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In the context of studying the mechanisms of early development of the vertebrate nervous system, agnatha (cyclostomata) is a unique group of animals. Since the branches of agnatha (jawless) and gnathostomata were separated at the earliest stages of vertebrate evolution, the genes of lampreys, as representatives of jawless, could most likely retain ancient expression patterns characteristic of the ancestors of vertebrates. Previous studies of the noggin family of gnathostomata have shown that all three vertebrate Noggin genes (Noggin1, Noggin2, and Noggin4) differ in expression pattern and functional properties. It was shown that Noggin genes are involved in a wide range of ontogenetic processes, including the early development of vertebrate anterior head structures and brain regions. In this paper, the expression patterns of four Noggin genes in the head structures of larvae of the European river lamprey Lampetra fluviatilis at the early stages of development are analyzed. The analysis finds a lot of similarities in the gene expression patterns of Noggin in lampreys with the expression of their homologues in gnathostomata. The NogginB gene, showing a high level of expression in the terminal part of the brain (telencephalon), can be used as a specific marker of this unique part of the vertebrate brain, which firstly appears in the evolution of gnathostomata.

The results of studying the thermal tolerance and thermoregulatory behavior of the river lamprey larvae Lampetra fluviatilis (L.) have been reported. The upper lethal temperatures, recorded at a waterheating rate of ~8°C/h–1 and acclimation temperature of 18°C, do not differ in the specimens regarded as descendants derived from the ancestors of anadromous and resident life forms, comprising 34.3 and 34.5°C, respectively (p > 0.05). In addition, no significant differences in the temperatures preferred by larvae from the populations of different life strategies are revealed. These individuals do not show any distinct thermal preferendum, distributing across the thermal gradient field presented to them. The mean values for the preferred temperatures on each day of a 3-day experiment comprised 18.3, 19.3, and 19.8°C.

One of the most important evolutionary innovations of vertebrates is a complexly structured telencephalon, which provides higher forms of nervous activity in animals and humans. This work is devoted to the study of the appearance of the telencephalon in the early stages of vertebrate evolution. At the same time, there is reason to believe that lampreys, due to their evolutionary antiquity, could retain some ancient expression patterns of genes that regulate the development of the brain in the very first vertebrates. The study of the features of spatio-temporal expression patterns of key genes that regulate the development of the forebrain in lampreys compared with other vertebrates can help to understand the molecular mechanisms underlying the appearance and evolutionary development of this unique structure of vertebrates. This paper presents the results from analyzing the gene-expression dynamics of Lanf, FoxG1, Otx2, Goosecoid, and HoxB9 in the early stages of development of the European river lamprey Lampetra fluviatilis. It was shown that lamprey genes involved in telencephalon differentiation (Lanf and FoxG1) exhibit heterochrony of expression compared with more evolutionarily advanced representatives of vertebrates. This fact confirms the idea that the telencephalon, being evolutionarily the youngest part of the brain, could appear in vertebrate ancestors as a superstructure in the late stages of their embryonic development.

Rheoreaction of the downstream migrating smolts of the European river lamprey was studied in the experimental conditions at illuminations of day and night intensity. It was found that at the daytime the smolts are mostly dormant and if move downstream then in active-passive form (with the head against the stream, and their speed going beyond the velocity). This data is well within the findings on the night downstream migration of the smolts during the 24 h period in natural conditions. Thus, the downstream migration of the smolts has an active form.

The results of the analysis of the bolus of the larval river lamprey Lampetra fluviatlis caught in the Chernaya River in May are presented. A quantitative analysis of the main food components is performed; the taxonomic composition of algae and invertebrates is determined. The content of the digestive tract consists mainly (>90% of weight) of sand and detritus as well as algae and invertebrates. A large amount of diatoms, other plankton, and periphyton unicellular algae and coenobia, as well as plankton rotifers, have been first found among food items. It is shown that organisms from the river flow may play a critical role in larval lamprey.

The secreted protein Noggin1 was the first discovered natural embryonic inducer produced by cells of the Spemann organizer. Thereafter, it was shown that vertebrates have a whole family of Noggin genes with different expression patterns and functional properties. For example, Noggin1 and Noggin2 inhibit the activity of BMP, Nodal/Activin and Wnt-beta-catenin signalling, while Noggin4 cannot suppress BMP but specifically modulates Wnt signalling. In this work, we described and investigated phylogeny and expression patterns of four Noggin genes in lampreys, which represent the most basally divergent group of extant vertebrates, the cyclostomes, belonging to the superclass Agnatha. Assuming that lampreys have Noggin homologues in all representatives of another superclass of vertebrates, the Gnathostomata, we propose a model for Noggin family evolution in vertebrates. This model is in agreement with the hypotheses suggesting two rounds of genome duplication in the ancestor of vertebrates before the divergence of Agnatha and Gnathostomata., Ermakova et al. report four Noggin genes in lampreys and using phylogenetics, gene synteny analysis, and in situ hybridization, suggest that the Noggin gene underwent two rounds of duplication and evolved specific functions before the divergence of vertebrate and lamprey lineages. These findings offer insight into early vertebrate genome and developmental evolution.

Agnathans, the most ancient of the extant vertebrates, evoke steadily increasing interest as the object of research on the basic processes of vertebrate ontogeny. Lampreys have been more accessible to researchers than myxines (hagfish), representatives of the other class of jawless vertebrates, for more than 100 years. Studies on the functional and evolutionary aspects of early ontogeny in lamprey at the molecular level became possible in the past two decades. Studies on the distinctive features of lampreys as the ancient representatives of vertebrates and comparison to gnathostomes, the more modern vertebrates, are of great interest. Molecular studies of lampreys can provide insight into the evolutionary mechanisms for the emergence and development of individual unique structures of vertebrates. The appearance of the telencephalon, which was first detected in lampreys, was one of the most important aromorphoses of vertebrates. Development and advancement of the telencephalon in the course of evolution enabled the implementation of higher forms of nervous activity in vertebrates, including humans. Research on the molecular mechanisms of basic ontogenetic events, such as early embryonic differentiation and neural induction, in the lamprey and other vertebrates is also important. Studies on the well-developed regeneration capacity of lampreys, in turn, give hope for at least partial use of the knowledge gained in future medical practice. This article is a review of recent data on the molecular aspects of the early development of the telencephalon, early embryonic differentiation, and regeneration of lampreys.

Behavior of smolts of European lamprey and changes in their locomotor activity have been studied at varying illumination regimes. The maximal level of the locomotor activity of the smolts in aquaria and in an Open Field experimental device is recorded at night at the lowest studied illumination (0.9 lx). This maximum coincides in time with the appearance of migrating smolts in the river channel flow. In daytime, at illumination of 900 lx, the locomotor activity of the smolts is lower, which corresponds to the absence of daytime downstream migration. The change in the locomotor activity over 24 h is one of the mechanisms by which the downstream migration of lamprey smolts is achieved. The increase in the locomotor activity starts soon after evening decrease in illumination below 0.1 lx and falls on the first half of night. The period of increased locomotor activity ends before morning twilight. The presence of the circadian rhythms of locomotor activity in smolts of the European river lamprey is suggested.

Rheoreaction of the downstream migrating smolts of the European river lamprey was studied in the experimental conditions at illuminations of day and night intensity. It was found that at the daytime the smolts are mostly dormant and if move downstream then in active-passive form (with the head against the stream, and their speed going beyond the velocity). This data is well within the findings on the night downstream migration of the smolts during the 24h period in natural conditions. Thus, the downstream migration of the smolts has an active form.

The presence of a complex structured brain, the anterior department of which (telencephalon) has no analogues in other groups of animals, is a significant peculiarity of vertebrates (including the human). Previously, a vertebrate-specific monogenic class of homeobox genes Anf, which plays a key role in the development of telencephalon, was discovered in the Laboratory of Molecular Bases of Embryogenesis (Institute of Bioorganic Chemistry, Russian Academy of Sciences). Out of all vertebrates, the Anf genes were not found only in the members of the most ancient group of jawless fishes (modern lampreys and hagfish), while the telencephalon was described in these animals. According to the literature data, a branch leading to jawless fishes separated from common vertebrate stem at the earliest stages of the their evolution, and detection of the Anf genes in jawless fishes is important, since it could confirm the previous hypothesis that the origin of telencephalon in evolution was associated with the appearance of the homeobox Anf gene. In the present work, the Anf gene was for the first time described in the Pacific lamprey (Lethenteron camtschaticum), the pattern and dynamics of its expression were studied at early stages of the development of this lamprey species, and the translation of its full-size cDNA was conducted in a eukaryotic expression system (clawed frog embryos).

Data on the seasonal and diurnal dynamics of downstream migration of smolts of the European river lamprey Lampetra fluviatilis are obtained. On the basis of published data and surveys in nature, it is shown that in the largest part of the area the downstream migration of smolts occurs mainly in spring, in the period of high water in rivers caused by snow melting. The smolts undertake downstream migration at night, under minimal illumination. It has been determined experimentally that the smolts are characterized by negative photopreferendum (>90% of smolts preferred illumination

Mechanisms of the initial dispersion of early larvae resident and anadromous forms of the European river lamprey have been experimentally explored. The flow (channel flow and underflow), type of bottom, and illumination are the key factors influencing the beginning and the end of downstream migration. Larvae leave the pebble ground of the spawning area when there is underflow and illumination is reduced to the night level, and then they migrate downstream in the channel stream. It is shown that the individuals dispersing from the spawning areas have switched to exogenous feeding. The end of the dispersion occurs after larvae reach oozy habitats of the riverbed, where they can find optimal feeding conditions.

The European river lamprey came to the Upper Volga from the Baltic Sea most probably via a system of shipways developed in the 18th and 19th centuries. The Vyshnii Volochek, Tikhvin, and Mariinskaya water systems are possible invasion pathways for this species. Dispersal and colonization of the Caspian Basin was likely a combination of upstream and downstream migrations. Analysis of museum and our own samples showed that lamprey possibly migrated upstream (for spawning) along rivers of the Baltic Basin until they reached the watershed boundary from which they could disperse downstream (in the juvenile period) into rivers of the Caspian Basin. Dispersal in the Volga River could occur in accordance with the migration cycle of this opportunistic lamprey species and lead to the present distribution. Key features (dentition and number of trunk myomeres) showed that lamprey from the studied area are similar to lampreys from the Baltic basin, although specimens in each population have their own peculiarities in morphology (size and coloration). Genetic data (Cyt-b) support the idea of a relatively recent invasion of lamprey into the Upper Volga. The haplotype, found in three rivers, is one of the most widespread in Europe and is found along the supposed route of invasion.

Long-term population dynamics of three-spined stickleback Gasterosteus aculeatus in the White Sea during the 20th century has patterns similar to that of eelgrass Zostera marina. In this study we address possible mechanisms of such association through analysis of spatial distribution of juvenile stickleback in the wild and their substrate preferences in experimental conditions. Samples from different habitats (Z. marina, Fucus spp.) in 13 localities of Kandalaksha Bay have shown that the juvenile sticklebacks occurred mainly in the eelgrass beds. Their density was significantly lower in fucoids. In the experiments, carried out in August 2008–2009, the juveniles were offered the following types of substrates: brown macroalgae (dense and scarce), eelgrass and control (no substrate). In the experiments sticklebacks also showed a tendency to prefer eelgrass to fucoids, even if the density of the latter was higher. This may explain their higher densities associated with eelgrass in the wild.

An amendment to this paper has been published and can be accessed via a link at the top of the paper.

Locomotor activity was investigated in smolts of the European river lamprey at alternation of light and darkness (12/12 h) and in the dark. Two groups of smolts were discerned differing in the level of locomotor activity. The presence of the circadian rhythm in smolts has been revealed, and its role in downstream migration has been shown. The locomotor activity leading smolts to channel flow increases with decreasing illumination at evening twilight. The period of high nocturnal activity is completed a short time before morning twilight, under the action of the individual circadian rhythm. This decreases the probability of impact of predators on migrating smolts.

The taxonomy and nomenclature of residential and anadromous forms of lampreys of the genus Lethenteron are still debated. For this reason, the distribution of mtDNA COI partial sequence haplotypes of lamprey (genus Lethenteron) in Eurasia has been studied. Many haplotypes occur throughout the genus range, their frequencies varying in different regions. Both rare haplotypes, some of them specific for particular geographic regions, and common ones have been found. The haplotype occurrences do not exhibit correlation with the life history strategy of their carriers. The first data on heteroplasmy in lampreys have been obtained. The results obtained and recent published data on the morphology and biology of Lethenteron indicate that the neither the region of habitat nor the life history can serve as criteria for species identification of these animals. We suggest that the residential lampreys described as separate species L. reissneri and L. kessleri should be regarded as ecological forms of L. camtschaticum, which was initially described as an anadromous parasitic species.

In the light gradient installation, the larvae of European river lamprey Lampetra fluviatilis of 0+ age, migrating downstream (downstream migrants), are distributed predominantly over the zone of dusk illumination (150–1 lx) and less so over the daylight zone (2500–150 lx) and night illumination zone (

FoxG1, a member of the Fox/Forkhead family of winged helix transcription factors, plays key roles in the induction and spatial compartmentalization of the telencephalon in vertebrates. Loss- and gain-of-function experiments have established FoxG1 as a maintenance factor for neural progenitors and a crucial player in the specification of the ventral telencephalon (subpallium). For the first time in evolution, the telencephalon appeared in the ancestors of vertebrates, including cyclostomes. However, although FoxG1 homologues are present in cyclostomes (i.e., in lampreys and hagfishes), no systematic study of the spatial-temporal expression of FoxG1 during the embryonic development of these animals has been carried out. Given these findings, we have now studied FoxG1 spatial-temporal expression patterns in the early development of the European river lamprey Lampetra fluviatilis. We show that in contrast to other vertebrates, in which the expression of FoxG1 begins during neurulation, the expression of this gene in L. fluviatilis starts after neurulation, first at stage 21 (early head protrusion) in the area of the otic placodes and then, beginning from stage 22, in the telencephalon. Such heterochrony of FoxG1 expression in the lamprey may reflect the fact that in this basally divergent representative of vertebrates, telencephalon specification occurs relatively late. This heterochrony could be related to the evolutionary history of the telencephalon, with a recent appearance in vertebrates as an extension to more ancient anterior brain regions. Another peculiarity of FoxG1 expression in lamprey, compared to other vertebrates, is that it is not expressed in the lamprey optic structures.

Arctic lamprey Lethenteron camtschaticum is an important and poorly studied component of the aquatic ecosystems in the Northern part of Eurasia. In this region, the species has two life history forms: anadromous and resident, which are very closely related genetically. In this review data on morphology, distribution, ecology, abundance, economic value and preservation of these two forms from the basins of the Barents, White, Kara, Laptev, East Siberian, Chukchi and Bering Seas are presented (over 70 rivers in 9 Russian watershed districts). For the first time, rigorous amounts of previously published and authors’ own experimental data, observations and Russian historical documents, normally unobtainable for English speaking researchers, have been comprehensively analyzed. The review leads to the understanding of the forms belonging to the same species.

Systematics of adult lampreys based on the “paired species” concept divides anadromous and residential specimens mostly on the size and size-depended criteria. Larvae of the paired species are poorly distinguished, so scientists keep looking for new diagnostic features. In the present paper structure and coloration of the tongue precursor in Arctic lamprey, Lethenteron camtschaticum, from the watersheds of the Russian Far East, including the species type locality are discussed. The data show that use of Tongue Precursor Pigmentation as a key for species identification is premature because tongue precursor within species inhabiting one river system or the same region demonstrates all types of coloration. Structure of tongue precursor changes from triangular into bulbous during growth.

Accumulated evidence indicates that the core genetic mechanisms regulating early patterning of the brain rudiment in vertebrates are very similar to those operating during development of the anterior region of invertebrate embryos. However, the mechanisms underlying the morphological differences between the elaborate vertebrate brain and its simpler invertebrate counterpart remain poorly understood. Recently, we hypothesized that the emergence of the most anterior unit of the vertebrate brain, the telencephalon, could be related to the appearance in vertebrates’ ancestors of a unique homeobox gene, Anf/Hesx1(further Anf), which is absent from all invertebrates and regulates the earliest steps of telencephalon development in vertebrates. However, the failure of Anf to be detected in one of the most basal extant vertebrate species, the lamprey, seriously compromises this hypothesis. Here, we report the cloning of Anf in three lamprey species and demonstrate that this gene is indeed expressed in embryos in the same pattern as in other vertebrates and executes the same functions by inhibiting the expression of the anterior general regulator Otx2 in favour of the telencephalic regulator FoxG1. These results are consistent with the hypothesis that the Anf homeobox gene may have been important in the evolution of the telencephalon.

This paper considers the major patterns of downstream migration in Arctic lamprey ammocoetes in Kamchatka rivers. Ammocoetes of different age groups are shown to be constantly noted in the composition of the migrant part of a river community. The greatest intensity of downstream migration in ammocoetes of the age class 0+ is noted in the period of their primary dispersion in late July-early August. The ammocoetes of the age groups 1+ and older migrate from spring to late autumn, but their concentrations are not high. The significant similarity of such a biologic feature as downstream migration in ammocoetes and juvenile salmonids serves as an example of ecological analogy.

Life history strategy has traditionally played an important role in the taxonomy of lampreys. In some cases, this was the basis for distinguishing socalled satellite species groups (1). Lamprey larvae within a satellite species group are morphologically identical; however, adult lampreys differ from one another in a number of species (primarily, the body length). It is believed that lampreys of some species migrate to large bodies of water (rivers, lakes, seas, and oceans) after metamorphosis, become parasites of bony fishes and begin to reproduce within 0.5-3 years, whereas lam� preys of other species remain in their native river, become mature within 6-10 months, and then die (1- 4). As a rule, a satellite species group comprises one parasitic anadromous species and several satellite resident species (nonparasitic or parasitic), which are assumed to have sympatrically originated from the first species (1, 4).