ON THE ORIGIN OF MOLLUSCS, THE COELOM, AND …...Apr 20, 2020 · mon ancestor toward both. Only differ-ences in the ontogeny could indicate direc-tion; a primitive condition in one

ON THE ORIGIN OF MOLLUSCS, THE COELOM,AND COELOMIC SEGMENTATION

JOSEPH VAGVOLGYI

AbstractMolluscs had a common origin with the annelids, as shown by remarkable ontogenetic

similarities. Their common ancestors were non-segmented (non-eumetameric), acoelomateanimals. Molluscs developed from the common stock through incorporation of the distin-guishing molluscan characters such as the shell, mantle, mantle cavity, radula and ctenidiumand annelids by the adoption of coelomic segmentation and of changes accompanying it.The assertion that molluscs hand ancestors with coelomic segmentation is contradictedby ontogenetic and anatomical facts as well as by theoretical considerations. The commonmoHuscan-annelid stock most likely originated from ancestral flatworms; this is indicatedby the developmental, and to a lesser extent, structural similarities between the flatworms,molluscs and annelids, and by the lower level of organization of the flatworms.

The coelom is a phylogenetically new structure in the molluscs and annelids, and wasacquired independently in the two phyla. Coelomic segmentation also is a phylogeneticallynew acquisition of the annelids; it came about through developmental changes affecting thegrowth of the mesoderm bands. These views are the corollaries of ontogenetic considerations.

A widely held hypothesis concerning theorigin of molluscs is the so-called annelidtheory. According to Hyman (1951:4), the"annelid theory" states that ". . . annelids,arthropods, and chordates are closely re-lated and [that] lower bilateral groups mayhave arisen from annelids by degeneration."In the present paper the term is restricted,referring to the theory that annelids gaverise to molluscs. Early proponents of thistheory (Pelseneer, 1899; Heider, 1914;Soderstrom, 1925; Naef, 1926) believed thatthe serial repetition of certain organs insome molluscs represented vestigial segmen-tation, and claimed on this basis that mol-luscs descended from the segmented worms,annelids. They also believed that the far-reaching similarities in cleavage and earlydevelopment were further indications of thisrelationship. More recent investigatorsadded other viewpoints to these arguments.Thus, Garstang (1928) theorized that mol-luscs evolved from the trochophore larvaeof the annelids by neoteny. Johansson(1952) aimed at giving a functional expla-nation to the annelid theory, when he pro-posed that the molluscs had lost the segmen-tation of their annelid ancestors in turningto living on hard, rocky surfaces of theintertidal zone, and assuming a creeping,

crawling mode of locomotion. And finally,Lemche (1957) reported the discovery of a"living fossil," a primitive, segmented mol-lusc, Neopilina galatheae Lemche, 1957.Soon two more species of Neopilina werefound, N. ewingi Clarke and Menzies, 1959,and N. veleronis Menzies and Layton, 1963.These discoveries were accepted by manyas evidence for the segmented origin ofmolluscs (Lemche, 1959a, 1959b, I960;Lemche and Wingstrand, 1959b; Portman,I960; Fretter and Graham, 1962). Lemchewent so far as to postulate that molluscs aremore closely related to the arthropods thanto the annelids, and that the latter aroseindependently of the former two groups.Fretter and Graham supported this argu-ment by claiming that the coelom is primar-ily small in the arthropods as well as in themolluscs.

Opponents of the annelid theory haverepeatedly pointed out the weaknesses ofit. Thus, Nierstrasz (1922), Hammerstenand Runnstrom (1925), Ivanov (1928, 1944),Beklemishev (1958a, 1958b), Boettger(1959), Steinbbck (1962) and Hunter andBrown (1965) argued that molluscs cannotbe considered as annelids with reducedsegmentation, because of fundamental ana-tomical and developmental differences in

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154 SYSTEMATIC ZOOLOGY

segmentation. Odhner (1961) pointed outthat molluscs attained segmentation inde-pendently of the annelids. Beklemishev(1958b), Boettger (1959), Steinbock (1962)and Hunter and Brown (1965) have arguedconvincingly that Neopilina cannot be con-sidered proof for the annelid origin of mol-luscs, because of differences in the segmen-tations, because Neopilina is not at the rootof the molluscan phylogeny, and for variousother reasons. Yochelson (1963) reached asimilar conclusion from paleontologicalstudies; he maintained that the monoplaco-phoran molluscs (to which Neopilina be-longs ) do not constitute the basic molluscanstock; rather, they are a primitive group ofthe more advanced molluscs. The results ofSchmidt's microscopic and crystallographicstudies (1959) on the shell of Neopilinaare neatly consistent with this conclusion.Further objections, not expounded in theliterature, also can be brought up againstthe annelid theory. The theory does notexplain why we must consider molluscansegmentation secondary and reduced, orwhy we must accept the ontogenetical sim-ilarities between molluscs and annelids as aproof of the annelid theory, when alterna-tive assumptions also are possible. Weak-nesses in Garstang's and Johansson's theoryalso are found, as I will show in a later sec-tion.

To supplant the annelid theory, Lang(1896), Nierstrasz (1922), and Graham(1955) proposed that molluscs evolved fromflatworms or ancestors to the flatworms,completely independently of the annelids.Hammarsten and Runnstrom (1925), Boet-tger (1959 and Beklemishev (1963, on theother hand, argued that molluscs and anne-lids evolved together but separated fromeach other before the annelids acquiredcoelomic segmentations. Whereas, however,Hammarsten and Runnstrom believed thatthe common molluscan-annelid stock origi-nated from the ancestors of the flatworms,Boettger thought that the common stockevolved from a group near the root of theaschelminths, and Beklemishev thoughtit evolved from "larval" coelenterates.

The claims of Lang, Nierstrasz and Gra-ham that molluscs originated independentlyof the annelids overemphasize the similari-ties between the molluscs and flatwormsand underemphasize those between the mol-luscs and annelids. Also, it is not certainwhether some of the molluscan-flatwormsimilarities are due to close relationships orto parallel evolution. For these reasons, Ireject these claims. It also seems doubtfulthat the construction by Beklemishev ofhypothetical larval forms satisfying superfi-cial morphological requirements is of anyhelp. The ideas expressed by Hammarstenand Runnstrom and Boettger (that the an-cestors of aschelminths came from ances-tors of the flatworms), on the other hand,account both for the molluscan-flatwormand the molluscan-annelid similarities, andavoid making unwarranted and unnecessaryassumptions. Therefore, they appear to rep-resent "the truth," according to our presentknowledge.

Thus, it seems that the problem of theorigin of molluscs already has been solved.Many zoologists, however, perhaps even themajority, are either unaware of, or unwillingto accept, this answer. The present paperhas been written with the purpose of sum-ming up the arguments, elaborating uponthose that were not explicit or expounded indue detail, adding some new arguments,and thereby presenting a unified and hope-fully convincing argument for the case.

DISCUSSION

It seems profitable to arrange the argu-ment around the three main points of thetheory followed here. These are: 1) mol-luscs and annelids had evolved together;2) the molluscs separated from the annelidsbefore they acquired the distinguishing mol-luscan criteria such as shell, mantle, mantlecavity, radula and ctenidium (Yonge, 1960;Morton and Yonge, 1964), and the annelidsacquired coelomic segmentation; 3) themost likely ancestors of the common mol-luscan-annelid stock were the forms ances-tral to the present-day flatworms.

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ON THE ORIGIN OF MOLLUSCS 155

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FIG. 1. Segmentation (pseudometamery) of the monoplacophoran mollusc Neopilina galatheae; dia-grammatic. Notice that the various segmented organs occur in different numbers, and that there is onlypartial harmony in their arrangement. The coelomic cavity is represented by the pericardial (not shown)and nephridial cavities. (From Lemche and Wingstrand, 1959b, Galathea Rep. 3:9-71, with permission ofthe editor.) 1, mouth; 2, pedal nerve cord; 3, nephridium; 4, pedal retractor muscle; 5, commissure; 6,gonad; 7, gill; 8, aorta; 9, ventricle; 10, auricle; 11, lateral nerve cord; 12, anus.

The common origin of molluscs and an-nelids.—This contention is based upon thesimilarities between the molluscs and anne-lids in cleavage, embryonic development,and early larval stage. Both the molluscs

and the annelids have spiral cleavage; thefate of certain cells is, with some exception,the same in the two groups; mesodermbands arise from cell 4d in both groups;and the early larval stage, the trochophore,

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is nearly identical. These similarities areaccepted as indications of a genuine andclose relationship by practically all zoolo-gists (Hyman, 1951; Barnes, 1963). A con-sensus, admittedly, does not constitute aproof; it does give, however, the best sup-port to the above view.

The developmental similarities in ques-tion were interpreted by some followers ofthe annelid theory (Naef, 1926) as support-ing the contention that the molluscs evolvedfrom the annelids. It is quite clear, how-ever, that this claim is unwarranted. Sim-ilarities in the ontogeny only "prove" thatthe groups in question are closely related,but they do not "prove" the direction ofevolution. On the basis of the developmen-tal similarities alone, the direction couldequally well be from molluscs to annelids,from annelids to molluscs, and from a com-mon ancestor toward both. Only differ-ences in the ontogeny could indicate direc-tion; a primitive condition in one group,and a more advanced in the other, wouldindicate that evolution proceeded from theformer to the latter.

There are two obvious, although slight,differences between the molluscan and an-nelid ontogenies. One is the formation ofthe crosses, the other that of the coelomiccavities. The cells forming the major partof the equatorial ciliary band of the troch-ophore larva are arranged, at an earlystage, in the shape of a cross centered onthe animal pole; the arms of the cross areradial in molluscs, interradial in annelids,and they are derived from cells Ia12-ld12 inmolluscs, from Ia112-ld112 in annelids (Nier-strasz, 1922). Now, if we could ascertainwhich type of cross formation were the moreprimitive, we could possibly draw someconclusion as to the direction of evolution;but, unfortunately, nothing is known on thissubject. In the formation of the coelom(p. 158), the direction seems to have beenfrom molluscs to annelids. Thus, summingup, the developmental similarities indicateclose relationship between the molluscs andannelids, they suggest that in some respectsmolluscs are more primitive than annelids,

but they do not support the claim that mol-luscs developed from annelids.

The separation of molluscs and anne-lids.—The separation of molluscs and anne-lids must have happened at or before thetime molluscs and annelids acquired theirdistinguishing features (Hammarsten andRunnstrom, 1925; Boettger, 1959), but notafter. There is no evidence whatsoever forthe assumption that annelids had ancestorswith characteristic molluscan features, orthat molluscs had ancestors with character-istic annelid feature. Therefore we have toassume that each line acquired its own char-acteristic features after the separation ofthe two lines.

Most zoologists would agree with thefirst part of this conclusion, that annelidsdid not come from molluscs; but manywould also maintain that molluscs did havesegmented ancestors. They argue that a)primitive molluscs are segmented, and thatb) this must mean that molluscs descendedfrom ancestors with a more complete seg-mentation.

The decision whether the primitive mol-luscs, or the molluscs in general, are or arenot segmented depends upon one's defini-tion of segmentation. Adherents of the an-nelid theory consider segmentation to beany repetition of organs along the main axisof the body. Thus, they say that the mol-luscs are segmented. Evidently, theseworkers consider the segmentation of mol-luscs of the same kind as that of the anne-lids. Many others, however, consider theserial repetition of certain organs, withoutcorresponding coelomic subdivisions andwithout the developmental characteristicsof the annelid segmentation (see below)merely regularization metamery or pseudo-metamery; and these others distinguish be-tween this and the mesodermal or coelomicor true segmentation, referred to henceforthas eumetamery, of the annelids (Ivanov,1928, 1944; Beklemishev, 1958a, 1958b;Steinbock, 1962; Clark, 1964; Hunter andBrown, 1965). In this view, then, the mol-luscs lack true segmentation or eumetameryand have only pseudometamery.

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FIG. 2. Segmentation (pseudometamery) of a polyplacophoran mollusc (chiton); diagrammatic. No-tice that the number and arrangement of the various segmented organs, as in Neopilina, is not matching.The coelom is represented by the pericardial (not shown) and nephridial cavities. (Redrawn fromBarnes, R., 1963, Invertebrate zoology, after Haller, Lang and Yonge, with permission of the author andthe publisher.) 1, mouth; 2, shell plate; 3, gill; 4, foot; 5, girdle; 6, anus; 7, ventricle; 8, auricle; 9, kidney;10, gonad; 11, aorta; 12, commissure; 13, pedal nerve cord; 14, lateral nerve cord; 15, brain.

The differences between the pseudo-metamery of molluscs and the eumetameryof annelids are anatomical, ontogenetical andphylogenetical. There are three main ana-tomical differences (Beklemishev, 1958a;Boettger, 1959; Steinbock, 1962). First, themolluscan coelom is not segmented (figs. 1and 2; also see p. 158 about the nephrocoel),whereas in annelids, there is typically a pairof coelomic sacs in each segment (Fig. 3).The molluscan coelom is not even fullyhomologous with the annelid coelom; thistopic may be discussed more profitablylater, after the ontogeny has been described.Second, in molluscs the various segmentedorgans may occur in different numbers.Thus, the monoplacophoran mollusc Neo-

pilina galatheae has two pairs of atria, fivepairs of gills, two pairs of gonads, six pairsof nephridia, eight pairs of pedal retractormuscles and ten pairs of nerve commissures;these numbers may slightly be different inN. ewingi and N. veleronis. Chitons haveeight shell plates with attached muscles, anda varying, sometimes very great, number ofgills and nerve commissures. Furthermore,the gills of chitons are not even paired,strictly speaking; their number may be dif-ferent on the right and left sides in as manyas 48% of the specimens in some species(Hunter and Brown, 1965). In contrast tothis, the segmented organs of the annelids,the parapodia, ganglia, commissures, circu-lar blood vessels, nephridia, coelomoducts

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and coelomic sacs occur in identical num-bers (or multiples), and are strictly paired.Third, the arrangement of the various seg-mented organs is less regular in the molluscsthan in the annelids. It is true that Neo-pilina exhibits an almost completely orderlyarrangement; but in chitons the gills areunevenly distributed between the body seg-ments, as determined by the shell plates,and the commissures are arranged discord-antly from both the gills and the shell plates.Thus, we have to maintain that molluscs asa group have a less orderly arrangementthan do annelids.

The ontogenetic differences between mol-luscan and annelid segmentation are as fol-lows. In molluscs, specifically in the chitonAcanthochiton discrepans Brown (Hammar-sten and Runnstrom, 1925; Raven, 1958),coelomic cavities do not develop inside themesodermal bands, and the latter do notbecome metamerized; instead, they differ-entiate into various organs, among themthe pericardial-nephridial complex. It istrue that Naef (1926), following earlier au-thors, speaks of coelomic cavities in themesodermal bands, but Hammarsten andRunnstrom categorically deny the existenceof these when they write: ". . . die vonKowalewsky beschriebenen Cblomsackenicht existieren . . ." (1925:277). These au-thors assume that Kowalewky mistook thenerve strands, the liver anlage, etc., for themesodermal bands. Raven, in his compre-hensive work on molluscan development(1958), follows Hammarsten and Runns-trom. According to these authors, a singlecoelomic cavity appears in chitons, in theanlage of the pericardial-nephridial com-plex. This cavity has, at the beginning, asingle pair of ducts, which will become thenephridia; the genital ducts appear onlylater, and primarily from ectodermalsources, not from the mesoderm whichmakes up the pericardial-nephridial com-plex. The coelomic cavity may become par-tially subdivided into pericardial and ne-phridial cavities, but it is the only cavity toappear. In the annelids, on the other hand,a series of coelomic cavities appear in the

mesodermal bands. Therefore, the mollus-can coelom is not entirely homologous withthe annelid coelom. It qualifies as a coelomsince it is surrounded by mesodermal tissue,but this is the extent of its homology withthe annelid coelom.

We turn now to the development of othersegmented organs. The shell plates firstappear in the early larva; they originate bythe simultaneous subdivision of the origi-nally undivided shell gland into six plates.Later, one more plate will be added anteri-orly and another posteriorly, and therebythe definitive number of eight will be estab-lished (Beklemishev, 1958a; Hunter andBrown, 1965). The gills appear weeks later,after thirty days of life; first the posteriorgills appear, and, as the animal grows, moregills are added anteriorly (Hunter andBrown, 1965). The nerve commissures orig-inate in a different manner again (Hammar-sten and Runnstrom, 1925; Raven, 1958).Isolated cells from the cerebral ganglia mi-grate posteriorly, dividing mitotically asthey go, and form thereby the lateral andpedal connectives and the ganglia there-upon. From the connectives, the commis-sures grow out presumably by this samemethod. Hammarsten and Runnstrom men-tion, however, that in other molluscs theganglia in the body and the foot arise fromlocal ectodermal thickenings, and the con-nection between them is established secon-darily (1925:311). They presume, how-ever, that the manner of growth observedin chitons is the primary, primitive method.We may conclude this section saying thatthe development of the various segmentedorgans is not coordinated in molluscs; thesegmented organs develop from differentrudiments, at different times and differentrates.

The ontogeny of the annelid segmenta-tion is completely different (Ivanov, 1928,1944; Beklemishev, 1958a; Dales, 1963). Wewill consider the presumably primitive modeof development, found in the oligochaetesand some polychaetes; but it must bepointed out that the other polychaetes alsofollow a basically similar course of develop-

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ment, the differences being inconsequentialfrom the point of view of the present argu-ment. In this primitive ontogeny of segmen-tation, the mesoderm of the early embryo,derived from 4d, becomes metamericallysubdivided into a small number of seg-ments, depending upon the number of theectodermal metameric organs. The subdi-vision of the mesoderm of the early larvais a simultaneous process. Not so the seg-mentation of the mesoderm of the metatro-chophore stage. This mesoderm also is de-rived from the cell 4d (in oligochaetes andsome polychaetes); it forms two bands, oneon each side of the body. Inside the meso-dermal bands, a series of cavities appear,in an anterior-to-posterior order. Each pairof cavities plus the surrounding tissues de-velop into a segment; thus, each segmentarises as a unit. The cavities become thecoelomic sacs, while their lining differen-tiates into the peritoneum, the musculatureof the gut and the body wall, the bloodvessels and the coelomoducts; from the ecto-derm of each segment, the epidermis, theganglia, the nerve strands and the chaetaedevelop. At the posterior end of the meso-dermal bands, cell division continues andnew coelomic cavities appear, and therebynew segments are continuously produced.Clearly, molluscs do not have this kind ofsegmentation.

The presumed phylogenetic differencesbetween the molluscan and annelid segmen-tation are as follows. The molluscan seg-mentation (pseudometamery) was prob-ably achieved in two stages. These can besharply distinguished for didactic purposesbut could have been concomitant in real-ity. In the first stage, there was an increasein the number of certain organs; this mayhave come about by actual multiplicationof an organ, or by the breaking up of onelarge organ into several smaller ones (thenephridia of Neopilina may exemplify this).The increase was not necessarily equal; cer-tain organs were multiplied to a greater ex-tent than others. In the second stage, therewas a regularization of the multiplied or-gans in number and position, so that they

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FIG. 3. Segmentation (eumetamery) of thepolychaete annelid, Nereis virens. Only the an-terior region is shown; the total number of seg-ments may reach 200. The dorsal body wall hasbeen partially removed; the ventral nervous systemis not shown. Notice that the number and arrange-ment of the various segmented organs are match-ing, and that there is a pair of coelomic sacs ineach segment. (From Brown, F. A. [ed.], 1950,Selected invertebrate types, with permission of thepublisher.) 1, palp; 2, prostomium; 3, eyespots; 4,peristomium; 5, parapodia; 6, coelomic sacs; 7, sep-tum, separating coelomic sacs; 8, stomach; 9, ven-tral blood vessel; 10, nephridium; 11, lateral bloodvessel; 12, esophageal coecum; 13, esophagus; 14,dorsal blood vessel; 15, pharynx; 16, cirri; 17,tentacle.

became arranged according to a unifiedplan. The second stage is now often incom-plete. The annelid segmentation (eumeta-mery), on the other hand, came about in

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one stage, by the production of identicalsets of organs in great numbers; thereby thenumber and arrangement of the varioussegmented organs immediately exhibit aunified, segmented pattern (Beklemishev,1958a).

The above presumptions are supportedby ontogenetic considerations. As ontogenyshows, the segmented organs of the annelidsdevelop in sets, each set differentiating outfrom an ectodermal and mesodermal blockof cells. The segmented organs of the mol-luscs, on the other hand, develop from dif-ferent rudiments, at different times anddifferent rates from one another. Further-more, in the various molluscan groups thatexhibit segmentation (monoplacophorans,polyplacophorans, some gastropods andcephalopods), different organs may be mul-tiplied, and the regularization may be onquite different levels. Thus, the mono-placophoran mollusc Neopilina galatheaehas six organs in multiple numbers (Fig. 1),which are quite harmoniously arranged;chitons have their shell plates, musculature,gills and commissures multiplied, but onlythe shell plates and the muscles are har-moniously arranged; some prosobranchsnails have but one structure, the commis-sures, multiplied; tetrabranch cephalopodshave their gills and atria multiplied, whichare in complete harmony. Had the mol-luscan segmentation evolved in the samemanner as the annelid segmentation, thischaotic pattern would make no sense.

Most of the differences between mollus-can and annelid segmentation were knownby the adherents of the annelid theory.Thus, Naef wrote (1926:41): "Man mussnun zugeben, dass ein solcher Prozess [seg-mentation of the mesoderm bands] bei Mol-lusken nicht in typisch unverkennbarerForm beobachtet ist. . . . Weiter ist zuzuge-ben, dass von einer Segmentierung desCb'loms in zahlreiche und regelmdssige Ab-schnitte und weiter von einem Colom vomfunktionellen Character dessen wohlausge-bildeter Anneliden bei Mollusken keineRede sein kann." But, in spite of these ad-missions, he equated the segmentation of

the molluscs and the annelids, and tried toderive the former from the latter. And,similarly, Lemche and Wingstrand wrote(1959b: 66): "We do not know whether thedorsal coelom is metamerically subdividedor not, but the metameric tendency is pres-ent in the gonads which may be regarded aspart of the coelomic system." And (p. 67):"The complete organization and the pres-ence of a heart in the last segment makes it[the last segment] very different from anarthropod or annelid telson, indicating thatthe metameres in 'Neopilina are not formedby a rhythmic activity of a terminal growthcentre. The more probable explanation isthat the mesoderm in the body region ofNeopilina is simultaneously subdivided inthe manner characteristic of the most an-terior segments in annelids and arthropods[i.e., those formed in the early larva]." But,nevertheless, they conclude (p. 66): "Themetamerism of Neopilina is so regular andis present in so many organ systems thatthere is no reason to regard it as differentfrom that of annelids and arthropods."Portman (1960) repeats this argument al-most word for word. Extending this argu-ment, one could maintain that there is noreason to regard the segmentation of thecestodes or the vertebrates as "different"from that of the annelids and arthropods,because all are very regular.

We may conclude this section saying thatthe molluscan segmentation differs from theannelid segmentation in anatomy, ontogenyand phylogeny; the molluscan segmentationis pseudometamery, the annelid eumeta-mery.

The second assumption of the annelidtheory is that molluscan segmentation de-veloped through reduction from a previousfuller segmentation. Generally this is in-terpreted as meaning that the molluscs de-veloped from annelids that lost their seg-mentation. This assumption is not onlyhypothetical (Hammarsten and Runnstrom,1925) but also erroneous. First of all, thesegmentation of molluscs is different in kindfrom that of the annelids, and thus irreduc-ible from the latter. A second considera-

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FIG. 4. Segmentation (pseudometamery) of thetriclad flatworm Procerodes lobata. Excretory sys-tem omitted. Notice that the number and arrange-ment of the commissures does not match that of theother segmented organs, and that there is no coelomat all. The segmentation of flatworms is of thesame kind as that of the molluscs. (From Lang, A.,1881, Mittheil. Zool. Stat. Neapel 3:187-251, withpermission of the publisher.) 1, brain; 2, commis-sure; 3, yolk gland; 4, proboscis; 5, circular nerveof proboscis; 6, mouth; 7, penis; 8, genital opening;9, albumen gland; 10, uterus; 11, genital atrium;

tion is as follows. An atypical or incom-plete segmentation such as that of the mol-luscs may be interpreted in two differentways: either as primarily incomplete or assecondarily reduced. The former is thesimpler interpretation, the latter the morecomplicated. On the principle of parsimonywe should accept the simpler interpretationas valid unless some evidence compels usto do otherwise. No such evidence has beenbrought forth by the annelid theory. There-fore, we should consider valid the simplerinterpretation, that the molluscan segmenta-tion is primary.

In Johansson's opinion however, this isnot so. He maintains that the segmentedcoelom of the presumed ancestors of mol-luscs was reduced when the latter became". . . adapted to hard bottoms in the surfregion and has developed a foot and ashell . . . . In this connection the segmentedcoelom, being no longer of importance forlocomotion, was reduced to form a singlecavity with one or two pairs of ducts" (1952:290). He considers the constancy in thenumber of the shell plates of chitons as theproof ". . . of a formerly complete true meta-mery as in the Arthropoda" (p. 287). Hefails to explain why the constant number ofthe shell plates has such significance. Hedid not explain either why he disregardedthe facts that, during ontogeny, the segmen-tation and the subsequent reduction of thecoelom can be followed step-by-step in thearthropods, not at all in the molluscs, orwhy life on the rock bottom in the surf zonehad to lead to the reduction of segmenta-tion. The truth is that coelomic segmenta-tion is fully compatible with life in suchhabitats, as shown by the fact that". . . poly-chaetes are extremely numerous in the rockyregions along the shore . . ." (McGinitieand McGinitie, 1949:194).

Contrary to Johansson's opinion, a com-parison of the locomotory mechanisms of

12, sperm duct; 13, testes; 14, salivary glands; 15,intestinal diverticulum; 16, intestine; 17, oviduct;18, nerve cord; 19, ovary; 20, eye.

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the molluscs and annelids makes it appearunlikely that the molluscs ever had coelomicsegmentation. The argument is as follows.The locomotion of the lower molluscs, suchas the polyplacophorans and primitivesnails, is rather primitive in kind; these ani-mals slide over the substrate on a sheet ofslime deposited by the mucous glands ofthe foot, by ciliary action or by locomotorywaves executed primarily by the longitud-inal muscles of the sole (Elves, 1961; Clark,1964). The annelids have a more efficientlocomotory mechanism, namely, a form ofperistaltic motion. These animals have twomuscle layers beneath the epidermis: anouter layer of circular muscles and an innerlongitudinal layer. By contracting the cir-cular muscles in a certain segment or seg-ments, pressure is exerted against the hy-draulic skeleton (coelomic fluid), and thisin turn stretches the relaxed longitudinalmuscles, leading to the elongation of thesegment or segments in question. Con-versely, the contraction of the longitudinalmuscles and the resulting stretching of thecircular muscles will cause the shorteningand thickening of the particular bodilyregion. By stretching out a certain region,anchoring it, and then pulling up the re-mainder of the body, the animal will beable to move. It should be emphasized thatperistaltic motion could be carried out witha single, unsegmented coelomic cavity, oreven without one (simply by using the tis-sues of the body as a hydraulic skeleton, asin nemertines); but the division of the coe-lomic cavity into many, at least partiallyisolated, compartments makes the systemmore controllable, maneuverable, and thusmore economical (Clark, 1964).

The loss of such an efficient system isunderstandable in arthropods, which ac-quired exoskeleton, some endoskeleton, skel-etal muscles, and, most of all, jointed ap-pendages, availing themselves of a loco-motory mechanism superior to peristalsis.But it is difficult to see why the primitivemolluscs should have abandoned peristalticlocomotion and regressed to the more prim-

itive ciliary-mucous-muscular locomotorymechanism that they still own today.

Actually, evolution of the molluscs pro-ceeded not toward but away from this prim-itive mechanism. Cephalopods developed avery advanced jet-propulsion system, andthe bivalves evolved a mechanism which,similarly to that of the annelids, utilizes thethe body fluids as hydraulic skeleton. Thelatter will be considered more closely. Thefoot in the bivalve molluscs contains a large,blood-filled cavity, the contents of which,when put under pressure by the contractionof the powerful adductor muscles, cause thedilation of the stretched-out foot; the latteris thereby anchored in the sand, and therest of the body can be pulled to it (True-man, 1960). Thus, bivalves developed away of digging, burrowing in the sand,which is superficially similar to that of theannelids. The differences are that, whereasthe cavity being utilized is coelomic in na-ture in the annelids, it is haemocoelic in themolluscs; the cavity is segmented in the an-nelids, unsegmented in the molluscs; andthe antagonistic muscles are located dif-ferently. The two animal groups thus haveevolved, in response to similar environmen-tal demands, superficially similar locomo-tory mechanisms; they represent a case ofconvergent evolution, rather than regres-sion.

According to Morton (1958:26, and inlitt., 1966) Garstang in prose and verse(1928, 1962) and conversation adumbratedthe idea that the molluscs developed fromthe annelids through neoteny; that is to say,molluscs are annelid larvae which becamesexually mature. According to Morton thiscan explain why the segmentation (eume-tamery) of the presumed annelid ancestorsis not observable in molluscs: because thepost-trochophoral stage, in which eumeta-mery ensues, is omitted from the life cycle.Garstang's article (1928) indeed impliesthat the molluscs developed from the larvaeof the annelids when he says (p. 88):". . . the Veliger [a post-trochoporal larvalstage, characteristic of the molluscs] . . . isa trochosphere [trochophore] transformed

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by the incorporation of Molluscan charac-ters . . . " (p. 88). It is also true, however,that this is far from proposing a theory onthe origin of molluscs. But whether Gar-stang elaborated upon it or not, I doubt thatneoteny could be the means by which themolluscs developed from the annelids. First,because molluscs have, in their life cycle, agenuine and sexually immature trochophorestage; one who assumes that the adult stagecorresponds to a sexually mature trocho-phore, has to explain the presence in the lifecycle of this "supernumerary" trochophore.Second, to claim neoteny, one ought to havea good agreement between the larva of acertain group and the adult of another, towhich the former supposedly gave rise. Insome more widely accepted cases of neo-teny this is actually the case; thus, the co-elenterates' planula larva is remarkably sim-ilar to the flatworm adult, and the diplopodlarva to the insect adult (Hyman, 1951;Hand, 1963; de Beer, 1946). In the annelidtrochophore and the molluscan adult, how-ever, the similarity could not be less. Thusit seems safe to say that molluscs are notneotenic annelids.

We may conclude this section saying thatevidence is lacking for the assumption thatthe segmentation of molluscs (pseudome-tamery) arose from the segmentation of theannelids (eumetamery) through reduction.The two kinds of segmentation are funda-mentally different, one cannot be reducedfrom the other. The explanations that thereduction and loss of segmentation in mol-luscs was due to functional reasons or neo-teny are groundless.

The origin of the molluscan-annelidstock.—The third topic to be discussed is:where did the common molluscan-annelidstock originate? One possible answer is,from the flatworms, or, more accurately,from the ancestors of flatworms (Hammer-sten and Runnstrom, 1925; Boettger, 1959).The evidence for this view comes from thesimilarity in cleavage between the flat-worms, molluscs and annelids, and from thefact that flatworms are on a lower level oforganization than are the other two groups.

The similarities in cleavage are widelyacknowledged (Nierstrasz, 1922; Naef, 1926;Hyman, 1951); typically, flatworms are saidto conform to the spiral cleavage pattern,found in molluscs and annelids. Deviationsfrom this pattern occur—e.g., having twoblastomeres instead of four—but these areregarded as secondary modifications (Ax,1963: Steinbock, 1963). Further similaritiesbetween the flatworms and the molluscs alsohave been noted; thus, the structure of thenervous system, the organzation of the mus-culature, body wall and the manner of loco-motion based thereupon, and the mode ofdigestion (primarily intracellular) are re-markably similar in the two groups (Nier-strasz, 1922; Graham, 1955).* As Hartman(1963) emphasized, however, similarities inlower levels of organization can easily oweto analogous solutions of the same problemsby unrelated groups. Thus, the manner oflocomotion, or the prevalence of intracellu-lar digestion are not unequivocal proofs ofrelationship. The structure of the nervoussystem may be a better indicator of the as-sumed relationships (figs. 1, 2, and 4).

The flatworms are said to be on a lowerlevel of organization than molluscs and an-nelids: they lack a coelom, anus, circulatorysystem, and have a very simple nervous sys-tem and primitive locomotory mechanisms.The molluscs, and particularly the annelids,are definitely on a higher level in most orall of these features. Some authors argue,though, that the simplicity of the flatwormsis secondary, the result of regression fromcoelomate animals (Ax, 1963; Remane,1963); but their theories are emphaticallyrejected by many (e.g., Beklemishev, 1963).Thus, we may conclude that evolution pro-ceeded from the flatworms toward the mol-luscs and annelids.

* The fact that the annelids do not share thesesimilarities does not contradict the flatworm originof the molluscan-annelid stock; the annelids, withthe "invention" of coelomic segmentation, haveradically departed from the flatworm-molluscantype of organzation, in structural and functionalaspects.

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The common ancestors of the molluscsand annelids may be reconstructed from thefeatures common to, or typical of, the prim-itive molluscs and annelids, as follows.They were small, probably pseudometa-meric, animals without a coelom (p. 156);with a ciliated body, a one-way alimentarycanal and a primarily intracellular digestion;probably with no circulatory system; withsexes separate, cleavage spiral, and trocho-phore larva; living in marine, benthic habi-tats.

A different origin for the molluscan-anne-lid stock was proposed by Beklemishev(1963). He began from a comparison ofthe planula stage of the coelenterates withthe adult stage of the flatworms (turbel-larians) and the protrochophore stage ofthe annelids (the latter he took as repre-sentatives of the trochophoric animals orTrochozoa, to which annelids, molluscs,etc., belong). The first two structures areso well known that they need not be de-scribed here. The protrochophore, accord-ing to Beklemishev (p. 240), ". . . is a pro-taxial larva with an aboral sense organ anda primary mouth opening on the oral pole. . . . [it] has a nervous system of the ortho-gon type, situated radially around the mainaxis of the body. . . . [In] all these respects. . . [it is] similar to the Turbellaria and,on purely promorphological grounds, to theplanula of the Coelenterata . . . . Whereasthe mouth in the Turbellaria is a small open-ing, . . . the primary mouth opening orblastopore of the protrochophore forms anarrow slit . . . . When the blastoporecloses, the definitive mouth and anus areformed at its ends and the physiologicallyventral side is formed along the wholeblastopore. The circumblastoporal nervousplexus gives rise to the ventral nervousstems of the Trochozoa . . . . The Turbel-laria do not possess anything homologousto the blastoporal side of the body or to thelongitudinal nervous stems of trochophoricanimals."

From the above findings, Beklemishevconcluded (loc. cit.) that the ". . . trocho-phoric animals, independently of the Tur-

bellaria, have developed from the larvae ofthe Coelenterata . . . . [which had] a slit-shaped mouth, an intestine with an epithe-lial lining, and a pair of aboral tentacles . . . .by means of 'progressive' neoteny."

I believe that Beklemishev has insuffi-cient ground to claim an independent originfor the flatworms and the Trochozoa. First,as he himself emphasized, the protrocho-phore is, in various respects, similar to theturbellarians (adult stage), not only differ-ent from them. Second, he had to create ahypothetical larval form to accommodatehis theories; this larva, a coelenterate withan intestine, seems quite unrealistic to me.Third, there is a huge difference betweena coelenterate larva with a slit-shapedmouth, and a trochozoan adult in which thegut was formed by the closure of the middleportion of the blastopore; it seems that Bek-lemishev too easily bridged this gap. Wehave to add that the cleavage pattern of theturbellarians is sufficiently similar to thatof the molluscs and annelids for most zool-ogists to consider them as having a commonorigin (Hyman, 1951), and that, were Bek-lemishev's theory true, we would have toaccept a dual origin for bilateral symmetryand cephalization, which is possible but notproven. On all these grounds it seems sim-pler to assume that the flatworms and themolluscs and annelids did not evolve inde-pendently, as Beklemishev suggested, buthad a common origin, and that the differ-ences Beklemishev emphasized arose afterthe trochozoan line branched off from theflatworms; possibly the changes in pro-morphology themselves played a role in theseparation of the two lines.

With this, we conclude the discussion ofthe origin of molluscs. Two other problemsseem pertinent to the subject. One is theorigin of coelomic segmentation (eumeta-mery), and the other that of the coelom.These are the two major "innovations" ac-quired about the time when the divergenceof the molluscan and annelid lines tookplace.

The origin of the coelom and coelomicsegmentation in molluscs and annelids.—

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Several theories have been put forth to ex-plain the origin of the coelom and coelomicsegmentation. Since they have been dis-cussed by recent authors (Hartman, 1963;Hyman, 1951; Clark, 1963, 1964; Remane,1963), I will consider them very briefly.The gonocoel theory suggests that the coe-lom arose from the expansion of the cavityof the gonads; the enterocoel theory saysthat it arose from the cavities of digestivediverticula, and the nephrocoel theory thatit came about by the expansion of the flamebulbs of protonephridia. The first twotheories assume that the organs giving riseto the coelom were serially arranged (pseu-dometameric), and thus their transforma-tion produced not one single coelomic cav-ity, but a series. In other words, these the-ories propose to solve the problem of theorigin of segmentation (eumetameric) to-gether with that of the coelom. This mayappear as an advantage, but in actuality itis one of the most serious objections to thesetheories. Because, having once acceptedthem, one also must assume that animalswith unsegmented coelom, such as molluscs,phoronids, ectoprocts, etc., all had to de-scend from ancestors with segmented coe-lom, which is not certain at all. Anotherserious objection to all of the above theoriesis that they consider the coelom homologousthroughout the animal kingdom, whichseems absurd in the case of independentphyletic lines such as the protostomes andthe deuterostomes. Further objections canbe found in the papers cited. The conclu-sion is that none of these theories is accept-able.

The coelom in the molluscs and annelidsseems to be a "new" structure, not only inthe sense of appearing for the first time,but also in being additional to any one ofthe already existing structures, not homol-ogous to them. This mode of origin of thecoelom was suggested by the schizocoeltheory, upheld by Hartman (1963). Ontoge-netic data support this contention, roughlyas follows: In molluscs and annelids thecoelom is formed in different manners; inmolluscs it develops inside the pericardial-

nephridial complex and in annelids insidethe mesoderm bands. Neither the gonocoel,the enterocoel or the nephrocoel theorieshave enough flexibility to explain these dif-ferences with ease. It is simpler to believethat both groups acquired the coelom inde-pendently and anew, and by their ownmethods (this also means that their com-mon ancestors did not have a coelom atall, p. 156).

Several theories have been proposed toexplain the origin of coelomic segmenta-tion (Hyman, 1951; Clark, 1964). Thegonocoel and enterocoel theories, as men-tioned above, combine the origin of seg-mentation with that of the coelom. Thetheory of cyclomerism, which says that seg-mentation arose by the bilateral, serial re-arrangement of originally radially situatedgastric pouches, is another form of the en-terocoel theory. Criticism of these theorieswas given previously. The fission or cormtheory, which says that segmented animalsarose from incomplete fission, i.e., fissionwithout subsequent separation of the pro-ducts of fission, has also been understand-ably rejected by Hyman. She finds that theorigin of segmentation can best be ex-plained by a combination of the theories ofpseudometamerism and locomotory mecha-nisms. According to the first, the ancestorsof the segmented animals were pseudometa-meric, with a series of gonads in the body(note similarity to the gonocoel theory).The swelling of the gonads during sexualmaturity made the bending of the body dif-ficult except at the sites between the go-nads, and this supposedly led to the serialconstriction—segmentation—of the body.The second theory also presupposes a longand pseudometameric body, but it empha-sizes the impact of locomotion on the mus-culature; it was, according to the theory,serpentine swimming motions that led tobreaking up of the musculature into seg-ments. I doubt that either of these explana-tions is valid. First, both are decisivelyLamarckian. Second, and mainly, becausesegmentation is primarily a developmental

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process, it needs a developmental explana-tion.

Such an explanation has come forth fromBerrill, concerning the origin of the segmen-tation of the chordate musculature. Hewrote (1955:171): "Segmentation . . . isprimarily a phenomenon of developmentand growth and requires analysis in termsof growth activity before we can considerhow it may have arisen during the course ofevolution." And (p. 173): "Segmenta-tion . . . is not something that can be grad-ually attained—it appeared suddenly as theresult of a critical modification of a devel-opmental process and could well have ap-peared as a single mutant type, as readilyas almost any other kind of innovation ormutation. The magnitude of the structural,functional, and evolutionary consequencesis somewhat beside the point. Admittedlyit would be a form of macro-evolution, butas the developmental outcome of just assmall an initial change as most others."Except for one reservation to be mentionedbelow, I agree with this theory and believethat the coelomic segmentation of the anne-lids has had a similar origin. This conclu-sion is derived from a comparison of themolluscan and annelid ontogenies as fol-lows.

In molluscs, the growth of the mesodermbands is short, differentiation sets in soon,and the mesoderm bands will give rise tovarious mesodermal organs. Rhythmicity ingrowth is not evident. This condition istaken as primitive, and the following one,found in the annelids, as advanced and de-rived. The latter arose presumably throughtwo changes from the former. First, thedifferentiation of the teloblasts, which bymitotic divisions produce the mesodermbands, is postponed; the teloblasts retaintheir capacity to divide, usually throughoutlife (Berrill, 1961:312). Second, the rate ofgrowth, or the rhythm of the differentiationof the products of growth, has changed fromnon-rhythmic to rhythmic. It seems thatboth kinds of changes can easily be ex-plained by mutations. It is neither neces-sary nor profitable to assume that the two

kinds of changes were achieved in a singlemutation, or that they occurred simultane-ously. I believe that these aspects of Ber-rill's theory do not apply to the origin ofannelid segmentation.

ACKNOWLEDGMENTS

I am most indebted to Dr. Carl W.Schaefer for his constant help in preparingthis article. I am also very grateful to Drs.William K. Emerson, William E. Fennel,Robert Robertson, and Ruth D. Turner, whohave read and criticized the manuscript oran earlier version of it, and to Mrs. StephaniSchaefer, who prepared the illustrations.

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Department of Biology, Brooklyn College,Brooklyn, N. Y. 11210.

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ON THE ORIGIN OF MOLLUSCS, THE COELOM, AND …...Apr 20, 2020 · mon ancestor toward both. Only differ-ences in the ontogeny could indicate direc-tion; a primitive condition in one

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