by Alexander MARTYNOV, Cand. Sc. (Biol.), Zoological Museum of Lomonosov Moscow State University

All known plants and animals have names, but mentioning them occasionally, one usually does not think much about what kind of fish, mollusk, or orchid species is meant. And a few of us can imagine what kind of dramatic discussions sometimes occurred in the history of biological systematics responsible for classification of modern and extinct organisms of our planet. This science forms a basis for the theory of evolution and for modern biology.

Biological systematics was never a simple discipline. We still are not quite sure what should be considered as a "base", what is a "superstructure", what is the cause and what is the effect and why not vice versa. Our science develops as if in two dimensions. On the one hand, there are molecular taxonomists, not interested in morphology and ontogenesis*, but trying to build a system and reconstruct the history of organisms only on the basis of statistical regularities (for example, substitution of DNA nucleotides in the course of evolution). On the other hand, there are classical taxonomists, using (since the mid-18th century) the "two names method", or binominal method, referring each species to just one definite genus.

The possibility of differentiating between the groups of organisms by diagnostic characters, "read" identically by any scientist, makes the binominal method the only real working instrument of a biologist-taxonomist. This method still has no adequate alternatives. Using the

* Ontogenesis is an individual cycle of any organism, leading to conservative reproductibility of its already existing organization in a series of subsequent generations.--Auth.

hierarchy construction principle, known to the scholastic of the Middle Ages and later used by an outstanding Swedish naturalist Carl Linney, Foreign Honorary Member of St. Petersburg Academy of Sciences (from 1754) in his famous "System of Nature" (1735), the specialists not only described more than a million of modern species of flora and fauna, but paved a path to the idea of evolution. For the prima facie combinative method of taxon formation (taxa are definite groups in classification) and their construction "according to one's wishes" (at first sight) eventually led to the discovery of real phenomena of the Nature. Armed with the "two names method", a student, expert, or just an amateur naturalist in any country of the world will confirm the existence of bivalves, Polychaeta class worms, or mammals. The biological systematics here is not inferior to exact sciences. The specialists proceed from in fact simple bases and need no sophisticated theoretical approaches. It would be appropriate to recollect here the well-known words of Max Plank, an outstanding German physicist, Nobel Prize Winner in physics in

1918, Foreign Honorary Member of the Russian Academy of Sciences (from 1926) on the practicability of any good theory.

But how can seemingly "immobile" taxonomy be united with a continuous evolutionary process, how can bridges between the present and past be constructed? Attempts to suggest this or that approach have been disturbing biological science for over 150 years, since Charles Darwin, celebrated English scientist, Foreign Member of St. Petersburg Academy of Sciences (from 1857) showed in 1859 that the systematic hierarchy could be "converted" to a sequence of evolutionary events or "the tree of life".

"BRIDGES" BETWEEN THE PAST AND THE PRESENT

This idea, superb at a theoretical level, was rather difficult for practical realization. The scientists resisted the evolutionary approach to taxa for a rather long time, but after 1859 the process of its "penetration" into taxonomy really started. One of the founders of the new field of research was Ernst Haeckel, a celebrated German biologist, with his works General Morphology (1866) and System-atie Phytogeny ( 1894-1896). It was to denote the process of historical development of "immobile" hierarchy of organic world representatives and suggested the term "phytogeny"*. The moment of emergence of new species was to be reflected in the classification, and the corresponding next branching of the "tree of life" substantiated the hierarchy of characters of organisms, developed by generations of scientists and seeming purely theoretical at first sight. Just so simple! However, it took 100 years for this approach to win recognition of scientists.

In 1966 a translation of the book Phylogenetic System-atics by Willi Hennig, a German entomologist, was published in the USA. This scientist regarded classification of organisms as genealogy. By using a strict system of arguments, he bound "higher" taxa to their ancestral species and in fact introduced Darwin's and Haeckel's ideas into practice. A field of research now called cladis-tics (kládos (Greek)--branch) was born then. Hennig's idea literally "exploded" the professional community of taxonomists. It seemed that as a result of the biologists' dissatisfaction with traditional taxonomy, which had been accumulating over so long a period, the common habitual concepts on taxonomy as a science of a limited

* Phylogeny or phylogenesis is historical development of an organism.--Auth.

Science in Russia, No. 3, 2011

circle of haughty experts or eccentric enthusiasts led to the most serious revision of the discipline. Logicians, philosophers, mathematicians were thus attracted to taxonomy.

Fulminant "self-organization" of the concept in the 1970s and 1980s, unfolding primarily in the USA, changed, largely irreversibly, this science. Starting from the 1990s the classical approach to taxonomy with a universally acknowledged taxon hierarchy became unpopular. Many scientists studied just individual characters, implying that the phylogenetic analysis would "assemble" anew a more reliable system. Dichotomic schemes of successive branching of new taxa--"cladistic trees"--were constructed for demonstration of the evolutionary process in different groups of organisms.

The unprecedented breakthrough in the overall availability of computer technologies in the 1990s led to a very rapid formalization of already sufficiently formal cladistic methods and an avalanche inflow of computer software "for reconstruction" of phylogeny. Today, 15 years later, it is obvious that despite tremendous efforts, old problems have been replaced by new ones, while "white spots" in taxonomy and reconstruction of evolutionary ways remained the same.

But let us return to the 20th century. No doubt, the years between Darwin's and Haeckel's works and Hennig's book were by no means "blank". Interpretation of the idea of evolution by classical taxonomists and by "new" biologists, oriented to studies of physiology and ecology, was difficult, contradictory, and led to the formation of a basically less rigid evolutionary and morphological cycle of studies of organisms, allowing certain pluralism of opinions. The significance of Russian scientific schools in the development of this field of research is really great. Russian specialists considered that studies of the ontogenesis of modern species and of morphological bases of their adaptation to changing environmental conditions are particularly significant for the reconstruction of evolutionary events.

In 1910, Alexei Severtsov, an outstanding morpholo-gist and embryologist (Academician from 1920) presented his concept of phylembryogeneses, which became an official doctrine of Russian and Soviet evolutionary morphology. Its gist is as follows. The changes in individual development of organisms of any species are the major source of evolutionary transformations. In the

1920s Vladimir Beklemishev, a specialist in comparative morphology, Professor of Perm University, suggested regarding an organism as a morphoprocess, in which all developmental stages are closely interrelated. Severt-sov's theory and Beklemishev's concept became a logical consequence of the "postbiogenetic age", when the famous Haeckel's law (ontogenesis is a brief repetition of phylogenesis) no longer limited the scientists in their search for a new theory.

In the second half of the 19th century, scientists of different countries (Fritz Miiller, a German zoologist, Adam Sedgwick, an English biologist, etc.) gradually realized that it was not phylogenesis that caused ontogenesis, but quite contrary: ontogenesis, in a certain sense, created evolution. However, these viewpoints in the form of a strict theory were for the first time generalized only in Severtsov's work Studies in the Theory of Evolution (1912). Beklemishev in his later works (1944, 1964) emphasized that the life cycle of a species was a unit of comparative morphology. Many Russian embryologists and evolutionary morphologists shared his views.

"ANTIDOTE" TO FORMAL SCHEMES

Strictly speaking, the concept of the cyclic pattern of natural processes is an intrinsic part of many philosophical and religious theories of the past and of modern science. Long before Beklemishev, Karl Gegenbaur, a German comparative morphologist, Foreign Member of St. Petersburg Academy of Sciences (from 1885), wrote (in 1859) that morphology studied organisms not only in their adult state, but in all preceding states of development as well. Today various cycles--cellular, replication of DNA, seasonal cycles in plants and animals, and the ontogenetic (life) cycle of all organisms--are well known to any biologist. Nevertheless, we almost never mention them speaking about the history of species formation, evolution, and phylogeny. Why?

Probably the "founder effect" (in biology these words are used when a character emerging in a small ancestor population becomes a common character in all descendants) is a key factor here. On the very first pages of his famous work Hennig for more strict substantiation of his theory, divided the entire ontogenetic cycle (life cycle of any species) into stages during which the organism becomes a bearer of certain distinctive characters, or a "semaphoront", as he called it. This methodological approach was later widely used and taxonomy since then was regarded mainly as a combinative discipline devoid of strict regularities.

Authors of concepts on cyclic nature of evolution often resorted to simplifications of different kinds. For example, Otto Schiendewolf, a German paleontologist, in 1950 tried to find in the historical development of taxa a strict correspondence to the three-phase ontogenesis of an organism: birth, development, death. However, there are many controversies here, as despite the fact that representatives of numerous orders and classes, inhabiting the Earth long ago, died out, all main phyla of multicellular animals, which had appeared in the Cambrian (about 540-490 mln years ago) exist up to the present time (mollusks, arthropods, annelids, and many others). Their morphological and hence, physiological, ontogenetic, molecular, and other fundamental properties have not principally changed over the last half-billion years.

Let us point out that this fact does not contradict the possibility of evolution of organisms within the framework of their life cycles by shifting certain stages of individual development in comparison with the adult (mature) state. These shifts do not correspond to stages of historical development of taxa; quite the contrary, they occur repeatedly during different geological periods in different unrelated representatives of this or that species, class, etc.

For example, describing our objects, we (taxonomists) often discovered a shift of larval morphology to adult stages of the organism's development. In other words, some creatures never become adult--the paedomorphosis phenomenon (Greek paidos--a child and morphe--form, species). The author of this paper in 2004-2010 studied skeletal elements, including vertebrae of brittle stars (a group of sea invertebrates belong to the phylum Echinodermata and related to starfish), at the laboratory of electronic microscopy of the biological faculty of Lomonosov Moscow State University. Ophiuroidea class is one of the most unusual groups of modern echinoderms. Of all multicellular organisms only these organisms and vertebrates have a system of vertebrae of similar construction. We have studied 178 species of 105 genera and 16 families of modern brittle stars and in some cases confirmed paedomorphosis in them. Thus, detailed information about their microstructure has been obtained for the first time. It suggests a critical revision of taxonomy of this class of organisms in general. Based on the new data on morphology and ontogenesis, it will be possible to say with almost mathematical

A new model of dorid nudibranch mollusk evolution (a fragment of the original scheme).

Formation of branchial cavity in notaspid sea slugs (shown in orange)

indicated the emergence of the cryptobranchial dorid group.

The further evolution led to reduction of the branchial cavity.

exactness what, specifically, kind of characters of adult paedomorphic (with characteristic shift of larval morphology to adult stages) brittle stars correspond to larval (juvenile) and early postlarval characteristics of their nonpaedomorphic "sisters".

Hence we have concluded: an analysis of cycles of ontogenesis is one of the best methods suggested for studies of the history of organic world development and a good "antidote" protecting from an increasing number of publications on taxonomy, in which the arguments are confined to just statistical data. Judging by the available facts (our and of other scientists), shifts in life cycles is one of the fundamental mechanisms of evolution. Half a century ago the majority of specialists understood this fact, but by the end of the 1960s meticulous work in search of correlation between morphological and ontogenetic changes and evolutionary processes was gradually replaced by more formal studies of gene frequency in populations and of genealogical relationships between taxa. Molecular phylogenetics entered our life, largely inheriting features of morphologically substantiated phylogenetic taxonomy, but promoting reduction (simplification) of all kinds of biologically valid evolutionary models except of statistical ones.

The last decade witnessed a violent discussion between the advocates of "morphological" and "molecular" approaches. In 2003, Robert Scotland with his colleagues from Oxford University (U.K.) doubted the values of traditional morphology for studies of evolution, while in 2009, Wolfgang Wiigele from the Zoological Museum in Bonn (Germany) with his colleagues criticized the formal molecular analysis. A sensible balance would, no doubt, eventually be restored. The professional community was recently disturbed on seeing that the real evolution of living organisms was virtually lost behind formal phylogenetic "trees". Perhaps time has come to revise "dusty attics and dark basements" of the old theories viable in modern molecular age.

Comparison of morphology of adult brittle stars (E, F), early juvenile specimens (A, B), and their paedomorphic descendant species (i.e. with juvenile characters persisting in adult organism) (E, F); d: disk diameter. OPHIURA SARSII: A, B-adult specimen (d = 21 mm); C, D-early postlarval stage (d = 500 fim). PERLOPHIURA PROFUNDISSIMA: E, F-adult animal (d = 2 mm). Micrographs by A. Martynov

WHAT UNITES TAXONOMISTS?

Unfortunately, there is still no complete theory of transformation of the form of organisms, which is understandable as studies of cellular and molecular mechanisms of their life cycles have become possible only recently. The evolutionary developmental biology or evo-devo, emerging on this basis (the term was introduced in 1992 by Brian Hall from the Dalhausy University in Canada), though a theoretical heiress of Haeckel's biogenetic law and Severtsov's theory of phylembryogeneses, now have become rather a modem technology for studies of life cycles. As a whole, this field and classical systematics and phylogenetics virtually do not cooperate. Their new synthesis (re-synthesis) is required; let us call it ontogenetic systematics. That is a probable starting point for the construction of a general theory of evolution of ontogeneses, as the latter is largely conditioned by changes in a small set of ancestral life cycles of multicellular animals (Metazoa), which emerged during the pre-Cambrian and early Cambrian (and these are phyla of classical taxonomy).

It goes without saying that evolution of organisms should not be regarded as a process always leading exactly to the initial form or as the above-mentioned "three-phase" model (birth, heyday, death). Novelties in ontogenesis of any organism can change the direction of general development. That was the case hundreds of millions of years ago and that is so today: the properties of life cycles determine and at the same time largely limit evolution.

No matter how many phylogenetic schemes were created, describing the origin and evolution of, say, Chordata, the best proof of Darwin's theory was the work of Alexander Kovalevsky, a Russian morphologist and embryologist, Academician of St. Petersburg Academy of Sciences (from 1890), published in 1866 and proving the similarity of mobile complex vertebrates and sacciform sessile ascidians* on the basis of an analysis of the ontogenetic cycle of these animals. The scientist described the mobile larva of these animals, which had a chord (in contrast to immobile individuals). Haeckel (1868) and Darwin (1874) immediately used these results as the most persuasive argument supporting the reality of evolution.

* Ascidians-a class of attached sacciform animals, Urochordata sub-phyltim, Chordata phylum, inhabiting a sea bottom.--Auth.

To realize this approach, it is essential not only to determine the sole ancestor species for animals, but also to construct models of its complete ontogenetic cycle. If characters of this or that (for example, juvenile) life stages of the ancestor "shifted" to the descendant's adult stage in the course of further evolution, underestimation of this fact can lead to very serious errors in the conclusions, including the above-mentioned assumption about the imaginary archaic ancestor status of these taxa.

In order to illustrate this point, let us analyze another group of invertebrates, nudibranch mollusks, we have been studying from this viewpoint for many years. By their life style, they are mainly benthic animals without shells, i.e., let us mention representatives of the Doridacea order with gills located around the anal opening on the back. More than 1,500 species with a well-developed branchial cavity (Cryptobranchia) are known; there also exist dorids with no branchial cavity (Phanerobranchia).

Traditionally the latter were assumed to be the ancestors of the former ones, but the facts indicating the opposite were neglected. Our task was to create a model of evolutionary development of these organisms, uniting main ontogenetic parameters of their initial (ancestor)

Proximal vertebrae of adult (A, B, D) and juvenile (C) brittle stars; d-disk diameter. Nonpaedomorphic species:

A-OPHIURA SARSII,

d= 15 mm;

B-OPHIOSPHALMA

ARMIGERUM (1), d = 23 mm; C-the same species,

d = 2.8mm.

Paedomorphic species:

D-PERLOPHIURA

PROFUNDISSIMA (1), d = 3 mm. Micrographs by A. Martynov

and derivative (descendant) cycles. And, according to our colleagues, we solved this problem.

The analysis has clearly demonstrated that the disappearance of the branchial cavity in dorids (their phaner-obranchial organization) could emerge only after the cryptobranchial organization. Besides, the evolutionary process led to changes in the number of life cycle stages in some species in comparison with the ancestors (called notaspids) and to a shift of the branchial system from the ventral to the dorsal side and hence, formation of the branchial cavity. It was found that all without exclusion modern representatives of this order, which had no branchial cavities, were not primary (ancestor) forms, but vice versa--secondary regressive derivatives of a more complex life cycle of cryptobranchial dorids. The important discovery of an intermediate link in the evolution of nudibranch mollusks, living in Kamchatka waters (we found and described a really existing organism) completely confirmed the new model of evolution of this group of animals. The discovery was made in 2008 by the author of this paper in collaboration with Tatyana Korshunova, Cand. Sc. (Biol.) from the Institute of Higher Nervous Activity and Neurophysiology, the Russian Academy of Sciences (Moscow), Karen and Nadezhda Sanamyan from the Kamchatka Branch of the Pacific Institute of Geography, Far Eastern Branch of the Russian Academy of Sciences (Petropavlovsk-Kamchatsky).

The new organism, belonging to the onchidoridid family and called Onchimira cavifera ("amazing onchidoridid with a branchial cavity), paradoxically combined the presence of a branchial cavity (a character heretofore unknown for representatives of its family) and strictly specialized characteristics of the internal structure, due to which the organism was without doubt referred to this family. This showed that the ancestor really had a branchial cavity, which later gradually reduced and eventually disappeared.

Realization of this fact leads to a true revolution in nudibranch mollusk phylogeny, and our work attracted great attention of our colleagues. At present we are studying this group of invertebrates in collaboration with Michael Schrodl from the Bavarian State Zoological Collection (Munich, Germany).

Thus, ontogenetic systematics is characterized by a more accurate definition of the causes and effects, in contrast to the modern cladistic approach, implying that almost everything is possible and any contradiction can be attributed to insufficient sampling of characters and taxa.

Today, as throughout almost 300 years of development of our science, specialists in taxonomy are engaged in their inconspicuous and sometimes not very prestigious, though exceptionally important work. They detect natural phenomena, the existence of which does not depend on man (species, genera, and other taxa in the systematic hierarchy). Our responsibility is great, as our conclusions--a starting point for all biologists, and modern phylogeneticists, who have to reconstruct the evolution on the basis of molecular data, are not an exclusion.