INVERTEBRATE ZOOLOGY IN THREE VOLUMES - VOLUME 1 - H.Y. Shcherbak - 1995

SUBKINGDOM MULTICELLULAR ANIMALS (METAZOA)

THE ORIGIN OF MULTICELLULARITY

The origin of Multicellular animals remains a subject of ongoing debate. As early as the 19th century, scientists debated various, sometimes quite fanciful, hypotheses regarding how multicellularity arose. Only a few of these theories have stood the test of time, primarily those proposing that Protozoans served as the ancestors of Multicellular Organisms. These hypotheses can be broadly divided into two groups.

The first group comprises theories suggesting that multicellular organisms evolved from protozoan colonies. In the 1870s, the prominent German biologist E. Haeckel formulated the gastraea hypothesis, viewing multicellularity as a development from colonial flagellates. According to this hypothesis, the ancestors of multicellular organisms were spherical flagellate colonies similar to those found today.

Haeckel based his theory on embryological data, attributing phylogenetic significance to the MAIN STAGES OF embryonic development. Just as a multicellular Organism in ontogeny develops from a single fertilized egg that undergoes Cleavage to form multicellular stages—the morula, blastula, and gastrula—so too in historical development: first, unicellular amoeboid organisms arose (cytaea), which then gave rise to colonies of several individuals (moraea), subsequently evolving into spherical single-layered colonies (blastaea) that possessed surface flagella and swam in the Water Column. Finally, the invagination of the blastaea wall inward led to The formation of a two-layered organism, the gastraea. The outer layer of its Cells bore flagella and performed a locomotory function, while the inner layer lined the primitive gut and served for Digestion. Thus, according to Haeckel's hypothesis, the primitive Mouth (blastopore) and closed primitive gut arose simultaneously. Because invagination was considered the sole method of Gastrulation known at the time—typical of higher animals like amphioxus, ascidians, and chaetognaths—Haeckel asserted that the phylogenetic formation of multicellular gastraeas must have occurred in the exact same manner. From this swimming two-layered organism, the gastraea, which settled onto the substrate on its aboral pole, began the evolution of Coelenterates, viewed by Haeckel as the most primitive multicellular animals from which all other Metazoa descended (Fig. 65, a–c).

For its time, the gastraea hypothesis was sufficiently well-founded. Haeckel proposed it even before I. I. Mechnikov discovered intracellular digestion. At the time, it was believed that food was digested exclusively within the gut cavity, which is why the primary endoderm was envisioned as the epithelium of a primary gut.

The gastraea hypothesis played a major role in The Development of evolutionary zoology. It was the first to substantiate the monophyletic origin of all multicellular animals. The hypothesis was supported by A number of zoologists, and with certain modifications, it is still accepted by many contemporary scientists, particularly in Western Europe, and features prominently in numerous foreign zoology textbooks.

However, even Haeckel's contemporaries pointed out flaws in the hypothesis. One of The most significant was the lack of an explanation for the physiological mechanisms driving the invagination of the blastaea wall during gastrulation. Furthermore, the gastraea hypothesis fails to account for the existence of parenchymula-type larvae in lower multicellular animals (such as Sponges and lower coelenterates), which lack an epithelialized endoderm.

One Modification of the gastraea hypothesis was the plakula hypothesis, proposed by the English scientist O. Bütschli (1884), who suggested that multicellular organisms originated from a two-layered, flat protozoan colony (the plakula). The layer of the plakula facing the substrate performed a nutritive function by absorbing food particles from the bottom. By arching upward on one side, this two-layered plakula transformed into a gastraea-like organism (Fig. 65, g–i).

Another popular modification among modern scientists is the bilaterogastraea hypothesis, put forward by the Swedish researcher T. Jägersten between 1955 and 1972. According to this hypothesis, the distant ancestor of multicellular animals was a spherical colony of plant-like flagellates resembling Volvox, which swam in the upper water layers and could feed both autotrophically and heterotrophically through the phagocytosis of small organic particles. Like modern Volvox, the colony possessed an anteroposterior polarity. Jägersten suggested that this blastaea transitioned to a benthic lifestyle by settling onto the bottom on one side, which flattened out.

This gave rise to a benthic, bilaterally symmetrical blastula-like animal—the bilateroblastaea (Fig. 65, j–l)—whose body could be divided along a single plane of Symmetry into two mirror-image halves. Because illumination at the bottom was insufficient for Photosynthesis, the bilateroblastaea fed primarily heterotrophically, phagocytosing food particles from the bottom using cells of its ventral epithelium. While transitioning to feeding on larger

prey, these animals would draw in the ventral layer to form a temporary cavity where ingested prey was trapped and digested. Gradually, this temporary cavity became a permanent gut cavity that opened externally through a slit-like mouth elongated along the anteroposterior axis. Thus, the bilaterogastraea—a gastrula-like, bilaterally symmetrical organism—originated.

According to Jägersten, Flatworms, which possess a gut cavity, descended from the bilaterogastraea. Later in the Evolution of the bilaterogastraea, three pairs of lateral invaginations appeared in the gut walls. All other animal phyla are thought to have descended from such a complex bilaterogastraea: coelenterates (primitive coral polyps) with three pairs of septa in the gastral cavity, as well as coelomate animals with three pairs of coeloms. Under this hypothesis, parenchymal and pseudocoelomate animals lost their coelom secondarily.

The plakula and bilaterogastraea hypotheses share the same shortcomings as the classical gastraea hypothesis: they assume that invagination is the primary type of gastrula formation, whereas it is extremely rare in lower multicellular animals. Moreover, the bilaterogastraea hypothesis relies on the premise that bilateral symmetry was the primary type of symmetry in multicellular animals, which contradicts embryological evidence showing that the ontogeny of lower multicellular animals lacks even traces of it. Paleontological studies indicate that Different types of symmetry could have arisen across various Metazoa simultaneously and independently.

Today, the most well-founded alternative to the gastraea hypothesis is the theory proposed by the Russian scientist I. I. Mechnikov, developed between 1877 and 1886. Studying the embryonic development of lower multicellular animals—sponges and coelenterates—Mechnikov established that the Formation of the two-layered stage occurs not through invagination, but primarily via immigration: individual Cells of the blastula wall crawl inward into its cavity. Mechnikov considered this primitive process of gastrula formation to be primary, viewing invagination as a secondary result of evolutionary compression and simplification of development.

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Fig. 65. Origin of multicellular animals: gastraea theory (a–c), plakula theory (g–i), bilaterogastraea theory (j–l), phagocytella theory (m): 2 — choanoflagellate colonies; 3 — early phagocytella (hypothetical ancestor of Prometazoa); 4 — primitive sponge; 5 — Placozoa; 6 — late phagocytella with mouth opening (hypothetical ancestor of Eumetazoa); 7 — gastraea (hypothetical ancestor of coelenterates); 8 — primitive turbellarian

According to Mechnikov's hypothesis, the ancestors of multicellular animals were spherical colonies of heterotrophic flagellates that swam in the water and fed by individual cells phagocytosing small particles. A prototype of such a colony can be seen in the pelagic spherical colonies of choanoflagellates (Sphaeroeca volvox). Individual cells, upon capturing a food particle, would lose their flagellum, transform into amoeboid cells, and sink deep into the colony, which was filled with a structureless gelatinous substance. Later, they could return to the surface. A similar phenomenon is observed in modern sponges, where flagellated choanocyte cells, once engorged with food, can transform into amoeboid cells and migrate into the parenchyma where digestion takes place, subsequently returning to their original position. Over time, cells differentiated into those primarily responsible for propelling the colony and those dedicated to feeding themselves and others. The colony ceased to be a hollow sphere; its interior became filled with an accumulation of phagocytes. Among modern animals, the closest relatives to this organizational type are collar flagellates (order Choanoflagellida) such as Proterospongia haeckeli, which form colonies featuring collar flagellates in the outer layer and amoeboid cells in the inner layer. Gradually, this temporary cellular differentiation became permanent, and a colony of unicellular organisms transformed into a multicellular animal comprising two Cell layers: an outer flagellated kinoblast and an inner amoeboid phagocytoblast. Nourishment in such an organism occurred as the flagellated cells of the kinoblast captured organic particles from the surrounding water and passed them on to the amoeboid cells of the phagocytoblast. Mechnikov named this hypothetical multicellular organism a phagocytella to emphasize The Role of phagocytosis in its origin (see Figs. 65, 66).

The Organization OF THE phagocytella closely resembles The Structure of sponge and hydroid larvae, known as parenchymulas. It is precisely during the formation of these larvae that cell migration occurs from the blastula surface into its cavity. According to Mechnikov, sponges and coelenterates descended from such phagocytella-like ancestors.

Mechnikov's hypothesis was supported by extensive embryological material and physiological research. Further validation and elaboration of the phagocytella hypothesis were carried out by prominent Russian zoologists A. A. Zakhvatkin (1949), V. N. Beklemishev (1944, 1964), A. V. Ivanov (1968), and the English researcher L. Hyman (1940, 1951). These scientists enriched the theory with new evidence derived from cytological, embryological, and protozoological studies, transforming it into a scientifically rigorous theory.

A. A. Zakhvatkin, who studied modern colonial protozoans, demonstrated the theoretical feasibility of a colony transforming into a cohesive multicellular organism. However, he believed that phagocytellas were not adult organisms, but rather free-swimming larvae that neither fed nor reproduced, serving solely for dispersal. In Zakhvatkin's view, the adult stages were sessile, bottom-attached colonial organisms resembling modern sponges and coelenterates. These primary multicellular animals possessed a complex life cycle similar to metagenesis (Hydrozoa), featuring an alternation of asexual polypoid generations and a sexual medusa generation.

A. V. Ivanov contributed significantly to the phagocytella theory. He not only provided new cytological and embryological evidence in its favor, but also detailed the structural and life-cycle characteristics expected of Metazoa ancestors. Expanding upon the phagocytella theory, Ivanov described the changes that could have occurred in phagocytella-like animals during their subsequent evolution, depending on whether they retained a swimming lifestyle or transitioned to a sessile or crawling existence. Some descendants of the phagocytella shifted from swimming to a sessile lifestyle (giving rise to sponges, which still lack a mouth, gut, Nervous system, and musculature), while others acquired The ability to crawl along the bottom, leading to the differentiation of their kinoblast into ventral and dorsal epithelia. These gave rise to Placozoa (Trichoplax), which, according to modern views, are relict animals that remain at the phagocytella level of organization. Among modern animals, Dicyemida and Orthonectida occupy a similar evolutionary grade.

Some phagocytella-like animals retained a swimming lifestyle, and in the course of evolution, they developed a mouth, a nervous system, and Muscles. From such advanced phagocytellas arose, on the one hand, primitive coelenterates that transformed into sessile polyps, and on the other hand, bottom-crawling ancestors of modern acoel turbellarians, which acquired bilateral symmetry while still lacking a gut—ultimately giving rise to flatworms (see Fig. 65).

Fig. 66. Diagram of the organization of the phagocytella:

1 — kinoblast; 2 — phagocytoblast; 3 — Germ Cells; 4 — phagocytosis; 5 — digestive vacuole

A second group of hypotheses concerning the origin of multicellular organisms comprises various modifications of the cellularization hypothesis. Its proponents proceed from the premise that a single-celled protozoan corresponds not to an individual cell of a multicellular organism, but rather to a whole multicellular organism itself. Cellularization is the subdivision into individual cells. The idea of cellularization was first put forward in the late 19th century by G. Néhring (1877) and Y. Delage (1896). In the 20th century, this concept was further developed by J. Hadži (1944, 1963) and other researchers. According to these scientists, multicellular organisms descended from multinucleated Ciliates. The transition from the unicellular to the multicellular state purportedly occurred within the bodies of ciliates simultaneously through the formation of cell boundaries around individual nuclei and their adjacent cytoplasmic regions—energids.

The complexly structured cell of ciliates was allegedly transformed into a fairly highly organized worm (turbellarian) or even a rotifer, whose Organs developed from its Organelles. The mouth and Pharynx supposedly formed from the cytostome and cytopharynx, the gut from the endoplasm, the anus from the cytoproct, the excretory organs from contractile vacuoles, and the Reproductive System from micronuclei. This concept has supporters among scientists in various countries. However, it is difficult to imagine how specialized, complexly organized ciliates—whose nuclear apparatus (nuclear dualism), differentiation of coverings (complex cortex), and Specifics of the sexual process (conjugation) and life cycle have nothing in common with the STRUCTURE AND Functions of other animals—could have given rise to multicellular animals. The greatest objections are raised by the assumption of cellularization proponents regarding the possibility of specialized organelles and cell regions transforming into multicellular Tissues and organs with analogous functions. Embryological data also contradict the hypothesis of cellularization. Furthermore, under this hypothesis, animals positioned lower than rotifers and turbellarians would have arisen through regressive evolution.

All of the aforementioned hypotheses are based on the premise that multicellular animals are monophyletic in origin, meaning they all arose in one way or another from a single ancestral form (the hypothetical gastrea, planula, bilaterogastrea, phagocytella, or Ciliate). However, in recent times, an increasing amount of

evidence has emerged suggesting that sponges have an origin independent of other Metazoa. Comparative electron microscopic studies of the structure of sponge choanocytes and choanoflagellates have revealed an almost complete identity between them, on the one hand, and significant differences from the collar flagellate cells of other multicellular organisms, on the other. Such cells are found, for instance, in the epithelium of hemichordates, certain Echinoderms, and others. This fact, along with the distinct uniqueness of sponges (the absence of a mouth, gut, nerves, muscles, and germ layers), indicates that sponges originated from ancient choanoflagellates or common ancestors shared with them, whereas all other Metazoa descended from some now-extinct heterotrophic colonial flagellates. If one adheres to this viewpoint, it must be accepted that the ancestors of sponges and those of other Metazoa were distinct animals, though their structural organization could have been similar. Indeed, the parenchymal forms of sponges and Cnidarians are identical, even if they may have had a different evolutionary origin.