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Jawed vertebrates have inner ears with three semicircular canals, the presence of which has been used as a key to understanding evolutionary relationships. Ostracoderms, the jawless stem gnathostomes, had only two canals and lacked the lateral canal 1 – 3 . Lampreys, which are modern cyclostomes, are generally thought to possess two semicircular canals whereas the hagfishes—which are also cyclostomes—have only a single canal, which used to be regarded as a more primitive trait 1 , 4 . However, recent molecular and developmental analyses have strongly supported the monophyly of cyclostomes 5 – 7 , which has left the evolutionary trajectory of the vertebrate inner ear unclear 8 . Here we show the differentiation of the otic vesicle of the lamprey Lethenteron camtschaticum and inshore hagfish Eptatretus burgeri . This is the first time, to our knowledge, that the development of the hagfish inner ear is reported. We found that canal development in the lamprey starts with two depressions—which is reminiscent of the early developmental pattern of the inner ear in modern gnathostomes. These cyclostome otic vesicles show a pattern of expression of regulatory genes, including OTX genes, that is comparable to that of gnathosomes. Although two depressions appear in the lamprey vesicle, they subsequently fuse to form a single canal that is similar to that of hagfishes. Complete separation of the depressions results in anterior and posterior canals in gnathostomes. The single depression of the vesicle in hagfishes thus appears to be a secondarily derived trait. Furthermore, the lateral canal in crown gnathostomes was acquired secondarily—not by de novo acquisition of an OTX expression domain, but by the evolution of a developmental program downstream of the OTX genes. The differentiation of the inner ear in the lamprey Lethenteron camtschaticum and hagfish Eptatretus burgeri sheds light on the evolution of the semicircular canals of jawed vertebrates.

The brain of the hagfish, a cyclostome related to the lamprey, develops domains equivalent to the median ganglionic eminence and the rhombic lip, resembling the brains of gnathostomes (jawed vertebrates), suggesting that brain regionalization in jawed vertebrates occurred before the divergence of cyclostomes and gnathostomes more than 500 million years ago. The early vertebrate brain revisited The brains of vertebrates are much more complex than those of their immediate invertebrate relations — tunicates and the amphioxus — raising questions about the origins and development of the brain. The jawless lamprey, an ancient vertebrate, was also thought to have a primitive 'ancestral' brain. In particular, the embryonic lamprey was thought to have characteristics resembling those of mutant mice lacking a structure called the medial ganglionic eminence (MGE). Shigeru Kuratani and colleagues now show that the hagfish, a close relative of the lamprey, develops domains equivalent to the MGE and also the rhombic lip, resembling the brains of jawed vertebrates (gnathostomes). A closer look at lampreys reveals that they too have similar structures. These findings suggest that brain regionalization as seen in jawed vertebrates dates back to the latest vertebrate ancestor prior to the divergence of cyclostomes and gnathostomes more than 500 million years ago. The vertebrate brain is highly complex, but its evolutionary origin remains elusive. Because of the absence of certain developmental domains generally marked by the expression of regulatory genes, the embryonic brain of the lamprey, a jawless vertebrate, had been regarded as representing a less complex, ancestral state of the vertebrate brain. Specifically, the absence of a Hedgehog- and Nkx2.1 -positive domain in the lamprey subpallium was thought to be similar to mouse mutants in which the suppression of Nkx2-1 leads to a loss of the medial ganglionic eminence 1 , 2 . Here we show that the brain of the inshore hagfish ( Eptatretus burgeri ), another cyclostome group, develops domains equivalent to the medial ganglionic eminence and rhombic lip, resembling the gnathostome brain. Moreover, further investigation of lamprey larvae revealed that these domains are also present, ruling out the possibility of convergent evolution between hagfish and gnathostomes. Thus, brain regionalization as seen in crown gnathostomes is not an evolutionary innovation of this group, but dates back to the latest vertebrate ancestor before the divergence of cyclostomes and gnathostomes more than 500 million years ago.

As animals forage for food and water or evade predators, they must rapidly decide what visual features in the environment deserve attention. In vertebrates, this visuomotor computation is implemented within the neural circuits of the optic tectum (superior colliculus in mammals). However, the mechanisms by which tectum decides whether to approach or evade remain unclear, and also which neural mechanisms underlie this behavioral choice. To address this problem, we used an eye–brain–spinal cord preparation to evaluate how the lamprey responds to visual inputs with distinct stimulus-dependent motor patterns. Using ventral root activity as a behavioral readout, we classified 2 main types of fictive motor responses: (i) a unilateral burst response corresponding to orientation of the head toward slowly expanding or moving stimuli, particularly within the anterior visual field, and (ii) a unilateral or bilateral burst response triggering fictive avoidance in response to rapidly expanding looming stimuli or moving bars. A selective pharmacological blockade revealed that the brainstem-projecting neurons in the deep layer of the tectum in interaction with local inhibitory interneurons are responsible for selecting between these 2 visually triggered motor actions conveyed through downstream reticulospinal circuits. We suggest that these visual decision-making circuits had evolved in the common ancestor of vertebrates and have been conserved throughout vertebrate phylogeny.

The Argentinian pouched lamprey, classified as Petromyzon macrostomus Burmeister, 1868 was first described in 1867 in De La Plata River, in Buenos Aires, Argentina, and subsequently recorded in several rivers from Patagonia. Since its original description, the validity of P. macrostomus was questioned by several ichthyologists and 36 years after its original discovery it was considered a junior synonym of Geotria australis Gray, 1851. For a long time, the taxonomic status of G. australis has been uncertain, largely due to the misinterpretations of the morphological alterations that occur during sexual maturation, including the arrangement of teeth, size and position of fins and cloaca, and the development of an exceptionally large gular pouch in males. In this study, the taxonomic status of Geotria from across the \"species\" range was evaluated using both molecular analysis and examination of morphological characteristics. Phylogenetic and species delimitation analyses based on mitochondrial DNA sequences of Cytochrome b (Cyt b) and Cytochrome C Oxidase Subunit 1 (COI) genes, along with morphological analysis of diagnostic characters reported in the original descriptions of the species were used to assess genetic and morphological variation within Geotria and to determine the specific status of the Argentinian lamprey. These analyses revealed that Geotria from Argentina constitutes a well differentiated lineage from Chilean and Australasian populations. The position of the cloaca and the distance between the second dorsal and caudal fins in sub-adult individuals, and at previous life stages, can be used to distinguish between the two species. In addition, the genetic distance between G. macrostoma and G. australis for the COI and Cyt b mitochondrial genes is higher than both intra- and inter-specific distances reported for other Petromyzontiformes. Our results indicate that the Argentinian pouched lamprey, found along a broad latitudinal gradient on the south-west Atlantic coast of South America, should be named as Geotria macrostoma (Burmeister, 1868) and not as G. australis Gray 1851, returning to its earliest valid designation in Argentina. Geotria macrostoma can now be considered as the single lamprey species inhabiting Argentinian Patagonia, with distinct local adaptations and evolutionary potential. It is essential that this distinctiveness is recognized in order to guide future conservation and management actions against imminent threats posed by human actions in the major basins of Patagonia.

The lamprey's thymoid and vertebrate immunity The immune system of lampreys — jawless fish with roots in the early separation of the vertebrates into jawed and jawless lines — is of particular interest to evolutionary biologists. Much has been made of the differences between the 'alternative' immune system in the lamprey and that of today's jawed vertebrates, but the recent discovery that lampreys have lymphocytes resembling B and T cells, which are central to the adaptive immune response of the jawed vertebrates, puts more emphasis on the search for similarities. Histological surveys of lampreys have failed to reveal an organ equivalent to the mammalian thymus, the organ that generates the development of T lymphocytes. Now, gene expression analysis reveals previously unrecognized thymus-like structures — termed thymoids — at the tips of gill filaments of lamprey larvae. This suggests that the common ancestor of the jawed and jawless vertebrates may have had not only T- and B-like lymphocytes, but also anatomically distinct tissues for their development. Jawless fish were recently shown to possess T- and B-like lymphocytes expressing diverse assembled antigen receptors. This study identifies and characterizes lympho-epithelial thymus-like structures at the tips of gill filaments of lamprey larvae, thus providing evidence that the similarities underlying the adaptive immune systems of both types of vertebrate appear to extend to primary lymphoid organs. Immunologists and evolutionary biologists have been debating the nature of the immune system of jawless vertebrates—lampreys and hagfish—since the nineteenth century. In the past 50 years, these fish were shown to have antibody-like responses and the capacity to reject allografts 1 but were found to lack the immunoglobulin-based adaptive immune system of jawed vertebrates 2 . Recent work has shown that lampreys have lymphocytes that instead express somatically diversified antigen receptors that contain leucine-rich-repeats, termed variable lymphocyte receptors (VLRs) 3 , 4 , and that the type of VLR expressed is specific to the lymphocyte lineage: T-like lymphocytes express type A VLR ( VLRA ) genes, and B-like lymphocytes express VLRB genes 5 . These clonally diverse anticipatory antigen receptors are assembled from incomplete genomic fragments by gene conversion 6 , 7 , 8 , 9 , which is thought to be initiated by either of two genes encoding cytosine deaminase 9 , cytosine deaminase 1 ( CDA1 ) in T-like cells and CDA2 in B-like cells 5 . It is unknown whether jawless fish, like jawed vertebrates, have dedicated primary lymphoid organs, such as the thymus, where the development and selection of lymphocytes takes place 10 , 11 . Here we identify discrete thymus-like lympho-epithelial structures, termed thymoids, in the tips of the gill filaments and the neighbouring secondary lamellae (both within the gill basket) of lamprey larvae. Only in the thymoids was expression of the orthologue of the gene encoding forkhead box N1 (FOXN1) 10 , a marker of the thymopoietic microenvironment in jawed vertebrates 12 , accompanied by expression of CDA1 and VLRA . This expression pattern was unaffected by immunization of lampreys or by stimulation with a T-cell mitogen. Non-functional VLRA gene assemblies were found frequently in the thymoids but not elsewhere, further implicating the thymoid as the site of development of T-like cells in lampreys. These findings suggest that the similarities underlying the dual nature of the adaptive immune systems in the two sister groups of vertebrates extend to primary lymphoid organs.

Cyclostomes, the living jawless vertebrates including hagfishes and lampreys, represent the most basal lineage of vertebrates. Although the monophyly of cyclostomes has been supported by recent molecular analyses, the phenotypic traits of hagfishes, especially the lack of some vertebrate-defining features and the reported endodermal origin of the adenohypophysis, have been interpreted as hagfishes exhibiting a more ancestral state than those of all other vertebrates. Furthermore, the adult anatomy of hagfishes cannot be compared easily with that of lampreys. Here we describe the craniofacial development of a series of staged hagfish embryos, which shows that their adenohypophysis arises ectodermally, consistent with the molecular phylogenetic data. This finding also allowed us to identify a pan-cyclostome pattern, one not shared by jawed vertebrates. Comparative analyses indicated that many of the hagfish-specific traits can be explained by changes secondarily introduced into the hagfish lineage. We also propose a possibility that the pan-cyclostome pattern may reflect the ancestral programme for the craniofacial development of all living vertebrates. An analysis of staged hagfish embryos shows that the hagfish adenohypophysis is ectodermal in origin, revealing it to be a developmental quirk unique to hagfishes that was hitherto misleading; from this and other observations a ‘pan-cyclostome’ developmental pattern is derived, indicating that it was primitive for all vertebrates. The face of early vertebrate evolution The hagfish is the most primitive extant vertebrate. Its anatomy and development hold clues to understanding the evolution of that most enigmatic of structures, the vertebrate head. Hagfish embryos are notoriously hard to obtain, but a few years ago Shigeru Kuratani and colleagues managed to prepare some, and — for the first time since 1899 — significant work on hagfish embryology began. This paper presents the first detailed report on the craniofacial development of a hagfish species, Eptatretus burgeri . The authors identify an embryonic development pattern shared only by the jawless lampreys and hagfish that may have been primitive for all vertebrates.

Studies of the head of the very primitive jawed vertebrate Romundina show that it combines jawed vertebrate architecture with cranial and cerebral proportions resembling those of extant jawless vertebrates such as lampreys. The jawless-to-jawed transition The development of jawed vertebrates from jawless fishes required more than just the addition of jaw to a jawless head — it necessitated a thorough reorganization of the skull morphology. Extant jawed vertebrates are so different from jawless ones (lampreys and hagfishes) that it is hard to see how this might have come about. Studies on a very primitive jawed vertebrate — the fossil placoderm fish Romundina — provide a glimpse of how that transition could have occurred. Vincent Dupret et al . show that the head of Romundina combines jawed vertebrate architecture with cranial and cerebral proportions resembling those of extant jawless vertebrates such as lampreys and some fossil jawless fishes. This combination appears to be primitive for jawed vertebrates and differs fundamentally from the morphology of sharks, traditionally used as a model for a generalized jawed vertebrate. Extant vertebrates form two clades, the jawless Cyclostomata (lampreys and hagfishes) and the jawed Gnathostomata (all other vertebrates), with contrasting facial architectures 1 , 2 . These arise during development from just a few key differences in the growth patterns of the cranial primordia: notably, the nasal sacs and hypophysis originate from a single placode in cyclostomes but from separate placodes in gnathostomes, and infraoptic ectomesenchyme migrates forward either side of the single placode in cyclostomes but between the placodes in gnathostomes 3 , 4 , 5 , 6 , 7 , 8 . Fossil stem gnathostomes preserve cranial anatomies rich in landmarks that provide proxies for developmental processes and allow the transition from jawless to jawed vertebrates to be broken down into evolutionary steps 7 , 9 , 10 , 11 , 12 . Here we use propagation phase contrast synchrotron microtomography to image the cranial anatomy of the primitive placoderm (jawed stem gnathostome) Romundina 13 , and show that it combines jawed vertebrate architecture with cranial and cerebral proportions resembling those of cyclostomes and the galeaspid (jawless stem gnathostome) Shuyu 11 . This combination seems to be primitive for jawed vertebrates, and suggests a decoupling between ectomesenchymal growth trajectory, ectomesenchymal proliferation, and cerebral shape change during the origin of gnathostomes.

The neurocranium is an integral part of the vertebrate head, itself a major evolutionary innovation 1 , 2 . However, its early history remains poorly understood, with great dissimilarity in form between the two living vertebrate groups: gnathostomes (jawed vertebrates) and cyclostomes (hagfishes and lampreys) 2 , 3 . The 100 Myr gap separating the Cambrian appearance of vertebrates 4 – 6 from the earliest three-dimensionally preserved vertebrate neurocrania 7 further obscures the origins of modern states. Here we use computed tomography to describe the cranial anatomy of an Ordovician stem-group gnathostome: Eriptychius americanus from the Harding Sandstone of Colorado, USA 8 . A fossilized head of Eriptychius preserves a symmetrical set of cartilages that we interpret as the preorbital neurocranium, enclosing the fronts of laterally placed orbits, terminally located mouth, olfactory bulbs and pineal organ. This suggests that, in the earliest gnathostomes, the neurocranium filled out the space between the dermal skeleton and brain, like in galeaspids, osteostracans and placoderms and unlike in cyclostomes 2 . However, these cartilages are not fused into a single neurocranial unit, suggesting that this is a derived gnathostome trait. Eriptychius fills a major temporal and phylogenetic gap in our understanding of the evolution of the gnathostome head, revealing a neurocranium with an anatomy unlike that of any previously described vertebrate. Computed tomography reveals that the cranial anatomy of Ordovician stem-group gnathostome Eriptychius americanus from the Harding Sandstone of Colorado, USA, is distinct among vertebrates.

The success of vertebrates is linked to the evolution of a camera-style eye and sophisticated visual system. In the absence of useful data from fossils, scenarios for evolutionary assembly of the vertebrate eye have been based necessarily on evidence from development, molecular genetics and comparative anatomy in living vertebrates. Unfortunately, steps in the transition from a light-sensitive ‘eye spot’ in invertebrate chordates to an image-forming camera-style eye in jawed vertebrates are constrained only by hagfish and lampreys (cyclostomes), which are interpreted to reflect either an intermediate or degenerate condition. Here, we report—based on evidence of size, shape, preservation mode and localized occurrence—the presence of melanosomes (pigment-bearing organelles) in fossil cyclostome eyes. Time of flight secondary ion mass spectrometry analyses reveal secondary ions with a relative intensity characteristic of melanin as revealed through principal components analyses. Our data support the hypotheses that extant hagfish eyes are degenerate, not rudimentary, that cyclostomes are monophyletic, and that the ancestral vertebrate had a functional visual system. We also demonstrate integument pigmentation in fossil lampreys, opening up the exciting possibility of investigating colour patterning in Palaeozoic vertebrates. The examples we report add to the record of melanosome preservation in Carboniferous fossils and attest to surprising durability of melanosomes and biomolecular melanin.

The optic tectum (called superior colliculus in mammals) is critical for eye–head gaze shifts as we navigate in the terrain and need to adapt our movements to the visual scene. The neuronal mechanisms underlying the tectal contribution to stimulus selection and gaze reorientation remains, however, unclear at the microcircuit level. To analyze this complex—yet phylogenetically conserved—sensorimotor system, we developed a novel in vitro preparation in the lamprey that maintains the eye and midbrain intact and allows for whole-cell recordings from prelabeled tectal gaze-controlling cells in the deep layer, while visual stimuli are delivered. We found that receptive field activation of these cells provide monosynaptic retinal excitation followed by local GABAergic inhibition (feedforward). The entire remaining retina, on the other hand, elicits only inhibition (surround inhibition). If two stimuli are delivered simultaneously, one inside and one outside the receptive field, the former excitatory response is suppressed. When local inhibition is pharmacologically blocked, the suppression induced by competing stimuli is canceled. We suggest that this rivalry between visual areas across the tectal map is triggered through long-range inhibitory tectal connections. Selection commands conveyed via gaze-controlling neurons in the optic tectum are, thus, formed through synaptic integration of local retinotopic excitation and global tectal inhibition. We anticipate that this mechanism not only exists in lamprey but is also conserved throughout vertebrate evolution. Significance Neurons in the optic tectum are involved in stimulus selection and also control gaze reorientation. This study relies on an in vitro preparation that allows visual activation of the retina while providing accessibility for whole-cell recordings from specific cells that control gaze action. We show the tectal (collicular in mammals) GABAergic interneurons generate rivalry between visual areas and that tectal gaze-controlling cells integrate this inhibition along with local retinal excitation to form stimulus selection commands that will move the eyes and head, and may also contribute to edge detection. We propose that this subcortical visuomotor circuit is phylogenetically conserved throughout vertebrate evolution.