Alexander Martynov

Deep-water Ophiuroidea of the northern Atlantic with descriptions of three new species and taxonomic remarks on certain genera and species

Abstract Based on material from the fourth cruise of the RV Akademik Mstislav Keldysh and the MAR-ECO cruise of the RV G.O. Sars, 31 species of Ophiuroidea were identified from the section of the Mid-Atlantic Ridge between the Reykjanes Ridge and the Azores. The taxonomy of the group of genera with reduced arm comb and tentacle pores restricted only to the proximal arm segments is reviewed. It is suggested that the genera Homalophiura H.L. Clark, 1915, Ophiurolepis Matsumoto, 1915, Theodoria Fell, 1961 and Homophiura Paterson, 1985 should be regarded as synonyms of the genus Ophioplinthus Lyman, 1878. From examination of the type specimens, it is demonstrated that the six-armed species Ophiacantha anomala G.O. Sars, 1871 also includes five-armed specimens previously identified as the separate species Ophiacantha cuspidata Lyman, 1878. The latter taxon is considered here as the junior synonym of O. anomala. Previously mentioned ‘deep-water populations of the common shallow water species Ophiacantha bidentata (Retzius, 1805)’ represent a separate species, Ophiacantha fraterna Verrill, 1885, which is well distinguished by the shape of the spicules of the disk, narrow outer oral papilla and narrower tentacle scale as well as a hermaphroditic nature. Three new species, i.e. Ophioplinthus pseudotessellata sp. nov., Ophiocamax patersoni sp. nov. and Ophiophyllum nesisi sp. nov., are described.

The new Arctic side-gilled sea slug genus Boreoberthella (Gastropoda, Opisthobranchia): Pleurobranchoidean systematics and evolution revisited

Most of the ca. 100 known pleurobranchoid side gilled sea slug species are confined to temperate and warm coastal waters worldwide. Exceptions were five enigmatic Antarctic and southern deep sea species. Herein the first Arctic deep water pleurobranchid, Boreoberthella augusta gen. et spec. nov., is anatomically described. To reveal the origin, relationships and phylogeography of Boreoberthella, a cladistic analysis of 24 pleurobranchoid taxa representing all genera and traditional higher groups was prepared. The morphological data set includes 72 characters; many of them, such as details of the copulatory apparatus, were explored for the first time. The monophyly of both Pleurobranchoidea and Pleurobranchaeidae is confirmed. In contrast to an earlier study, the southern Ocean deep-water species Tomthompsonia antarctica results as basal offshoot of the monophyletic though poorly supported Pleurobranchidae which show a secondary, internal shell. The traditional genus Berthella with worldwide temperate and tropical members may represent an evolutionary grade rather than a clade. The monotypic genera Parabathyberthella and Polictenidia are synonymized with Bathyberthella according to taxonomic and phylogenetic evidence. The basal pleurobranchaeid genus Pleurobranchella, together with Tomthompsonia, Bathyberthella, and Boreoberthella are discussed as potential relics of a cold-water related early nudipleuran radiation in Antarctica, with subsequent dispersal through the depths of the world oceans. The ancestor of Pleurobranchus species, the closest relatives of Boreoberthella, colonized coastal and warmer waters and radiated there.

Restructuring higher taxonomy using broad-scale phylogenomics: The living Ophiuroidea

The power and throughput of next-generation sequencing is instigating a major transformation in our understanding of evolution and classification of life on our planet. The new trees of life are robust and comprehensive. Here we provide a landmark phylogeny of the living ophiuroids and use it as the basis for a major revision of the higher classification of this class of marine invertebrates. We used an exon-capture system to generate a 1484 exon (273kbp) data-matrix from DNA extracted from ethanol-preserved museum samples. We successfully obtained an average of 90% of our target sequence from 576 species spread across the known taxonomic diversity. The topology of the major lineages was robust to taxon sampling, exon-sampling, models and methods. However, estimates of node age were much less precise, varying by about a quarter of mean age. We used a combination of phylogenetic distinctiveness and temporal-banding to guide our revision of the family-level classification. Empirically, we determined that limiting family crown age to 110±10Ma (mid Cretaceous) selected phylogenetically distinct nodes while minimising disruption to the existing taxonomy. The resulting scheme of 32 families and six orders considerably expands the number of higher taxa. The families are generally longitudinally widespread across the worlds oceans, although 17 are largely confined to temperate and equatorial latitudes and six to relatively shallow water (less than 1000m depth).

Polyphyly of the traditional family Flabellinidae affects a major group of Nudibranchia: aeolidacean taxonomic reassessment with descriptions of several new families, genera, and species (Mollusca, Gastropoda)

Abstract The Flabellinidae, a heterogeneous assembly of supposedly plesiomorphic to very derived sea slug groups, have not yet been addressed by integrative studies. Here novel material of rarely seen Arctic taxa as well as North Atlantic, North and South Pacific, and tropical Indo-West Pacific flabellinid species is investigated morpho-anatomically and with multi-locus markers (partial COI, 16S rDNA, 28S rDNA and H3) which were generated and analysed in a comprehensive aeolid taxon sampling. It was found that the current family Flabellinidae is polyphyletic and its phylogeny and taxonomic patterns cannot be understood without considering members from all the Aeolidacean families and, based on a robust phylogenetic hypothesis, morpho-anatomical evolution of aeolids is more complex than suspected in earlier works and requires reclassification of the taxon. Morphological diversity of Flabellinidae is corroborated by molecular divergence rates and supports establishing three new families (Apataidae fam. n., Flabellinopsidae fam. n., Samlidae fam. n.), 16 new genera, 13 new species, and two new subspecies among the former Flabellinidae. Two families, namely Coryphellidae and Paracoryphellidae, are restored and traditional Flabellinidae is considerably restricted. The distinctness of the recently described family Unidentiidae is confirmed by both morphological and molecular data. Several species complexes among all ex-“Flabellinidae” lineages are recognised using both morphological and molecular data. The present study shows that Facelinidae and Aeolidiidae, together with traditional “Tergipedidae”, deeply divide traditional “Flabellinidae.” Diagnoses for all aeolidacean families are therefore provided and additionally two new non-flabellinid families (Abronicidae fam. n. and Murmaniidae fam. n.) within traditional tergipedids are established to accommodate molecular and morphological disparity. To address relationships and disparity, we propose a new family system for aeolids. Here the aeolidacean species are classified into at least 102 genera and 24 families. Operational rules for integration of morphological and molecular data for taxonomy are suggested.

Paedomorphosis as an Evolutionary Driving Force: Insights from Deep-Sea Brittle Stars

Heterochronic development has been proposed to have played an important role in the evolution of echinoderms. In the class Ophiuroidea, paedomorphosis (retention of juvenile characters into adulthood) has been documented in the families Ophiuridae and Ophiolepididae but not been investigated on a broader taxonomic scale. Historical errors, confusing juvenile stages with paedomorphic species, show the difficulties in correctly identifying the effects of heterochrony on development and evolution. This study presents a detailed analysis of 40 species with morphologies showing various degrees of juvenile appearance in late ontogeny. They are compared to a range of early ontogenetic stages from paedomorphic and non-paedomorphic species. Both quantitative and qualitative measurements are taken and analysed. The results suggest that strongly paedomorphic species are usually larger than other species at comparable developmental stage. The findings support recent notions of polyphyletic origin of the families Ophiuridae and Ophiolepididae. The importance of paedomorphosis and its correct recognition for the practice of taxonomy and phylogeny are emphasized.

Ontogenetic systematics: The synthesis of taxonomy, phylogenetics, and evolutionary developmental biology

The main purpose of the present review is to draw attention to growing problems in the modern systematics and phylogenetics which are presently underestimated by the professional community. The dramatic reduction of the importance of ontogeny and morphology in phylogenetic studies of the second part of the 20th century is considered among the major factors of the modern taxonomic and evolutionary paradigm. The deep contradiction of modern approaches, which either merely consider systematics and phylogeny as genealogy or even in a neotypolgical manner irrespective of the evolutionary idea, is demonstrated. Thus, despite the widespread opinion that the evolutionary theory is the major basis for taxonomy, the processes, which in fact caused the origin and formation of the systematic hierarchy are often considered as redundant for the procedure of classification. In this respect, the classical, but well forgotten statement that evolution is a modification of ontogeny is specially highlighted. Tight relationships between evolution, ontogeny, systematics, and phylogenetics are prima facie obvious, but also presently underestimated, although the field of the evo-devo is continuously growing. Paradoxically, even despite the outburst of various molecular ontogenetic approaches, the commonly accepted evolutionary paradigm still lacks a general theory for changes in the shape of organisms. As a step towards the development of such a theory, a synthesis (or more exactly, resynthesis) of still largely independently developing major biological fields, i.e., ontogenetic and evolutionary studies, on the one hand, and traditional taxonomy, on the other hand, a new concept of ontogenetic systematics is proposed. The new concept is intended for integration of supposedly “immobile” traditional taxonomy with the dynamics, but predominantly considered as hypothetical, evolutionary field based on the process of ontogeny, which, in contrast to the evolution itself, can be observed in the real time. Therefore, it is concluded that, for instance, the evolution of the main group of living organisms Metazoa, is primarily the evolution of a very limited number of ontogenetic cycles that were formed as early as the Early Cambrian. A significant underestimation of cyclic properties of ontogeny in the evolution and systematics is shown. Using two model groups, echinoderms of the class Ophiuroidea and dorid nudibranch mollusks (Gastropoda: Doridacea), practical importance of the integrative approach developed here is demonstrated. The “disruption” of the ancestral ontogenetic cycle and further formation of a new descendant cycle (which implies some continuity of ancestral and descendant characters) is considered to be a major evolutionary pattern. The model proposed implies either progressive (addition of stages and characters) or regressive (reduction of already existing stages and structures) modification of ancestral taxon, the diagnosis of which corresponds to the model of its ontogenetic cycle. In the extreme cases of disruption of the ancestral ontogenetic cycle, adult characters of descendants are substituted by juvenile ancestral features, demonstrating paedomorphoses in the narrow sense. Within the framework of the approach proposed, the evolutionary and ontogenetic models of ancestral ontogenetic cycles of brittle stars and dorid nudibranchs are developed and discussed. Based on the original material of the extinct Paleozoic ophiuroid group Oegophiurida, the origin of key evolutionary novelties is discussed. A major conclusion of the present review is the high necessity of integration of new molecular data with already well-established taxonomic hierarchy and ontogenetic information as a basis for the development of the general theory of transformations of organisms, i.e., the theory of evolution in its true sense.

External diversity is restrained by internal conservatism: New nudibranch mollusc contributes to the cryptic species problem

Cryptic species are an important concept of modern biodiversity studies and a potential basis for immensely increasing the amount of biological diversity worldwide; however, the conceptual grounds of cryptic species still need to be refined. Here, using a remarkable example from marine invertebrates, the case of a species complex of common large‐sized nudibranchs of the genus Dendronotus in European waters is presented, which is relevant for the ongoing cryptic species discussion. Based on extensive sampling in the seas of Northern Hemisphere from United Kingdom to the Sea of Japan, a morphological and molecular framework is constructed for understanding the diversity of European Dendronotus nudibranchs. The present study discovered notable multilevel character diversity within the common Dendronotus “frondosus” species complex. This implies the highest degree of variation of external characters with parallel colour patterns among different species and significantly constrained conservatism of internal characters. The molecular data are congruent with the stable differences in the internal features and confirm the presence of three distinct species in this complex. While two species were already known, the third species is evidently new, based on morphological and molecular evidence and is described here as Dendronotus europaeus sp. n. In the light of multilevel character diversity, the general problem of plausibility of the distinction and practical usage of the terms “cryptic” and “pseudocryptic” species is discussed.

When Ontogeny Matters: A New Japanese Species of Brittle Star Illustrates the Importance of Considering both Adult and Juvenile Characters in Taxonomic Practice

Current taxonomy offers numerous approaches and methods for species delimitation and description. However, most of them are based on the adult characters and rarely suggest a dynamic representation of developmental transformations of taxonomically important features. Here we show how the underestimation of ontogenetic changes may result in long term lack of recognition of a new species of one of the most common ophiacanthid brittle stars (Echinodermata: Ophiuroidea) from the North Pacific. Based on vast material collected predominantly by various Japanese expeditions in the course of more than 50 years, and thorough study of appropriate type material, we revise the complex of three common species of the ophiuroid genus Ophiacantha which have been persistently confused with each other. The present study thus reveals the previously unrecognized new species Ophiacantha kokusai sp.nov. which is commonly distributed off the Pacific coast of Japan. The new species shows developmental differentiation from the closely related species Ophiacantha rhachophora H. L. Clark, 1911 and retains clearly expressed early juvenile features in the adult morphology. Another species, Ophiacantha clypeata Kyte, 1977, which had been separated from O. rhachophora, is in turn shown to be just a juvenile stage of another North Pacific species, Ophiacantha trachybactra H.L. Clark, 1911. For every species, detailed morphological data from both adult and juvenile specimens based on scanning electron microscopy are presented. A special grinding method showing complex internal features has been utilized for the first time. For all three species in this complex, a clear bathymetric differentiation is revealed: O. rhachophora predominantly inhabits shallow waters, 0–250 m, the new species O. kokusai lives deeper, at 250–600 m, and the third species, O. trachybactra, is found at 500–2,000 m. The present case clearly highlights the importance of considering developmental transformations, not only for a limited number of model organisms, but as part of the taxonomic process.

[Heterochronies in the Formation of the Nervous and Digestive Systems in Early Postlarval Development of Opistobranch Mollusks: Organization of Basic Functional Systems of the Arctic Dorid Cadlina laevis].

For the first time using laser confocal microscopy and histochemical and immunocytochemical methods (detection of F-actine, catecholamines, acetylcholintransferase, substance P and FMRFamide) in combination with classical histological methods and electron microscopy of whole-mount preparations, the structure and patterns of formation of the nervous, muscular, and digestive systems in early postlarval development (from 2 days to 4 months) in the opisthobranch mollusk Cadlina laevis were studied. Heterochronies manifested in positive allometry of the sensory organs, ganglia of the central nervous system, and the pharyngeal region of the digestive system in relation to overall body size in juvenile specimens compared to adult animals were detected.

Ontogeny, systematics, and phylogenetics: Perspectives of future synthesis and a new model of the evolution of bilateria

Ontogeny is considered as a process that allows linking two key components of biological systematics in an objective way: historically independent character attribution and phylogeny. It is proposed to designate the general theory that unifies the “static” traditional taxonomy and the dynamic evolutionary process on the basis of ontogenetic transformation of shapes of organisms as the ontogenetic systematics. One of the important practical applications is a new model of the evolution of bilaterian animals, which supposes an ancestral status of clonal asexual reproduction and its multiple reduction in different lines of Bilatera.