Lamprey Species Research Articles

Phylogeography of the European brook lamprey (Lampetra planeri) and the European river lamprey (Lampetra fluviatilis) species pair based on mitochondrial data.

The European river lamprey Lampetra fluviatilis and the European brook lamprey Lampetra planeri (Block 1784) are classified as a paired species, characterized by notably different life histories but morphological similarities. Previous work has further shown limited genetic differentiation between these two species at the mitochondrial DNA level. Here, we expand on this previous work, which focused on lamprey species from the Iberian Peninsula in the south and mainland Europe in the north, by sequencing three mitochondrial marker regions of Lampetra individuals from five river systems in Ireland and five in southern Italy. Our results corroborate the previously identified pattern of genetic diversity for the species pair. We also show significant genetic differentiation between Irish and mainland European lamprey populations, suggesting another ichthyogeographic district distinct from those previously defined. Finally, our results stress the importance of southern Italian L. planeri populations, which maintain several private alleles and notable genetic diversity.

An experimental study to evaluate predation threats on two native larval lampreys in the Columbia River Basin, USA

AbstractExperimental predation studies were conducted to evaluate and compare the predation threats of 10 species of native and non‐native fishes on larvae of Pacific Lamprey, Entosphenus tridentatus, and Western Brook Lamprey, Lampetra richardsoni. The relative predatory threats were examined over four sets of binary factors, including the following: (a) short (2‐day) or long (7‐day) duration, (b) presence/absence of fine sediment, (c) live or dead larvae and (d) species of lampreys. Our short‐term results showed a positive correlation with the sizes of predator fishes and consumed lamprey larvae. Also, most predator fishes had a significantly higher propensity to prey on lamprey larvae when sediment was absent. Conversely, this demonstrated the importance of sediment in protecting lamprey larvae from predation. Based on the predatory behaviour for live and dead larvae, predator fishes were classified into four groups using principal component analysis. Predation rates of larvae in sediment by piscivorous predators including Northern Pikeminnow Ptychocheilus oregonensis and Smallmouth Bass Micropterus dolomieu were lower and showed no differences even when the study duration was extended. In contrast, predation rates by benthic predators including White Sturgeon Acipenser transmontanus and Common Carp Cyprinus carpio, increased when we extended the study duration. This suggests that when given longer duration, benthic predators are more adept at consuming larvae within the sediment. These results provide important context for assessing the potential threat of predation on lampreys in streams, which is a key knowledge gap for lampreys.

Review of the lampreys (Petromyzontidae) in Bosnia and Herzegovina: a current status and geographic distribution

The general status of lampreys (family Petromyzontidae) in Bosnia and Herzegovina was reviewed to determine the species composition and geographical distribution of this group in the region. This paper reviews the available literature to provide a critical analysis of the current status of lamprey species. According to the available data, their status can be considered as indeterminate, largely due to limited published records. While eight species are recorded as present in the region (Eudontomyzon danfordi, E. mariae, E. vladykovi, Lampetra fluviatilis, L. planeri, L. soljani, Lethenteron zanandreai, Petromyzon marinus), only three species (E. vladykovi, L. soljani, P. marinus) are confirmed to occur. Their distribution is recorded in waters of both the Danube and the Adriatic Sea catchments. Given the deficiencies in our understanding of the taxonomic status of some populations and knowledge of the geographical distribution of lampreys inhabiting both catchments, research focused on improving understanding of the phylogenetic, morphological and phenotypic traits of lampreys in Bosnia and Herzegovina is warranted to resolve these uncertainties. Problems related to threats and conservation, and future perspectives for protective management strategies are discussed. This paper provides the context for future biodiversity conservation and management with regard to lamprey species in Bosnia and Herzegovina.

Descriptions of spawning of the pouched lamprey (Geotria australis) in tanks and of morphological changes leading up to and following spawning

The anadromous Geotria australis, one of only three lamprey species representing the early agnathan (jawless) stage of vertebrate evolution in Australia and New Zealand, is declining in abundance. Its adults were caught soon after they had entered rivers on their non-trophic upstream migration and maintained in laboratory tanks for 13–15 months through to spawning. As adult G. australis are susceptible to haemorrhagic septicaemia, they were treated prophylactically and maintained in 3-m3 aquaria supplied with a flow-through charcoal filtration system and UV steriliser. Air temperature and the light:dark regime were constantly adjusted to parallel those in the environment. Males developed the very large suctorial disc and gular pouch characteristic of maturity and both sexes matured at the same time as in the wild. While males frequently showed aggressive behaviour towards each other, the same male and female mated on several occasions. The male coiled around the female and, with his urogenital papilla close to the female’s cloaca, twisted and vibrated, leading to egg release. These eggs formed coagulated clusters as in the wild, with many progressing through to the eight-cell stage. Remarkably, numerous G. australis were still alive 95–392 days after the end of the short spawning period, and one male after a further 119 days. Postspawning survival would be facilitated inter alia by extensive proteolysis, reflected in a shortening of the body. The data in this paper emphasise that G. australis is a highly atypical lamprey and provides invaluable information for conserving this declining species.

Utilizing DNA metabarcoding to characterize the diet of marine-phase Arctic lamprey (Lethenteron camtschaticum) in the eastern Bering Sea

To understand the marine feeding ecology of Arctic lamprey (Lethenteron camtschaticum) in the eastern Bering Sea, visual observations and DNA metabarcoding of gut contents (N = 250) were used to characterize Arctic lamprey diet composition in 2014 and 2015. Differences among individual diets were evaluated by collection year, capture site, and fish size. Hard structures and tissues were observed during visual examinations of gut contents, and 10 ray-finned fish taxa were identified by DNA metabarcoding. The most frequently observed taxa included capelin (Mallotus villosus), Pacific herring (Clupea pallasii), Pacific sand lance (Ammodytes hexapterus), and gadids. Six taxa were reported for the first time as prey for Arctic lamprey. Individual diets differed between collection years, among capture sites, and among size classes; however, both collection year and size class explained only a small portion of diet variability (R2 = 0.01 and 0.04, respectively) relative to capture site (R2 = 0.49). These study results indicate that Arctic lamprey is a flesh-feeding species and highlight the value of DNA metabarcoding to characterize the diet of a poorly understood lamprey species.

Characterization and Evolution of Germ1, an Element that Undergoes Diminution in Lampreys (Cyclostomata: Petromyzontidae).

The sea lamprey (Petromyzon marinus) undergoes substantial genomic alterations during embryogenesis in which specific sequences are deleted from the genome of somatic cells yet retained in cells of the germ line. One element that undergoes diminution in P. marinus is Germ1, which consists of a somatically rare (SR) region and a fragment of 28S rDNA. Although the SR-region has been used as a marker for genomic alterations in lampreys, the evolutionary significance of its diminution is unknown. We examined the Germ1 element in five additional species of lamprey to better understand its evolutionary significance. Each representative species contained sequences similar enough to the Germ1 element of P. marinus to be detected via PCR and Southern hybridizations, although the SR-regions of Lampetra aepyptera and Lethenteron appendix are quite divergent from the homologous sequences of Petromyzon and three species of Ichthyomyzon. Lamprey Germ1 sequences have a number of features characteristic of the R2 retrotransposon, a mobile element that specifically targets 28S rDNA. Phylogenetic analyses of the SR-regions revealed patterns generally consistent with relationships among the species included in our study, although the 28S-fragments of each species/genus were most closely related to its own functional rDNA, suggesting that the two components of Germ1 were assembled independently in each lineage. Southern hybridizations showed evidence of genomic alterations involving Germ1 in each species. Our results suggest that Germ1 is a R2 retroelement that occurs in the genome of P. marinus and other petromyzontid lampreys, and that its diminution is incidental to the reduction in rDNA copies during embryogenesis.

Occurrence of pathogens in Pacific lamprey (Entosphenus tridentatus)

Pacific lamprey (Entosphenus tridentatus) is a First Food of Native Americans. Declines in lamprey abundance due to dam construction and habitat loss have curtailed traditional harvest opportunities. Artificial propagation is an emerging recovery tool for this imperiled species, and other lamprey species in Finland and Japan. To manage disease risk at prospective lamprey hatcheries, it is critical to understand the pathogens and parasites most likely to affect lamprey and other fish, both in culture and in the wild. We assembled data from regional fish health laboratories to assess pathogen prevalence in Pacific lamprey sampled from various sources (518 adults, 275 larvae, and one juvenile). In adults, Aeromonas salmonicida was identified using standard health screening methods in 0–69% of dead lamprey samples submitted, but no other pathogens were typically observed. All larvae were negative for bacterial and viral infections, and larvae experimentally exposed to A. salmonicida showed no infection or mortality. Conspicuously absent were detailed health assessments for metamorphosed larvae (juveniles). However, external examinations of over 20,000 juveniles captured at dams on the lower Columbia River indicated that they are susceptible to fungal infection in warm water conditions (> 12 °C), which can lead to mortality. To fully evaluate the disease risk associated with lamprey culture, directed research is needed along with standardized health screenings of lamprey at all life stages. Control of A. salmonicida, the etiological agent for furunculosis, will be a top priority for Pacific lamprey use, as this was the only pathogen regularly identified in this species.

Genomic sequence analyses of classical and non-classical lamprey progesterone receptor genes and the inference of homologous gene evolution in metazoans

BackgroundNuclear progesterone receptor (nPR) is an evolutionary innovation in vertebrates that mediates genomic responses to progesterone. Vertebrates also respond to progesterone via membrane progesterone receptors (mPRs) or membrane associated progesterone receptors (MAPRs) through rapid nongenomic mechanisms. Lampreys are extant agnathan vertebrates, residing at the evolutionary juncture where vertebrates diverged from invertebrates. A survey of the progesterone receptor (PR) gene sequences in lamprey genomes would inform PR gene evolutionary events during the transition from invertebrates to vertebrates.ResultsIn this study, we annotated sequences of one nPR, four mPR (β, γ, δ and ε) and four MAPR genes from genomes of two lamprey species (Petromyzon marinus and Lethenteron japonicum). To infer the origin and evolutionary history of PR genes, we constructed phylogenetic trees of PR homologous sequences across representative species of metazoans. Phylogenetic analyses revealed that the mPRγ gene first appeared in non-bilaterians, and the mPRβ gene likely arose from a duplication of mPRγ. On the other hand, the mPRγ gene gave rise to the mPRδ and ε genes much later in the vertebrate lineage. In addition, the mPRα gene first appeared in cartilaginous fishes, likely derived from duplication of mPRβ after the agnathan-gnathostome divergence. All known MAPR genes were present in the lamprey genomes. Progesterone receptor membrane component 1 (PGRMC1), neudesin and neuferricin genes probably evolved in parallel in non-bilaterians, whereas two copies of PGRMC genes probably derived from duplication of ancestral PGRMC1 sequence and appeared before the speciation of lampreys.ConclusionsNon-classical mPR and MAPR genes first evolved in non-bilaterians and classical nPR genes evolved later in basal vertebrates. Sequence repertoires for membrane progesterone receptor genes in vertebrates likely originated from an ancestral metazoan sequence and expanded via several duplication events.

Length‐based assessment of larval lamprey population structure at differing spatial scales

Abstract Perspectives on lamprey management contrast between pest control in the US Great Lakes and species conservation in the Pacific Northwest, New Zealand, and Europe. Five lamprey species are listed in the European Union (EU) Habitats Directive (HD) as requiring conservation measures. Assessments of HD ‘conservation status’ for these lampreys mainly target the larval (ammocoete) stage. Larval lamprey populations can be assessed by evaluating presence or absence, density and demographic structure in riverine samples. Demographic structure has typically been described from length–frequency data using qualitative approaches and the statistical assignment of age classes. Length‐based indicators (LBIs) may provide a more rapid and flexible framework. The demographic structure of a fish population can be described by univariate length metrics: length range (LRANGE) and 90th percentile of length (L90). This study used a pooled data set from seven Irish catchments to estimate a reference point (RP) value for each metric corresponding to a healthy larval lamprey population. Two LBIs were then derived that can be estimated for an observed (OBS) population as LBIRANGE = LRANGE_OBS/LRANGE_RP and LBI90 = L90_OBS/L90_RP. Simulated lamprey population length structures, representing a range of status values, were used to develop a reference gradient (RG) to support population assessment using LBIs. The assessment framework was applied to each of the seven Irish catchments, and also to subcatchment and sampling‐site scales within the Barrow system. The LBIs and RG suggested that most catchments had favourable conservation status overall, whereas smaller assessment scales revealed a spread of status values. The proposed framework allows the rapid assessment of demographic structure and comparison across systems. There is potential to track states across sampling sites, events, and legislative reporting cycles, and to interpret change in relation to the local environment. The general approach may be adaptable for other fish species monitored during juvenile stages.

Spiny Softshell (<i>Apalone spinifera</i>) turtles exhibit scarring consistent with attempted lamprey bites

We captured 46 Spiny Softshells (Apalone spinifera) during a mark–recapture study on Lake Erie (2012–2015). Six (13%) exhibited circular scars consistent with the bites of small parasitic lampreys. Two species of parasitic lampreys occur in Lake Erie: the invasive Sea Lamprey (Petromyzon marinus) and the native Silver Lamprey (Ichthyostomyzon unicuspis). The scars showed only the marks of the putative teeth surrounding the suctorial mouth, preventing identification based on the position of the supraoral teeth and suggesting that lampreys are rapidly dislodged from the turtles. To our knowledge, this is the first evidence of lampreys biting freshwater turtles.

New Red List assessments proposed for the recently described freshwater fish species in Greece

New Red List assessments proposed for the recently described freshwater fish species in Greece

Brook lampreys of life: towards holistic monitoring of boreal aquatic habitats using ‘subtle signs’ and oral histories

In this article the observation and spread of brook lamprey (Lampetra planeri) will be discussed as a bio-indicator and a ‘subtle sign’ in the boreal. Brook lamprey is a small non-parasitic freshwater lamprey species indicating good ecological health of aquatic habitats. This article presents knowledge co-produced through a 7-year monitoring programme in the south boreal catchment area of the Jukajoki River, North Karelia, Finland. Over the past one hundred years, this basin has been negatively affected by human land use. Monitoring methods employed as part of this programme have included both rigorous scientific sampling and large-scale traditional and local knowledge (TEK) monitoring. International long-running community monitoring efforts are assessed to position these Finnish traditional knowledge flows. Examples provide for the discussion of new monitoring and restoration methods of boreal aquatic habitats and contribute to the new realisation of these landscapes that were once hidden and now positioned to emerge, providing the suitable social-geographical space is present and accessible to allow for that.

Crowding reduces feeding rate, effectiveness of diet selection, and efficiency of digestion by Northern Brook Lamprey ammocetes (Ichthyomyzon fossor)

We studied the effect of larval density on food utilization by sediment-dwelling northern brook lamprey (Ichthyomyzon fossor) larvae in the Otter River, Baraga County, MI, USA using field surveys and in situ cage experiments. Field surveys found that food utilization was inversely proportional to density across the range of 1 to 10 larvae/m2. Compared to 1 larvae/m2, values at 10 larvae/m2 were lower by an average of 36% for gut fullness, by 32% for selective ingestion of organic matter, and by 71% and 58% for assimilation of diet organic matter and diet amino acids, respectively. In situ cage experiments and additional field studies in other nearby rivers revealed the same relationships. We hypothesize that physical disturbance of the sediment by adjacent larvae interferes with food utilization with the frequency of disturbance proportional to density. Condition factors were not correlated with density and indicate that individual larvae minimize the effect of crowding by moving away from higher density patches. We conclude that these findings are generalizable to other lamprey species in similar environments in which lower rates of growth, maturation, and survivorship of lamprey larvae at higher densities have been reported by other researchers.

Expansions, diversification, and interindividual copy number variations of AID/APOBEC family cytidine deaminase genes in lampreys

Cytidine deaminases of the AID/APOBEC family catalyze C-to-U nucleotide transitions in mRNA or DNA. Members of the APOBEC3 branch are involved in antiviral defense, whereas AID contributes to diversification of antibody repertoires in jawed vertebrates via somatic hypermutation, gene conversion, and class switch recombination. In the extant jawless vertebrate, the lamprey, two members of the AID/APOBEC family are implicated in the generation of somatic diversity of the variable lymphocyte receptors (VLRs). Expression studies linked CDA1 and CDA2 genes to the assembly of VLRA/C genes in T-like cells and the VLRB genes in B-like cells, respectively. Here, we identify and characterize several CDA1-like genes in the larvae of different lamprey species and demonstrate that these encode active cytidine deaminases. Structural comparisons of the CDA1 variants highlighted substantial differences in surface charge; this observation is supported by our finding that the enzymes require different conditions and substrates for optimal activity in vitro. Strikingly, we also found that the number of CDA-like genes present in individuals of the same species is variable. Nevertheless, irrespective of the number of different CDA1-like genes present, all lamprey larvae have at least one functional CDA1-related gene encoding an enzyme with predicted structural and chemical features generally comparable to jawed vertebrate AID. Our findings suggest that, similar to APOBEC3 branch expansion in jawed vertebrates, the AID/APOBEC family has undergone substantial diversification in lamprey, possibly indicative of multiple distinct biological roles.

Spatial Differences in the Distributions of Arctic and Pacific Lampreys in the Eastern Bering Sea

AbstractThe Arctic Lamprey Lethenteron camtschaticum and Pacific Lamprey Entosphenus tridentatus are ecologically and culturally valuable native species that co‐occur in the eastern Bering Sea. Lamprey wounds are often observed on fishes in this region, yet there is a paucity of information on the distribution of anadromous lampreys, lamprey–host interactions, and foraging behavior in the ocean. Our hypothesis was that each lamprey species would be positively associated (distribution and abundance) with their presumed hosts: Arctic Lampreys with smaller fishes that could easily be killed, and Pacific Lampreys with larger hosts that could sustain blood feeding. To examine lamprey distribution, abundance, and associations, we utilized data from two fishery‐independent surveys—one epipelagic trawl survey and one benthic trawl survey—conducted between 2002 and 2012 in the eastern Bering Sea. Distinct distributions of lamprey species were evident in models of their presence and absence by latitude and longitude. Arctic Lampreys inhabited the northern regions on the inner/middle continental shelf in depths less than 100 m, while Pacific Lampreys inhabited waters deeper than 150 m along the continental slope. Pacific Herring Clupea pallasii and juvenile salmonids were found in regions with relatively high Arctic Lamprey catches in the epipelagic trawl survey, and catches of lampreys and these potential hosts were positively correlated. Demersal groundfishes were found in regions with relatively high Pacific Lamprey abundance in the benthic trawl survey, but catches of Pacific Lampreys and these hosts were not consistent. We conclude that Arctic Lampreys and Pacific Lampreys are segregated in the eastern Bering Sea, and although differences in their distributions may be explained by species‐specific host preferences, alternate explanations include differences in seasonal movements, source river locations, and marine residence times. This study provides an initial baseline of the oceanic ecology of lampreys, which increases our understanding of species‐specific differences beyond traditional freshwater studies.

Hearing capabilities and behavioural response of sea lamprey (Petromyzon marinus) to low-frequency sounds

Hearing ability is well studied across teleost fishes in general, and vertebrates more broadly, but little is known about sound detection abilities of lampreys (Petromyzontiformes), a basal extant vertebrate group. The sea lamprey (Petromyzon marinus) is a destructive invader of the Laurentian Great Lakes, while numerous lamprey species (including the sea lamprey) are imperiled in their native ranges. In both management scenarios, behavioral manipulation tactics to control movement and distribution are desired. Therefore, we describe the hearing ability and behavioral responses of adult and juvenile sea lamprey to sound to reveal how hearing may have evolved in vertebrates and determine possible management applications. Based on auditory evoked potentials, sea lamprey detected tones of 50–300 Hz with equal sensitivity, but did not detect sounds above 300 Hz. In a laboratory bioassay, sea lamprey behaviorally responded to sound range of 50–200 Hz, with a general increase in swimming and a decrease in resting behaviours at both juvenile and adult stages relative to no-sound controls. To our knowledge, this is the first test of lamprey hearing, and the results support that sound may be a means to modify lamprey behaviour for management purposes.

First observations of spawning nests in the pouched lamprey (Geotria australis)

The pouched lamprey (Geotria australis), one of four Southern Hemisphere lamprey species, is New Zealand’s only freshwater representative of the agnathans. In contrast to that of Northern Hemisphere lampreys, the reproductive ecology of Southern Hemisphere lampreys is poorly understood, with no documented nesting sites or spawning behaviours. In the present study, we utilized passive integrated transponder tags to track migratory adult G. australis to locate spawning sites. Across 2 years, six cryptic nesting sites were discovered, each containing eggs and a single male and female lamprey. The postspawning pairs were all located underneath large boulders, with the eggs forming a coagulated cluster that adhered to the underside of the boulder. Both the male and female lamprey survived spawning for over 105 days. The observed spawning nests highlight a substantial divergence in the reproductive behaviour between Northern and Southern Hemisphere lampreys, as the present observations of G. australis are the first that support clustered cryptic egg deposition and an extended time to mortality postspawning. This study offers the first insights to the long-standing mystery of Southern Hemisphere lamprey reproduction.

Voltage-gated sodium channel gene repertoire of lampreys: gene duplications, tissue-specific expression and discovery of a long-lost gene.

Studies of the voltage-gated sodium (Nav) channels of extant gnathostomes have made it possible to deduce that ancestral gnathostomes possessed four voltage-gated sodium channel genes derived from a single ancestral chordate gene following two rounds of genome duplication early in vertebrates. We investigated the Nav gene family in two species of lampreys (the Japanese lamprey Lethenteron japonicum and sea lamprey Petromyzon marinus) (jawless vertebrates-agnatha) and compared them with those of basal vertebrates to better understand the origin of Nav genes in vertebrates. We noted six Nav genes in both lamprey species, but orthology with gnathostome (jawed vertebrate) channels was inconclusive. Surprisingly, the Nav2 gene, ubiquitously found in invertebrates and believed to have been lost in vertebrates, is present in lampreys, elephant shark (Callorhinchus milii) and coelacanth (Latimeria chalumnae). Despite repeated duplication of the Nav1 family in vertebrates, Nav2 is only in single copy in those vertebrates in which it is retained, and was independently lost in ray-finned fishes and tetrapods. Of the other five Nav channel genes, most were expressed in brain, one in brain and heart, and one exclusively in skeletal muscle. Invertebrates do not express Nav channel genes in muscle. Thus, early in the vertebrate lineage Nav channels began to diversify and different genes began to express in heart and muscle.

Rearing river lamprey Lampetra fluviatilis (L.) larvae under controlled conditions as a tool for restitution of endangered populations

A method for actively protecting river lamprey and increasing the number of river lamprey populations is presented as protocol of rearing stocking material. The objective of the study was to accommodate lamprey larvae during the most critical life period under controlled conditions until they reach a sufficient size, which will increase their chances to survive in the natural environment. The eggs obtained from wild breeders were incubated in Weiss’s jars at the water temperature of 12 °C. The larvae were reared in tanks set up in closed recirculating aquaculture systems. During the rearing period, the water temperature was 20 °C and the density of larvae was 150 individuals per 1 dm2 of bottom. In the initial rearing phase, the main focus was on the type of feeds and the nourishment method. It was determined that the most suitable feed type was Artemia nauplii combined with Hikari dry food. Additionally, the type of substrate was tested under controlled conditions. In this case, the optimum one was composed of sand of the grain size between 0.3 and 0.5 mm. The experiment proved that it is possible to successfully conduct river lamprey larvae rearing under controlled conditions. The growth rates are comparable to or better than those achieved under natural conditions. After 30 days of the rearing period, the lamprey larvae were 25 mm long. The results create a possibility to develop a technology for the restitution of river lamprey and other lamprey species, which are endangered throughout the world.

Presence of homeobox gene of Anf class in Pacific lamprey Lethenteron camtschaticum confirms the hypothesis about the importance of emergence of Anf genes for the origin of telencephalon in vertebrate evolution

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).