Review Article |
Corresponding author: Ilya A. Gavrilov-Zimin ( coccids@gmail.com ) Academic editor: Valentina G. Kuznetsova
© 2023 Ilya A. Gavrilov-Zimin.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Gavrilov-Zimin IA (2023) Ancient reproductive modes and criteria of multicellularity. Comparative Cytogenetics 17: 195-238. https://doi.org/10.3897/compcytogen.17.109671
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It is demonstrated that the initial method of fertilization in animals (Metazoa), embryophyte plants (Embryophyta), most groups of multicellular oogamous algae, oogamous and pseudoogamous multicellular fungi was internal fertilization (in the broad meaning) in/on the body of a maternal organism. Accordingly, during the bisexual process, the initial method of formation of a daughter multicellular organism in animals was viviparity, and in embryophyte plants and most groups of oogamous multicellular algae – the germination of a zygote in/on the body of maternal organism.
The reproductive criteria of multicellularity are proposed and discussed. In this regard, the multicellularity is considered to subdivide terminologically into three variants: 1) protonemal, the most simple, characteristic of multicellular prokaryotes, most groups of multicellular algae and gametophytes of some higher plants; 2) siphonoseptal, found among multicellular fungi, some groups of green and yellow-green algae; 3) embryogenic, most complicated, known in all animals (Metazoa), all sporophytes and some gametophytes of higher plants (Embryophyta), charophyte green algae Charophyceae s.s., oogamous species of green and brown algae, some genera of red algae.
In addition to the well-known division of reproduction methods into sexual and asexual, it is proposed to divide the reproduction of multicellular organisms into monocytic (the emergence of a new organism from one cell sexually or asexually) and polycytic (fragmentation, longitudinal / transverse division or budding based on many cells of the body of the mother organism), since these two ways have different evolutionary and ontogenetic origins.
Evolution, gametogenesis, multicellularity, oogamete, polyembryony, sexual and asexual reproduction, spore, viviparity
The origin of multicellularity in the evolution of living organisms remains one of the most important discussion topics in evolutionary biology over the past one and a half centuries. The main hypotheses explaining the sequential phylogenetic transformation of colonial protists into the first truly multicellular organisms are well known and discussed many times in specialized scientific and educational literature (see, for example,
The traditional, well-known division of reproduction modes into two large groups, sexual and asexual, has an almost universal meaning, since it is to some extent applicable to all living systems, with the exception of only prokaryotic organisms and viruses. To avoid confusion, it should be noted right away that asexual and sexual methods of reproduction are not always accompanied by the increasing of a population. For example, in higher plants (Embryophyta), as well as in most groups of algae and fungi, producing of numerous descendants occurs primarily with the asexual formation of spores, while as a result of the sexual process, only one daughter organism (usually a sporophyte) often develops on one maternal organism (usually a gametophyte), that is, there is no increase in the number of individuals. The sexual process in prokaryotic organisms and in some protists is not at all directly connected with reproduction.
Significant terminological confusion also occurs when discussing variants of parthenogenesis, i.e. development of an organism from a gamete without its fusion with another gamete. In recent decades, especially in the English-language literature (see, for example,
In addition, when considering methods of reproduction of multicellular organisms, it is important not to lose sight of the following aspect. A daughter multicellular organism can arise from a single cell of the mother’s body (spore, zygote, haploid gamete, parthenogenetic egg with restored diploidy, or simply a separate somatic cell that has retained totipotency [that is, the ability to produce various types of differentiated cells]) or simultaneously from many mother cells (with various variants of budding, fragmentation, simple division of the body into two or many parts). According to this criterion, the reproduction of multicellular organisms can be divided into monocytic and polycytic; the second term only partly overlaps with the concept of “vegetative reproduction”, since in the botanical literature, simple mitotic division of unicellular algae is also called vegetative (see, for example,
Numerous taxonomic names of organisms are used in the analysis below. It is important for the reader who does not have a serious personal experience of taxonomic work to take into account that there is no single universal system of living nature and a universal method of taxonomic constructions. For any group of organisms, the scientific literature presents competing views of various specialists and scientific schools on the phylogeny of the corresponding group and its “internal” classification. At the same time, phylogenetic schemes and taxonomic systems published later in date are by no means necessarily more correct or more reasoned than those published earlier. In this article, I do not have the opportunity to discuss any particular aspects of phylogenesis, the ideological basis of numerous classification schemes, contradictions between evolutionary and cladistic systematics, the suitability/unsuitability of various computer-molecular approaches, etc. Solely for practical convenience, I use the names of algal taxa appearing in the AlgaeBase database (https://www.algaebase.org/), since this database compiles all nominal taxa of algae (as well as cyanobacteria) at the same time and reveals the corresponding nomenclature of names. The use of AlgaeBase does not mean my automatic agreement with all classification constructions implemented in this database. The same applies to the use of the names of higher taxa of heterotrophic protists and invertebrate animals, the classifications of which differ quite significantly in the works of different authors published in recent decades. In general, I follow the approach used in one of the most famous modern manuals on invertebrate zoology, a two-volume edition edited by Westheide and Rieger (
For further discussions, it is necessary to clearly define the range of organisms that can be considered multicellular. Unfortunately, the border between the coloniality of unicellular protists and simple forms of multicellularity is understood in the scientific literature very vaguely. With an expanded approach to this issue (for example,
In addition, there is no clear unequivocal separation of different types of multicellularity. Usually, one speaks only of simple and complex multicellularity (
In a broad interpretation, “clonal” and “aggregative” multicellularity are also distinguished (
I consider it logical to proceed from the fact that a unitary multicellular organism, unlike a colonial one, obligatorily develops as a multicellular organism and reproduces itself only after it reaches the multicellular «vegetative» stage of ontogenesis. That is, the life cycle of a unitary multicellular organism is as follows (Fig.
Generalized scheme of the life cycle of a multicellular organism (protonemal multicellularity).
A similar situation occurs in the case of the formation of various specialized colonies (coenobia) of unicellular algae (for example, Coelastrum Nägeli, 1849, Scenedesmus Meyen, 1829, Sphaerocystis Chodat, 1897 and many others, especially among green and diatom algae), which are the result of secondary accretion or immersion in a common mucosal capsule of initially independent, self-feeding and reproducing cells. Inside each cell of the coenobium, small zoospores are again formed, which coalesce into a tiny daughter coenobium inside the mother cell, and then are released due to the rupture of the wall of this cell (
I also do not consider as multicellular organisms various multinucleated coenocytes (= somatella, cytoids, polycystids, etc.), known in some complexly organized ciliates, opalines, sporozoans, dinoflagellates, foraminifera and other protists. All these organisms do not meet the first reproductive criterion of multicellularity formulated above. The bodies of some “colonial” ciliates, for example, from the genus Zoothamnium Bory de St. Vincent, 1824, formed as a result of incomplete monocytic budding. Nevertheless, the resulting “colony” remains a de facto unicellular formation, within which there are no partitions, and all parts of which are connected by cytoplasmic strands caused by the so-called spasmonemes (
Some difficulty can be caused by the application of the first reproductive criterion in relation to various cases of asexual reproduction at the initial stages of development of a multicellular organism. So, for example, in some cnidarians (Cnidaria) under experimental conditions, individual blastomeres retain the ability to give rise to independent embryos (
Regular polyembryony, which occurs in a number of groups of highly developed animals and plants, is all the more not an example of unicellular reproduction, since it is realized on a multicellular basis (with the exception of random developmental anomalies in some individuals). First, a multicellular body of the embryo begins to form from a zygote or a parthenogenetic egg, and only then it is divided into several or many daughter embryos (
A certain difficulty is also caused by the understanding of multicellularity in secondarily simplified parasitic animals – orthonectids (Orthonectida), in which one of the stages of the life cycle is a multinuclear “plasmodium”, capable of reproducing by monocyte budding. However, inside such a plasmodium, in addition to trophic nuclei, there are also generative nuclei with isolated sections of the cytoplasm, which are agametes (
The second reproductive criterion of multicellularity determines exactly how a multicellular body reproduces itself by the monocyte method of forming a daughter organism and allows us to divide all known ways of implementing obligate multicellularity into three fundamentally different variants.
The simplest and most archaic variant is protonemal multicellularity, in which a spore or zygote divides monotomically (by mitosis or simple cytokinesis), forming a single filament, a protonema (Fig.
Monotomic division implies the obligatory growth of daughter cells after their division. As a result, a multicellular structure is formed from cells of approximately the same size, quite similar to the original cell or even exceeding its size. Such a single-row thread can then grow, branch many times, intertwine, forming a multilayer body (thallus). Protonemic multicellular organisms include the following groups:
The second variant is siphonoseptal multicellularity (Fig.
Unfortunately, the ultrastructural and biochemical mechanisms of septa formation in multicellular algae, fungi, and, especially, prokaryotes, remain insufficiently studied, and the available knowledge is limited to single model objects (
It should be noted that the structure of the septate bodies of fungi and algae is not similar to the complicated construction of some protists (Protista), for example, gregarine (Gregarinea). In the latter, a single cell is sometimes divided into communicating parts by a “tangle of thin fibrils” (
Siphonoseptal multicellularity is characteristic of the following groups:
Finally, the third and most complicated variant is embryogenic multicellularity (Fig.
Generalized scheme of the life cycle and initial stages of development in embryogenic multicellular organisms.
The embryogenic variant of multicellularity is observed in the following organisms.
It is interesting that in a number of works on various genera of brown algae, for example, in the articles by
Embryoid gametophytes of higher plants. a–c Reboulia hemisphaerica (Linnaeus, 1753) (Marchantiophyta) d, e Frullania muscicola Stephani, 1894 (Marchantiophyta) f–h Selaginella spp. (Lycopodiophyta); i–k Isoetes sp. (Lycopodiophyta) a–e after
From the above list of organisms, it can be seen that embryogenic multicellularity did not arise on the basis of prokaryotic cells. This fact, of course, is not accidental and is probably due to the fact that prokaryotic cells are not capable of providing effective intercellular transport of substances and, accordingly, of the formation of differentiated tissues. As a result, prokaryotes do not have examples of the embryonic development required for initial cell differentiation. Moreover, due to the absence of the endoplasmic reticulum, the transport of substances within prokaryotic cells is limited by the possibilities of diffusion, which imposes significant restrictions on cell size. Large sizes (sometimes up to 0.75 mm in diameter) of cells in some prokaryotes, for example, in the bacterium Triomargarita namibiensis
Monocytic bisexual reproduction in protonemal multicellular organisms can proceed according to the type of isogamy, heterogamy, oogamy, or analogs of oogamy, whereas asexual monocytic reproduction can proceed according to the type of zoosporia or aplanosporia. Evolutionary models for the emergence of gamete diversity (anisogamy) from the initial isogamous sexual process have been repeatedly proposed in the specialized literature (Parker at al. 1972;
The various evolutionary transformations within the broadly understood oogamy deserve more detailed consideration, since, as will be shown below, oogamy is a necessary prerequisite for the transition to complex forms of multicellularity. The oogamous sexual process (or its analogues) in protonemal multicellularity is still carried out in an extremely achaic way, since in this case the oogamete (with rare exceptions) does not accumulate nutrients for further development, but remains comparable in volume to usual somatic cells or even turns out to be significantly smaller than the latter. As a result of this, the further development of the parthenogenetic or fertilized oogamete (zygote) inevitably occurs through monotomic germination, i.e. successive division and growth of daughter cells forming a filamentous structure (protonema).
It should be noted that examples of archaic oogamy are already found in unicellular and unicellular-colonial organisms. Thus, some genera of colonial diatoms (Diatomophyceae), for example, the so-called centric diatoms (orders Thalassiosirales, Coscinodiscales, Melosirales, Chaetocerotales) and pennate diatoms of the genus Rhabdonema Kützing, 1844, demonstrate oogamy, in which germ cells are smaller than somatic ones (
Formation of syzygy and copulation in the gregarine Stylocephalus longicollis (Stein, 1848).
In the related group of coccidia (Coccidea), the oogamete is formed directly from the haploid parent cell (merozoite) without division of the latter, and biflagellated (rarely non-flagellated) male gametes arise as a result of syntomic division of the merozoite. The possibility of fusion of gametes in this case is achieved by the fact that the parent cells are in close proximity to each other inside the body of the host organism. Meiosis in the life cycle of coccidia, as in gregarines, occurs in the “oocyst” formed from the zygote (
Some highly developed ciliates that form “colonies” by incomplete budding (
Analogy of the oogamous sexual process in the ciliate Zoothamnium arbuscula Ehrenberg, 1839 a colony with macrozooids (ma) b conjugation (mac – macroconjugant, mic – microconjugant, mi – microzooid). After
Relatively few examples of archaic oogamy (without an increase in the size of the gamete) are known among protonemal multicellular organisms. For example, such oogamy has been well studied in green algae of the genus Prasiola Meneghini, 1838 (Trebouxiophyceae: Prasiolales). In the upper part of their multicellular diploid thallus, meiotic divisions occur and biflagellated spermatozoa and non-flagellated oogametes (ova) are formed. Female gametes are about twice as large as male, but smaller than the original diploid cells of thallus. They are released due to the destruction (“dissolution”) of the lower cell walls of thallus and end up in a bubble-like space bounded by the persistent outer common shell of the thallus (“persisting bladder-like coating lamella”). At the same time, hundreds or even thousands of heterosexual gametes are released into this space and fertilization occurs. A protonema grows from the zygote, and a new diploid thallus grows from it (
Even rarer in protonemal multicellular organisms, accumulative oogamy occurs, in which an increase in the volume of the egg takes place in comparison with the cells of the “vegetative” body that preceded it (Fig.
Accumulative oogamy in protonemal multicellularity in Oedogonium stellatum Wittrock ex Hirn, 1900 (after
A peculiar analogy of archaic oogamy among protonemal organisms occurs in red algae (Rhodophyta) (Fig.
Scheme of development of the “carposporophyte generation” of floridian red algae (Rhodophyta: Florideophyceae). After
The increase in the number of individuals in protonema-multicellular organisms occurs mainly during the production of spores. In fact, the spore in archaic organisms is quite homologous to the unfertilized gamete, which was convincingly shown, for example, in the fundamental work of
It is well known that, similar to the evolutionary transition from small mobile gametes to large immobile gametes, in various groups of organisms there is a transition from small zoospores to immobile aplanospores, which in many cases do not exceed ordinary somatic cells in volume, but in a number of organisms they accumulate nutrients and increase significantly in size. At the same time, the production of a large number of small spores is typical for most protonemal multicellular organisms. Particularly impressive examples are demonstrated by some genera of red algae: each sporophyte produces about 12 million carpospores, and one tetrasporophyte produces 100 million tetraspores (
Homologous to the process of sporulation can be considered monocytic budding of protonemal multicellular organisms. Thus, in one of the isogamous genera of brown algae, Sphacelaria Lyngbye, 1818, vegetative reproduction is carried out by multicellular structures formed at the ends of branches (
The sexual process is predominantly isogamous or heterogamous. However, in some groups, archaic oogamy occurs (without an increase in the size of the eggs in comparison with the original cells of the mother’s body), analogues of oogamy, or somatogamy (fusion of two somatic cells).
Thus, in Chytridiomycota of the order Monoblepharidales, the multinuclear mycelium usually does not contain septa, but zoosporangia, oogonia, and antheridia are separated from the body by septae (
Asexual and sexual reproduction in siphonoseptal multicellularity on the example of Monoblepharis spp. a–c asexual reproduction by zoospores d branching of zoosporangia e–l successive stages of the sexual process m section of the siphon-septal body with genital organs and zygotes (after
In some genera of yellow-green algae (Xanthophyceae or Tribophyceae) from the order Vaucheriales, multinuclear branching siphons are usually devoid of septae, but sporangia and gametangia are separated by septae. In Vaucheria de Candolle, 1801 and Pseudodichotomosiphon Yamada, 1934, a single small egg cell is formed in the spherical oogonium, while numerous biflagellated spermatozoa are formed in the antheridia. The sperm enters the oogonium through a pore in the membrane. The diploid zygote, after a dormant period, germinates into a new thallus (
In green algae of the genus Sphaeroplea Agardh, 1824 (Sphaeropleales), multinuclear siphonal bodies are separated by centripetally formed septae, but no special organs of sexual reproduction are formed. Small eggs and spermatozoa are formed in any of the segments of the body (
An analogue of archaic oogamy in siphonoseptal multicellular organisms can be considered sexual reproduction of multicellular ascomycetes (Ascomycota), basidiomycetes (Basidiomycota), oomycetes (Oomycota) and some others. True oogamy is completely absent in these organisms. Instead, there are different variants of fusion of hyphae segments that function as unicellular gametangia, as well as the formation of male gametes (spermatia) in the absence of female ones, or vice versa (
Asexual monocytic reproduction of siphonoseptal multicellular organisms is usually carried out by small unicellular zoospores or immobile, including multicellular, aplanospores (ascospores, basidiospores, etc.). The formation of unicellular or multicellular conidia in many groups of fungi is considered a special variant of spore formation (
Monocytic reproduction of embryogenic organisms in all known cases is associated either with accumulative oogamy (during the sexual process or parthenogenesis), or with accumulative aplanosporia (during asexual reproduction). In both cases, a new organism begins to develop from one immobile cell, which is larger than the usual somatic cells of the organism. The division of such a cell occurs according to the type of palintomy, i.e. rapidly recurring karyokinesis and cytokinesis, without a period of growth of daughter cells, or by the type of syntomy, i.e. rapidly recurring karyokinesis followed by simultaneous division of all cytoplasm of the mother cell into numerous compartments (Fig.
Embryo — the initial stage of development of embryogenic multicellular organisms, from the first division of the zygote (or parthenogenetic egg) to the beginning of independent life (exit from the shell of the zygote (egg) or separation from the mother’s organism).
Embryoid — an analogue (in some cases also a homologue) of an embryo, the initial stage of development of embryogenic multicellular organisms during asexual monocytic reproduction, from the first divisions of the original cell (spore or spore-like cell) to the beginning of independent life.
Probably the most simple embryogenesis is saved in Charophyceae algae. Their zygote (“oospore”), while still inside its shell, undergoes syntomic divisions of meiosis, resulting in the formation of a four-nuclear cell. One of these haploid nuclei is separated by a septum, undergoes another palintomic division, and gives rise to root and stem cells. The remaining trinuclear cell performs the function of storing nutrients (
Oogamy and embryogenesis are most complex in animals (Metazoa). In them, unlike plant and fungal organisms, the process of female meiosis is in the nature of unequal division, resulting in the formation of one egg and several reductional (polar) bodies. The evolutionary meaning of this phenomenon is not clear, since it is not known in other embryogenic multicellular organisms. It is worth mentioning that in some animals, for reasons that are not entirely clear, male meiosis is also unequal (
In addition, a special variant of embryogenesis “a cell within a cell”, known for a number of secondarily simplified parasitic animals (myxosoporidia, cnidarians of the genus Polypodium Ussov, 1885, orthonectids, dicyemids), as well as for angiosperms (Magnoliopsida) looks unclear in terms of evolutionary meaning and causes of occurrence.
For a century and a half, myxosporea (Mixozoa) were considered by most zoologists as one of the groups of protists (Pugachev, Podlipaev 2007: 1045–1080), although the hypothesis of their belonging to multicellular animals (Metazoa) was first put forward as early as 1899 (
In an even more aberrant, but still insufficiently studied way, the reproductive system functions in another parasitic representative of the coelenterates, Polypodium hydriforme Ussov, 1885 (Cnidaria: Polypodiozoa). The sexual generation of this species is a free-swimming, dioecious freshwater jellyfish. Their female gonads are appeared during ontogenesis, but do not function. The male gonads produce non-flagellate, binuclear gametes that inexplicably enter the oocytes of the host organism (fish). Further, these gametes, without fertilization, proceed to unequal cleavage, as a result of which a kind of morula is formed, which is placed inside a large polyploid cell called a trophamnion. Embryogenesis lasts several years, in accordance with the development of the host’s oocytes, and ends with the formation of a larva that looks like an inside-out planula. Numerous “buds” are formed on the body of this larva and the whole organism takes the form of a stolon. Shortly before host spawning, the stolon inside the oocyte turns inside out and acquires the normal position of the cell layers for the coelenterates. The release of stolons from the eggs of the host occurs in the reproductive ducts of the fish. After entering the water, the polypodium stolon undergoes fragmentation with the formation of daughter medusoid forms (
The body of dicyemides (Dicyemida) is arranged in an extremely simplified way, consists of only 8–40 cells and does not have any tissues, organs and intercellular cavities. The total number of cells is determined and characteristic of each species. The body of adult worm-like stages (nematogen and rhombogen) is formed by one layer of integumentary (somatic) ciliated cells and one (rarely several) large internal axial (generative) cell (Fig.
The structure of the nematogen and the cycle of parthenogenetic reproduction of Dicyemida.
In orthonectids (Orthonectida), the main stage of the life cycle (Fig.
The formation of the embryo sac in angiosperm plants (Magnoliopsida) and the processes of embryo and endosperm formation occurring inside this single multinucleated cell are so well known that there is no need to dwell on them in more detail here. However, it is worth noting the remarkable and rather strange circumstance that among plants, embryogenesis according to the “cell within a cell” type appears only in this youngest, evolutionarily advanced group, while the analogous examples listed above among animals are characteristic only of very simply organized groups that have passed to parasitism.
Based on the well-known evolutionary advantages of sexual reproduction over asexual reproduction (see, for example,
The situation is quite different in multicellular organisms. First, due to the increase in the size of their bodies, each multicellular organism occupies a place in space that is many times greater than the size of the gametes it produces. Secondly, before the start of gametogenesis, such an organism must reach the complex multicellular stage of the “vegetative” body (see the first reproductive criterion of multicellularity above), which creates a certain (often very significant) individual variation in terms of readiness for the sexual process and maturation of gametes. Thirdly, the appearance of oogamy in multicellular organisms leads to the fact that only male gametes retain their own mobility (and sometimes it is lost in gametes of both sexes). Considering all these features, it is possible to achieve cross-fertilization of gametes at the multicellular level of organization in the following ways: 1) by keeping immobile female gametes in the body of the mother’s organism until they are found by spermatozoa (internal fertilization in the broad sense); 2) forcibly ejecting female gametes into the external environment synchronously with the ejection of spermatozoa by other individuals of the population (external fertilization); 3) providing a passive release of numerous gametes into the external environment at a strictly defined time (also external fertilization).
The first way, undoubtedly, turns out to be technically simpler and is implemented independently in the vast majority of groups of archaic multicellular organisms. Thus, in the vast majority of sponges, in trichoplax, in archaic turbellarians, in extremely simplified orthonectids and dicyemids, in multicellular fungi, in volvox, in most oogamous multicellular algae, as well as in all higher plants, internal fertilization of the egg occurs, and the initial stages of embryogenesis take place inside the body of the mother organism, or the zygote becomes a resting stage and finds itself in the external environment after the death and disintegration of the mother’s body. A clear understanding of this circumstance allows us to answer the age-old question of classical biology about whether for animals and other multicellular organisms the original method of reproduction was external fertilization with the corresponding complete development of the daughter organism in the external aquatic environment. In many old and modern general theoretical works, this was taken for granted so much that it was not even specially argued (see, for example,
Graphical interpretation of the “sedentary” hypothesis of the origin of multicellular animals under the assumption of the initial external fertilization (according to
Scheme of the origin of multicellular animals (Metazoa), based on the hypothesis of primary viviparity. Maximal figure size, please!
In some oogamous multicellular algae, due to the simplicity of their structure, it turns out to be rather difficult to draw a clear line between fertilization inside the mother’s body and on its surface. Thus, in Laminariales brown algae, the egg is released from the oogonium before fertilization, but remains attached to its edges. The zygote germinates without detaching from the maternal gametophyte. If, due to random events, the egg or zygote loses its connection with the mother plant, then differentiation processes are disrupted during germination and the resulting defective thallus soon dies (
External fertilization is well known and studied in many groups of marine and freshwater animals, in which this process is ensured by the presence of the nervous system, sensory organs, muscles, and various genital ducts. Receiving a certain signal (visual, tactile, chemical) from each other, sexual partners implement a forced synchronous release of gametes into the external aquatic environment. However, for the most archaic animals and plants, the only possible way is the passive release of gametes, in particular, through the rupture of the shells of the “gametangia”, synchronized by external causes. A comparative analysis of the reproductive strategies of various multicellular organisms shows that it is extremely difficult to achieve synchrony with the passive variant. This path was realized only in a few small groups of marine organisms, strictly synchronized in their reproductive activity with the lunar cycles and/or the corresponding periodicity of tides. In this case, the passive release of gametes is technically provided in two different methods, but both of them are associated with significant limitations and remain evolutionarily dead ends.
The first method is known in some highly developed Demospongiae, which are built according to the progressive “leucon” type and reach large body sizes. The structure of the body allows these sponges to regulate the flow of water passing through the body and carrying out a large number of immobile eggs and motile spermatozoa (
The second way of passive synchronous release of gametes is implemented in a number of genera of brown and green algae. They are unable to regulate water flows, but their reproduction is coordinated in a complex way with the lunar cycle and tidal rhythms (
In laboratory conditions, it is very often possible to achieve synchronous opening of gametangia due to a sharp change in illumination (see review in
There does not seem to be any other effective means of precise synchronization of gamete release, apart from tidal, in multicellular plants. Understanding this, one can offer an explanation for why plants do not have egg-laying, similar to that of animals, and why asexual reproduction with sporophyte/gametophyte alternation absolutely predominates in plants, despite the obvious evolutionary advantage of bisexual reproduction and the diploid state of the multicellular body. The answer lies in the fact that plants are not able to independently release eggs into the external environment synchronously with spermatozoa. Their eggs in the vast majority of cases remain on the mother’s body, wait until spermatozoa (or sperm) reach them in one way or another, and then germinate inside or on the body of the mother’s body. In this case, reproduction and distribution are not provided by gametes or zygotes, but by spores, since no synchronization is required for this at all. Up to the highest stages of plant evolution, they fail to switch to normal independent sexual reproduction, and most flowering plants in their sexual process are also completely dependent on animals, especially pollinating insects. There are examples of plant gamete transfer in some marine plants, for example, in some red algae, for which crustaceans act as pollinators (
In animals, on the contrary, bisexual reproduction absolutely predominates, and synchronization of the release of gametes is achieved at fairly early stages of their evolution, starting with the most complexly organized sponges and coelenterates. The latter develop a simple nervous system, gonads, and musculature, in particular, a muscular intestine/stomach, through which, in the simplest case, sexual products are excreted. Some ctenophores (Ctenophora) even have specialized reproductive ducts (
The simplest version of polycytic reproduction, which consists in restoring the whole body from separate fragments, is observed in almost all archaic multicellular organisms and probably represents the original (plesiomorphic) method of polycytic reproduction for most phylogenetic lines. Despite its extreme archaism, the ability to restore the whole body from fragments is retained during the entire further evolution in most groups of plants, including the most highly developed angiosperms (Magnoliopsida), as well as in most fungi. On the contrary, among animals, this method remains possible only in organisms that are at a relatively low level of morpho-anatomical organization: sponges (Porifera), coelenterates (Coelenterata), various taxa of flatworms (Plathelminthes), some nemerteans (Nemertini), and annelids (Annelida). A somewhat more complicated version of fragmentation can be considered the division of the body in two by lacing or splitting. Such methods are known, for example, in trichoplax, some coelenterates and flatworms. At the same time, division without previous morphogenetic preparation (architomy) and division after preliminary doubling of body parts (paratomy) are distinguished – see, for example,
An apomorphic feature inherent in some protonemal and embryogenic multicellular organisms, as well as representatives of “complex” organisms – lichens (Lecanoromycetes) — can be considered the appearance in them of a special polycytic budding (= blastogenesis), as a result of which specialized outgrowths are regularly formed from groups of somatic cells, over time, separating and growing into independent individuals. In many groups of organisms, such polycytic budding occupies a strictly defined place in the life cycle or even represents the main way of reproduction and distribution in space. So, in many highly organized representatives of lichens, polycytic budding is the only way of reproduction (not counting accidental fragmentation of the body). This process is carried out through the formation of the so-called soredia and isidia (Fig.
Polycytic budding in lichens: reproduction by isidia (after
Polycytic budding is highly developed in Charophyceae s.s. and is provided by special nodules on rhizoids or by special “stellate cell clusters” (
A significant diversity of polycytic “brood bodies” is observed in gametophytes of various liverworts (Marchantiophyta) and mosses (Bryophyta) (
In animals, polycytic budding is widespread among sponges (Porifera), trichoplax (Fig.
Scheme of the life cycle of Trichoplax adhaerens Schulze, 1883; asexual reproduction is provided by polycytic budding.
Polyembryony can be considered a special type of polycytic budding, apomorphic for some embryogenic multicellular organisms. This term, like many others used in reproductive biology, has a rather vague meaning. In most cases (and in this article), polyembryony means the regular division of a developing zygotic embryo into several secondary embryos (see, for example,
Polyembryony is extremely widely understood in the literature on flowering plants (
Rare cases of polyembryony among animals are known in some genera of cyclostomes (Cyclostomatida), monogenetic flukes (Monogenea), endoparasitic hymenopterans (Hymenoptera) and Strepsiptera, as well as in mammals – armadillos of the genus Dasypus Linnaeus, 1758 (
An extremely peculiar analogue of polyembryony can be seen in the development of the so-called “carposporophyte generation” of red floridian algae (Rhodophyta: Florideophyceae) (Fig.
A number of groups of multicellular organisms completely lose the ability for polycytic reproduction (with the exception of the rarest cases of polyembryony mentioned above). Such, for example, are various taxa within the polyphyletic group of Nemathelmintes, echiurids (Echiurida), brachiopods (Brachiopoda), arthropods (Arthropoda), mollusks (Mollusca), vertebrates (Vertebrata). Obviously, such a loss is associated with a high degree of specialization of the tissues and organs of these organisms and the corresponding loss of totipotency in most of the somatic cells that make up their body. At the same time, the almost total absence of polycytic reproduction in gymnosperms and even in such simply organized multicellular plants as Volvox spp. is not entirely clear.
The multiple origin of multicellularity in different groups of organisms allows at the present time to give only a very approximate minimum estimate of the total number of such evolutionary events. Apparently, there were at least 50 cases of independent origin of multicellularity among eukaryotes and at least several dozens among prokaryotes. Examples of protonemal multicellularity among bacteria and algae are of particular difficulty for calculation, since the modern systems of these organisms abound in genera that simultaneously include species with simple unicellular, colonial-unicellular and obligate-multicellular bodies (see, for example, AlgaeBase: https://www.algaebase.org/). It is equally difficult to count the numerous cases of transition from siphon-unicellular to siphonoseptal multicellularity among fungi and algae, developing through the initial stage of a multinuclear “siphon”. A much clearer picture emerges with regard to embryogenic multicellular organisms. Thus, there is no doubt about the single independent appearance of animals and separately Volvox spp. on the basis of the corresponding ancestral spherical colonies with an internal cavity (
It is noteworthy that all complex multicellular organisms that have tissues and organs develop according to the type of embryogenic multicellularity based on obligate accumulative oogamy or accumulative aplanosporia. This is probably due to the well-known fact that a large volume of cytoplasm in the egg and its complex structure are very important for the initial differentiation, which then ensures the predetermination of cleavage and the formation of specific tissues and organs from certain blastomeres. For animals, in addition to the initial predetermination of cleavage, the formation of internal body cavities, in particular, the primary cavity (the blastocoel), is also important, and this, probably, cannot be achieved on the basis of protonemal or siphonoseptal development.
Summing up all of the above, I can highlight the following final suggestions:
The author is extremely grateful to his colleagues who made valuable comments on the text of the article, especially V.G. Kuznetsova, A.V. Ereskovsky, A.L. Rizhinashvili, M.V. Vinarsky and anonymous reviewers. The work was carried out within the framework of the budget theme of the Zoological Institute RAS (No. 122031100272-3).
Ilya A. Gavrilov-Zimin https://orcid.org/0000-0003-1993-5984