Modern Lampreys Research Articles

A new species of fossil lamprey (Petromyzontida: Petromyzontiformes) from Hebei, China

ABSTRACT A subclass of Mesozoic lamprey from Chengde, Hebei, China, Caeruleum miraculum gen. et sp. nov. is described. This new species has typical characteristics of another subclass of lamprey including an eel-like slender body, no paired appendages, absent jaws, round at anterior and laterally flat at posterior, and seven gill foramina, with anterior dorsal fin, posterior dorsal fin, and caudal fin. In addition, the total length of this species is between 240 mm (Table 1)-462 mm (Figure 4), which is 16.47 times the body depth, 4.01 times the head length, and 4.24 times the caudal length. Its body size is huge and very close to modern lampreys. This article briefly compared this species with the known Mesomyzon mengae. The discovery of these new fossils provides new evidence to study the evolution of Chinese lampreys during the Mesozoic and to explore the origin of modern lampreys.

N-terminal domain influences steroid activation of the Atlantic sea lamprey corticoid receptor

Lampreys are jawless fish that evolved about 550 million years ago at the base of the vertebrate line. Modern lampreys contain a corticoid receptor (CR), the common ancestor of the glucocorticoid receptor (GR) and mineralocorticoid receptor (MR), which first appear in cartilaginous fish, such as sharks. Until recently, 344 amino acids at the amino terminus of adult lamprey CR were not present in the lamprey CR sequence in GenBank. A search of the recently sequenced lamprey germline genome identified two CR sequences, CR1 and CR2, containing the 344 previously un-identified amino acids. CR1 also contains a novel four amino acid insertion in the DNA-binding domain (DBD). We studied corticosteroid and progesterone activation of CR1 and CR2 and found their strongest response was to 11-deoxycorticosterone and 11-deoxycortisol, the two circulating corticosteroids in lamprey. Based on steroid specificity, both CRs are close to elephant shark MR and distant from elephant shark GR. HEK293 cells that were transfected with full-length CR1 or CR2 and the MMTV promoter have about 3-fold higher steroid-mediated activation compared to HEK293 cells transfected with these CRs and the TAT3 promoter. Deletion of the amino-terminal domain (NTD) of lamprey CR1 and CR2 to form truncated CRs decreased transcriptional activation by about 70% in HEK293 cells that were transfected with MMTV, but increased transcription by about 6-fold in cells transfected with TAT3. This indicated that the promoter has an important effect on NTD regulation of transcriptional activation of the CR by steroids. Our results also indicate that the entire lamprey CR sequence is needed for an accurate determination of steroid-mediated transcription.

Thyroid and endostyle development in cyclostomes provides new insights into the evolutionary history of vertebrates

BackgroundThe endostyle is an epithelial exocrine gland found in non-vertebrate chordates (amphioxi and tunicates) and the larvae of modern lampreys. It is generally considered to be an evolutionary precursor of the thyroid gland of vertebrates. Transformation of the endostyle into the thyroid gland during the metamorphosis of lampreys is thus deemed to be a recapitulation of a past event in vertebrate evolution. In 1906, Stockard reported that the thyroid gland in hagfish, the sister cyclostome group of lampreys, develops through an endostyle-like primordium, strongly supporting the plesiomorphy of the lamprey endostyle. However, the findings in hagfish thyroid development were solely based on this single study, and these have not been confirmed by modern molecular, genetic, and morphological data pertaining to hagfish thyroid development over the last century.ResultsHere, we showed that the thyroid gland of hagfish undergoes direct development from the ventrorostral pharyngeal endoderm, where the previously described endostyle-like primordium was not found. The developmental pattern of the hagfish thyroid, including histological features and regulatory gene expression profiles, closely resembles that found in modern jawed vertebrates (gnathostomes). Meanwhile, as opposed to gnathostomes but similar to non-vertebrate chordates, lamprey and hagfish share a broad expression domain of Nkx2-1/2-4, a key regulatory gene, in the pharyngeal epithelium during early developmental stages.ConclusionsBased on the direct development of the thyroid gland both in hagfish and gnathostomes, and the shared expression profile of thyroid-related transcription factors in the cyclostomes, we challenge the plesiomorphic status of the lamprey endostyle and propose an alternative hypothesis where the lamprey endostyle could be obtained secondarily in crown lampreys.

Non-ammocoete larvae of Palaeozoic stem lampreys.

Ammocoetes-the filter-feeding larvae of modern lampreys-have long influenced hypotheses of vertebrate ancestry1-7. The life history of modern lampreys, whichdevelop from a superficially amphioxus-like ammocoete to a specialized predatory adult, appears to recapitulate widely accepted scenarios of vertebrate origin. However, no direct evidence has validated the evolutionary antiquity of ammocoetes, and their status as models of primitivevertebrate anatomy is uncertain. Here we report larval and juvenile forms of four stem lampreys from the Palaeozoic era (Hardistiella, Mayomyzon, Pipiscius, and Priscomyzon), including a hatchling-to-adult growth series of the genus Priscomyzon from Late Devonian Gondwana. Larvae of all four genera lack the defining traits of ammocoetes. They instead display features that are otherwise unique to adult modern lampreys, including prominent eyes, a cusped feeding apparatus, and posteriorly united branchial baskets. Notably, phylogenetic analyses find that these non-ammocoete larvae occur in at least three independent lineages of stem lamprey. This distribution strongly implies that ammocoetes are specializations of modern-lamprey life history rather than relics of vertebrate ancestry. These phylogenetic insights also suggest that the last common ancestor of hagfishes and lampreys was a macrophagous predator that did not have a filter-feeding larval phase. Thus, the armoured 'ostracoderms' that populate the cyclostome and gnathostome stems might serve as better proxies than living cyclostomes for the last common ancestor of all living vertebrates.

The evolution of lamprey (Petromyzontida) life history and the origin of metamorphosis

Modern lampreys (Petromyzontiformes) are one of two lineages of surviving jawless fishes (agnathans), and are thus of critical importance to understanding the evolution of the vertebrates. Although their fossil record is meager, it appears they have remained morphologically conserved for at least 360 million years, but the origin of their multi-stage life history is unclear. Unlike hagfishes, the other extant group of jawless fishes, which exhibit direct development, all modern lampreys possess a complex life cycle which includes a long-lived freshwater larval (or ammocoete) period, followed by a true metamorphosis into a sexually-immature juvenile and then mature adult which differ dramatically in their morphology and ecology from the larva. Because of their basal position, it is critical to understand when the extant lamprey life history evolved, and if such a life history was present in the last common ancestor of agnathans and gnathostomes. Recent discoveries in paleontology, genomic analyses, and developmental biology are providing insights into this problem. The current review synthesizes these findings and concludes that the ancestral lamprey life cycle followed a direct development. We suggest that the larval period was short and relatively limited if present at all, but that the juvenile included modern larval traits; over the course of evolution, differential selection pressures throughout the lifetime produced distinct larval and juvenile/adult periods. Each period required the dramatically different morphologies seen in modern lampreys, ultimately requiring a true metamorphosis to accommodate the large changes in the body plan and to maximize the efficiency of each life period. As a result, modern lamprey life histories are a patchwork of ancestral and derived characters.

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).

A lamprey from the Devonian period of South Africa

Lampreys are the most scientifically accessible of the remaining jawless vertebrates, but their evolutionary history is obscure. In contrast to the rich fossil record of armoured jawless fishes, all of which date from the Devonian period and earlier, only two Palaeozoic lampreys have been recorded, both from the Carboniferous period. In addition to these, the recent report of an exquisitely preserved Lower Cretaceous example demonstrates that anatomically modern lampreys were present by the late Mesozoic era. Here we report a marine/estuarine fossil lamprey from the Famennian (Late Devonian) of South Africa, the identity of which is established easily because many of the key specializations of modern forms are already in place. These specializations include the first evidence of a large oral disc, the first direct evidence of circumoral teeth and a well preserved branchial basket. This small agnathan, Priscomyzon riniensis gen. et sp. nov., is not only more conventionally lamprey-like than other Palaeozoic examples, but is also some 35 million years older. This finding is evidence that agnathans close to modern lampreys had evolved before the end of the Devonian period. In this light, lampreys as a whole appear all the more remarkable: ancient specialists that have persisted as such and survived a subsequent 360 million years.

Occurrence of two functionally distinct proopiomelanocortin genes in all modern lampreys

The lampreys (family Petromyzontidae) are divided into three subfamilies, the Petromyzontinae in the Northern Hemisphere and the Geotriinae and Mordaciinae in the Southern Hemisphere. We previously found two proopiomelanocortin subtypes, proopiocortin (POC) and proopiomelanotropin (POM) in sea lamprey, Petromyzon marinus (Petromyzontinae). POC encoding adrenocorticotropic hormone (ACTH) and β-endorphin (β-END) is expressed in the pars distalis of the pituitary, while POM encoding melanophore-stimulating hormone (MSH)-A and B together with a different β-END is expressed in the pars intermedia of the pituitary. All these hormonal segments are encoded on the third exon in both POC and POM. Here, we demonstrate the presence of both POC and POM genes in Geotria australis (Geotriinae) and Mordacia mordax (Mordaciinae) by molecular cloning of the third exons with the polymerase chain reaction using genomic DNA or pituitary cDNA. Molecular phylogenetic analysis showed that the POC and POM are distinctly different for the Southern Hemisphere lampreys as they are for P. marinus. Moreover, the relationship of each hormonal segments in POC and POM between Geotria, Mordacia, and Petromyzon is inconsistent. Immunocytochemical studies showed that the distribution of POC and POM in the pituitaries of the Southern Hemisphere lampreys is the same as that in the Northern Hemisphere. Taken together, these findings suggest that the duplication event which generated the two genes may have occurred in a common ancestor of the three extant lamprey subfamilies.

Head and backbone of the Early Cambrian vertebrate Haikouichthys.

Agnathan fish hold a key position in vertebrate evolution, especially regarding the origin of the head and neural-crest-derived tissue. In contrast to amphioxus, lampreys and other vertebrates possess a complex brain and placodes that contribute to well-developed eyes, as well as auditory and olfactory systems. These sensory sytems were arguably a trigger to subsequent vertebrate diversifications. However, although they are known from skeletal impressions in younger Palaeozoic agnathans, information about the earliest records of these systems has been largely wanting. Here we report numerous specimens of the Lower Cambrian vertebrate Haikouichthys ercaicunensis, until now only known from the holotype. Haikouichthys shows significant differences from other fossil agnathans: key features include a small lobate extension to the head, with eyes and possible nasal sacs, as well as what may be otic capsules. A notochord with separate vertebral elements is also identifiable. Phylogenetic analysis indicates that this fish lies within the stem-group craniates. Although Haikouichthys somewhat resembles the ammocoete larva of modern lampreys, this is because of shared general craniate characters; adult lampreys and hagfishes (the cyclostomes if monophyletic) are probably derived in many respects.

Origin and early evolution of the vertebrates: new insights from advances in molecular biology, anatomy, and palaeontology.

Recent advances in molecular biology and microanatomy have supported homologies of body parts between vertebrates and extant invertebrate chordates, thus providing insights into the body plan of the proximate ancestor of the vertebrates. For example, this ancestor probably had a relatively complex brain and a precursor of definitive neural crest. Additional insights into early vertebrate evolution have come from recent discoveries of Lower Cambrian soft body fossils of Haikouichthys and Myllokunmingia (almost certainly vertebrates, possibly related to modern lampreys) and Yunnanozoon and Haikouella (evidently stem-group vertebrates). The earliest vertebrates had an unequivocally marine origin, probably evolved mineralised pharyngeal denticles before the dermal skeleton, and evidently utilised elastic recoil of the visceral arch skeleton for suction feeding. Moreover, the new data emphasise that the advent of definitive neural crest was supremely important for the evolutionary origin of the vertebrates.

Evolutionary relationships among lamprey families: Amino acid composition analysis of lactate dehydrogenase

Modern lampreys are grouped into three families, with the Mordaciidae and Geotriidae restricted to the Southern hemisphere and Petromyzontidae occurring only in the Northern hemisphere. The evolutionary relationships among these families are uncertain. Amino acid composition analysis of lactate dehydrogenase purified from the lampreys Petromyzon marinus, Mordacia mordax and Geotria australis implies that the Petromyzontidae and Geotriidae share a more recent common ancestor than either does with the Mordaciidae.

Comments on the Classification and Nomenclature of Lampreys — An Alternative View

Current classifications of lampreys as reflected in this symposium are incongruent and unnecessarily split. It is suggested that modern lampreys be classified in one family, three subfamilies, and six genera. Most species are in a single genus Lampetra consisting of six subgenera. Intraspecific variation in dentition is greater than recognized previously. Reasons are given for use of the stem Petromyzont- for suprageneric names based on Petromyzon.Key words: taxonomy, terminology, morphology, lampreys