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On the Origin of Molluscs, the Coelom, and Coelomic Segmentation

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On the Origin of Molluscs, the Coelom, and Coelomic Segmentation ON THE ORIGIN OF MOLLUSCS, THE COELOM, AND COELOMIC SEGMENTATION JOSEPH VAGVOLGYI Abstract Molluscs had a common origin with the annelids, as shown by remarkable ontogenetic similarities. Their common ancestors were non-segmented (non-eumetameric), acoelomate Downloaded from https://academic.oup.com/sysbio/article-abstract/16/2/153/1647154 by guest on 20 April 2020 animals. Molluscs developed from the common stock through incorporation of the distin- guishing molluscan characters such as the shell, mantle, mantle cavity, radula and ctenidium and annelids by the adoption of coelomic segmentation and of changes accompanying it. The assertion that molluscs hand ancestors with coelomic segmentation is contradicted by ontogenetic and anatomical facts as well as by theoretical considerations. The common moHuscan-annelid stock most likely originated from ancestral flatworms; this is indicated by 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 was acquired independently in the two phyla. Coelomic segmentation also is a phylogenetically new acquisition of the annelids; it came about through developmental changes affecting the growth of the mesoderm bands. These views are the corollaries of ontogenetic considerations. A widely held hypothesis concerning the crawling mode of locomotion. And finally, origin of molluscs is the so-called annelid Lemche (1957) reported the discovery of a theory. According to Hyman (1951:4), the "living fossil," a primitive, segmented mol- "annelid theory" states that ". annelids, lusc, Neopilina galatheae Lemche, 1957. arthropods, and chordates are closely re- Soon two more species of Neopilina were lated and [that] lower bilateral groups may found, N. ewingi Clarke and Menzies, 1959, have arisen from annelids by degeneration." and N. veleronis Menzies and Layton, 1963. In the present paper the term is restricted, These discoveries were accepted by many referring to the theory that annelids gave as evidence for the segmented origin of rise to molluscs. Early proponents of this molluscs (Lemche, 1959a, 1959b, I960; theory (Pelseneer, 1899; Heider, 1914; Lemche and Wingstrand, 1959b; Portman, Soderstrom, 1925; Naef, 1926) believed that I960; Fretter and Graham, 1962). Lemche the serial repetition of certain organs in went so far as to postulate that molluscs are some molluscs represented vestigial segmen- more closely related to the arthropods than tation, and claimed on this basis that mol- to the annelids, and that the latter arose luscs descended from the segmented worms, independently of the former two groups. annelids. They also believed that the far- Fretter and Graham supported this argu- reaching similarities in cleavage and early ment by claiming that the coelom is primar- development were further indications of this ily small in the arthropods as well as in the relationship. More recent investigators molluscs. added other viewpoints to these arguments. Opponents of the annelid theory have Thus, Garstang (1928) theorized that mol- repeatedly pointed out the weaknesses of luscs evolved from the trochophore larvae it. Thus, Nierstrasz (1922), Hammersten of the annelids by neoteny. Johansson and Runnstrom (1925), Ivanov (1928, 1944), (1952) aimed at giving a functional expla- Beklemishev (1958a, 1958b), Boettger nation to the annelid theory, when he pro- (1959), Steinbbck (1962) and Hunter and posed that the molluscs had lost the segmen- Brown (1965) argued that molluscs cannot tation of their annelid ancestors in turning be considered as annelids with reduced to living on hard, rocky surfaces of the segmentation, because of fundamental ana- intertidal zone, and assuming a creeping, tomical and developmental differences in 153 154 SYSTEMATIC ZOOLOGY segmentation. Odhner (1961) pointed out The claims of Lang, Nierstrasz and Gra- that molluscs attained segmentation inde- ham that molluscs originated independently pendently of the annelids. Beklemishev of the annelids overemphasize the similari- (1958b), Boettger (1959), Steinbock (1962) ties between the molluscs and flatworms and Hunter and Brown (1965) have argued and underemphasize those between the mol- convincingly that Neopilina cannot be con- luscs and annelids. Also, it is not certain sidered proof for the annelid origin of mol- whether some of the molluscan-flatworm Downloaded from https://academic.oup.com/sysbio/article-abstract/16/2/153/1647154 by guest on 20 April 2020 luscs, because of differences in the segmen- similarities are due to close relationships or tations, because Neopilina is not at the root to parallel evolution. For these reasons, I of the molluscan phylogeny, and for various reject these claims. It also seems doubtful other reasons. Yochelson (1963) reached a that the construction by Beklemishev of similar conclusion from paleontological hypothetical larval forms satisfying superfi- studies; he maintained that the monoplaco- cial morphological requirements is of any phoran molluscs (to which Neopilina be- help. The ideas expressed by Hammarsten longs ) do not constitute the basic molluscan and Runnstrom and Boettger (that the an- stock; rather, they are a primitive group of cestors of aschelminths came from ances- the more advanced molluscs. The results of tors of the flatworms), on the other hand, Schmidt's microscopic and crystallographic account both for the molluscan-flatworm studies (1959) on the shell of Neopilina and the molluscan-annelid similarities, and are neatly consistent with this conclusion. avoid making unwarranted and unnecessary Further objections, not expounded in the assumptions. Therefore, they appear to rep- literature, also can be brought up against resent "the truth," according to our present the annelid theory. The theory does not knowledge. explain why we must consider molluscan Thus, it seems that the problem of the segmentation secondary and reduced, or origin of molluscs already has been solved. why we must accept the ontogenetical sim- Many zoologists, however, perhaps even the ilarities between molluscs and annelids as a majority, are either unaware of, or unwilling proof of the annelid theory, when alterna- to accept, this answer. The present paper tive assumptions also are possible. Weak- has been written with the purpose of sum- nesses in Garstang's and Johansson's theory ming up the arguments, elaborating upon also are found, as I will show in a later sec- those that were not explicit or expounded in tion. due detail, adding some new arguments, To supplant the annelid theory, Lang and thereby presenting a unified and hope- (1896), Nierstrasz (1922), and Graham fully convincing argument for the case. (1955) proposed that molluscs evolved from flatworms or ancestors to the flatworms, DISCUSSION completely independently of the annelids. Hammarsten and Runnstrom (1925), Boet- It seems profitable to arrange the argu- tger (1959 and Beklemishev (1963, on the ment around the three main points of the other hand, argued that molluscs and anne- theory followed here. These are: 1) mol- lids evolved together but separated from luscs and annelids had evolved together; each other before the annelids acquired 2) the molluscs separated from the annelids coelomic segmentations. Whereas, however, before they acquired the distinguishing mol- Hammarsten and Runnstrom believed that luscan criteria such as shell, mantle, mantle the common molluscan-annelid stock origi- cavity, radula and ctenidium (Yonge, 1960; nated from the ancestors of the flatworms, Morton and Yonge, 1964), and the annelids Boettger thought that the common stock acquired coelomic segmentation; 3) the evolved from a group near the root of the most likely ancestors of the common mol- aschelminths, and Beklemishev thought luscan-annelid stock were the forms ances- it evolved from "larval" coelenterates. tral to the present-day flatworms. ON THE ORIGIN OF MOLLUSCS 155 Downloaded from https://academic.oup.com/sysbio/article-abstract/16/2/153/1647154 by guest on 20 April 2020 10 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 only partial 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 of the 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- and the annelids have spiral cleavage; the nelids.—This contention is based upon the fate of certain cells is, with some exception, similarities between the molluscs and anne- the same in the two groups; mesoderm lids in cleavage, embryonic development, bands arise from cell 4d in both groups; and early larval stage. Both the molluscs and the early larval stage, the trochophore, 156 SYSTEMATIC ZOOLOGY is nearly identical. These similarities are but they do not support the claim that mol- accepted as indications of a genuine and luscs developed from annelids. close relationship by practically all zoolo- The separation of molluscs and anne- gists (Hyman, 1951; Barnes, 1963). A con- lids.—The separation of molluscs and anne- sensus, admittedly, does not
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