by Field el al. (1988). A re-analysis by Lake (1990) ofthe recentlyarguedthatthehomology holdsbecausethefore-
1988 data positioned Sipuncula closest to Mollusca and gut and oral-shield epitheliaaredifferent, andthe presence
Brachiopoda, with Annelida and Pogonophora as sister ofthecuticleissecondary. Inaschematicdrawingthrough
groups. The presence of hemerythrins in Brachiopoda, an oral shield, Salvini-Plawen (1990, fig. 7) showed asep-
Sipuncula, and some Annelida affords independent sup- aration, the "mantle rim," between the oral shieldcuticle
port from molecular data for some ofthe results ofField and bodycuticle, but thisseparation does notexist in my
t't al. (Curry and Runnegar, 1990). experience (Scheltema et al., in press, fig. 9B). The ar-
The relationships among Sipuncula, Mollusca, and gument would be clarified ifit were known whether the
Brachiopoda, however, remain unresolved, and possible oral shield is stomadeal in origin.
synapomorphies of sipunculan and molluscan larval Severalsynapomorphiessuggestthatthetwoaplacoph-
characterswere nottaken intoaccountby Lake. Although oran taxaaremonophyletic. Theoutgroup forcomparison
the molecularevidence isstill incomplete, it suggeststhat is Polyplacophora.
molluskshavedescended from acoelomate ancestor, and Thetetraneural nervoussystem, includingthecerebral
thatsipunculansaretheirclosestsistergroup. In proposing commissure, lateral and ventral nerve cords, and supra-
that the last common ancestor ofthe Annelida-Mollusca rectal commissure, is more heavily ganglionated in both
lineagewas hemocoelicand segmented. Lakedid notdis- neomenioidsandchaetodermsthan inchitons. Theradula
APLACOPHORA: PROGENETIC COELOMATES 65
Figure7. (A-C)Chaetodermomorpha.(A. B)(.'kern'dermalurnerae. entireanimal(antenortoleft)and
divided oral shield (I'rom Scheltema, 1985, fig. 3L, O. P). (C) Oral shield ofSculOfiim megaradulalu.i (cf.,
Fig.8A)(fromScheltema, 1988,fig.6).(D.E)Neomeniomorpha. (D)Dorymeniasp.(E)Anewneomenioid
genusand species in the family Simrothicllidae. Dand E aredrawn to the same scale, anteriorto left; the
midgutandgonad lie between X-X and Y-Y.
in its plesiomorphic state in Aplacophora is distichous, U-shaped gametoducts lead from the posteriorend ofthe
that is, only two teeth per row (Scheltema, 1988; Schel- pericardium, first anteriorly and then posteriorly, to the
tema el al, 1989), a reduction in number from the doco- mantle cavity (Figs. 5A, 6A, 9D). Separate gonaduct
glossate chiton radula. Both neomenioids and chaeto- openings in species of Phyllomenia (Salvini-Plawen,
derms have a dorsoterminal sense organ (= dorsocaudal 1978) are interpreted here as a derived condition ofthat
sensory pit), or sometimes several, in the epidermis. It is genus.
ofunknown function, although homology to the osphra- The mantle cavity in both neomenioids and chaeto-
dium has been conjectured (Spengel, 1881; Haszprunar, derms is small and posterior, acting as little more than a
1987). Whether or not this homology is correct, the po- cloaca. In neomenioids, the groove on either side ofthe
sition ofthe dorsoterminal sense organ is an autapomor- foot-foldcanalsobeconsideredasreduced mantlegrooves
phy ofthe Aplacophora, for there is no compelling evi- (Figs. 6A, 8C). Thepairedctenidiainchaetoderms, which
dencethatthisposition, postulated tobeprimitive forthe fill mostofthe mantlecavity, isprobablyaplesiomorphy.
molluscan osphradium (Salvini-Plawen, 1985), is other with loss in the neomenioids resulting from the space re-
than an apomorphy shared only by neomenioids and quirements ofa secondarily more complicated reproduc-
chaetoderms. tive system, including sometimes very large copulatory
Thetwoaplacophoran taxashareasimilarreproductive spicules.
system unique among mollusks. Paired gonads, some- Finally, the worm shape itselfis hereconsidered a syn-
timesfused, opendirectlyintothepericardium,andpaired apomorphy of the Aplacophora. and not separate.
Figure8. (A)Cross-section through theoral shield ofachaetoderm,Scutopusmegaradulatus, showing
continuity between pharyngeal and oral-shield cuticle. Arrow indicates transition between homogeneous
pharyngealcuticleandmorespecialized fibrillaroral-shieldcuticlewithathickenedouterlayer(fromSchel-
tema, 1988, fig. 5).(B)Sagittalsectionthroughaneomenioid, liymnomeniasp.,showingseriallateroventral
musculature. (C)Cross-section through the nonmuscular, heavily ciliated foot ofa neomenioid, Helicora-
domeniajuani. Thearrowheadindicatesthenonspiculosecuticleofthemantlecavityextendingalongeach
side ofthe foot groove, which was considered homologous to the chaetoderm oral shield by S. Hoffman
(1949). (D)Cross-section through the radula. radulabolsters, and paired, hollowradulavesiclesinHelicor-
adomenia/lunu(from Scheltemaand Kuzinan, 1991. fig. 4D). 1 oral-shieldcuticle, 2 pharyngeal cuticle, 3
cuticleofbodywall,4 nervefibersfrom precerebralganglion, 5 ovarian region ofhermaphroditicgonad, 6
digestive cells ofundifferentiated midgut. 7 copulatory spicule pocket, 8 foot. 9 radula vesicle, 10 radula,
11 dorsal cecum ofstomach/digestivegland.
66