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As the only surviving lineages of jawless fishes, hagfishes and lampreys provide a crucial window into early vertebrate evolution 1 – 3 . Here we investigate the complex history, timing and functional role of genome-wide duplications 4 – 7 and programmed DNA elimination 8 , 9 in vertebrates in the light of a chromosome-scale genome sequence for the brown hagfish Eptatretus atami . Combining evidence from syntenic and phylogenetic analyses, we establish a comprehensive picture of vertebrate genome evolution, including an auto-tetraploidization (1R V ) that predates the early Cambrian cyclostome–gnathostome split, followed by a mid–late Cambrian allo-tetraploidization (2R JV ) in gnathostomes and a prolonged Cambrian–Ordovician hexaploidization (2R CY ) in cyclostomes. Subsequently, hagfishes underwent extensive genomic changes, with chromosomal fusions accompanied by the loss of genes that are essential for organ systems (for example, genes involved in the development of eyes and in the proliferation of osteoclasts); these changes account, in part, for the simplification of the hagfish body plan 1 , 2 . Finally, we characterize programmed DNA elimination in hagfish, identifying protein-coding genes and repetitive elements that are deleted from somatic cell lineages during early development. The elimination of these germline-specific genes provides a mechanism for resolving genetic conflict between soma and germline by repressing germline and pluripotency functions, paralleling findings in lampreys 10 , 11 . Reconstruction of the early genomic history of vertebrates provides a framework for further investigations of the evolution of cyclostomes and jawed vertebrates. A chromosome-scale genome assembly for the hagfish Eptatretus atami , combined with a series of phylogenetic analyses, sheds light on ancient polyploidization events that had a key role in the early evolution of vertebrates.

Cyclostomes, comprising jawless vertebrates such as lampreys and hagfishes, are the sister group of living jawed vertebrates (gnathostomes) and hence an important group for understanding the origin and diversity of vertebrates. In vertebrates and other metazoans, Hox genes determine cell fate along the anteroposterior axis of embryos and are implicated in driving morphological diversity. Invertebrates contain a single Hox cluster (either intact or fragmented), whereas elephant shark, coelacanth, and tetrapods contain four Hox clusters owing to two rounds of whole-genome duplication (“1R” and “2R”) during early vertebrate evolution. By contrast, most teleost fishes contain up to eight Hox clusters because of an additional “teleost-specific” genome duplication event. By sequencing bacterial artificial chromosome (BAC) clones and the whole genome, here we provide evidence for at least six Hox clusters in the Japanese lamprey (Lethenteron japonicum). This suggests that the lamprey lineage has experienced an additional genome duplication after 1R and 2R. The relative age of lamprey and human paralogs supports this hypothesis. Compared with gnathostome Hox clusters, lamprey Hox clusters are unusually large. Several conserved noncoding elements (CNEs) were predicted in the Hox clusters of lamprey, elephant shark, and human. Transgenic zebrafish assay indicated the potential of CNEs to function as enhancers. Interestingly, CNEs in individual lamprey Hox clusters are frequently conserved in multiple Hox clusters in elephant shark and human, implying a many-to-many orthology relationship between lamprey and gnathostome Hox clusters. Such a relationship suggests that the first two rounds of genome duplication may have occurred independently in the lamprey and gnathostome lineages.

All extant jawless vertebrates (lampreys and hagfishes) possess a unique adaptive immune system characterized by highly variable lymphocyte receptors (VLR) that are assembled in developing lymphocytes using leucine-rich-repeat donor cassettes. Five VLR types have been identified in lampreys: VLRA, VLRB, VLRC, VLRD, and VLRE. VLRB-expressing lymphocytes are functional analogs to B cells, whereas VLRA, VLRC, VLRD, and VLRE-expressing lymphocytes are more akin to T cells of jawed vertebrates. Here we define an additional VLR, designated VLRF. VLRF is phylogenetically closest to VLRA , with which it likely shares a common ancestral gene of at least 250 million years in the past. VLR assembly analyses show that VLRA , VLRC , VLRD , VLRE , and VLRF share donor cassettes through long-range intra- and inter-chromosomal interactions, whereas VLRB utilizes a distinct, dedicated cassette set. The pattern of gene expression, donor cassette usage, and distinctive amino acid composition in the C-terminal stalk suggest that VLRF⁺ lymphocytes may represent an additional T-like sub-lineage, adding further complexity to the VLR-based adaptive immune system. Extant jawless vertebrates, such as lampreys and hagfishes, express variable lymphocyte receptors (VLRs) that are different from adaptive immune receptors in mammals. Here, the authors show that, in addition to the well-described five VLRs, a sixth VLR is expressed in lamprey T-like cells and evolved at least 250 million years ago.

The human race faces many global to local challenges in the near future. Among these are massive biodiversity losses. The 2012 IUCN/SSC Red List reported evaluations of ~56 % of all vertebrates. This included 97 % of amphibians, mammals, birds, cartilaginous fishes, and hagfishes. It also contained evaluations of ~50 % of lampreys, ~38 % of reptiles, and ~29 % of bony fishes. A cursory examination of extinction magnitudes does not immediately reveal the severity of current biodiversity losses because the extinctions we see today have happened in such a short time compared to earlier events in the fossil record. So, we still must ask how current losses of species compare to losses in mass extinctions from the geological past. The most recent and best understood mass extinction is the Cretaceous terminal extinction which ends at the Cretaceous–Paleogene (K–Pg) border, 65 MYA. This event had massive losses of biodiversity (~17 % of families, >50 % of genera, and >70 % of species) and exterminated the dinosaurs. Extinction estimates for non-dinosaurian vertebrates at the K–Pg boundary range from 36 to 43 %. However, there remains much uncertainty regarding the completeness, preservation rates, and extinction magnitudes of the different classes of vertebrates. Fuzzy arithmetic was used to compare recent vertebrate extinction reported in the 2012 IUCN/SSC Red List with biodiversity losses at the end of K–Pg. Comparisons followed 16 different approaches to data compilation and 288 separate calculations. I tabulated the number of extant and extinct species (extinct + extinct in the wild), extant island endemics, data deficient species, and so-called impaired species [species with IUCN/SSC Red List designations from vulnerable (VU) to critically endangered (CR)]. Species that went extinct since 1500 and since 1980 were tabulated. Vertebrate extinction moved forward 24–85 times faster since 1500 than during the Cretaceous mass extinction. The magnitude of extinction has exploded since 1980, with losses about 71–297 times larger than during the K–Pg event. If species identified by the IUCN/SSC as critically endangered through vulnerable, and those that are data deficient are assumed extinct by geological standards, then vertebrate extinction approaches 8900–18,500 times the magnitude during that mass extinction. These extreme values and the great speed with which vertebrate biodiversity is being decimated are comparable to the devastation of previous extinction events. If recent levels of extinction were to continue, the magnitude is sufficient to drive these groups extinct in less than a century.

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.

Developing frameworks to identify knowledge gaps and prioritize research on diet studies in marine fish species is critical, as this knowledge is required for ecosystem-based management. We applied a framework in central Patagonia, Argentina, which faces a demand for gap assessments in diet knowledge and ecosystem management due to changes in marine fish assemblages' structure and function linked to industrial fishing and tropicalization. Our framework effectively identified gaps by examining the history of research efforts regarding spatial and temporal coverage, sampling sizes, fish life stages, and information quality of studies per species. We found critical gaps in local diet studies, particularly for mostly bony, Petromyzonti, and Myxini species, whereas elasmobranchs received the best coverage of the diet described. Most studies lack evaluation of ontogenetic diet changes and prey cumulative curves. Fixing these shortcomings improves research quality and reduces data uncertainties in community assessments. The prioritization framework identified high-priority species as those that require updated diet information, had shifted ranges, and lacked data. Our framework can be tailored to other biological traits and regions based on specific contextual needs to identify research gaps and priorities for fish assemblages impacted by global change while disseminating knowledge from diverse sources and languages.

Two rounds of whole-genome duplications are thought to have played an important role in the establishment of gene repertoires in vertebrates. These events occurred during chordate evolution after the split of the urochordate and cephalochordate lineages but before the radiation of extant gnathostomes (jawed vertebrates). During this interval, diverse agnathans (jawless fishes), including cyclostomes (hagfishes and lampreys), diverged. However, there is no solid evidence for the timing of these genome duplications in relation to the divergence of cyclostomes from the gnathostome lineage. We conducted cDNA sequencing in diverse early vertebrates for members of homeobox-containing (Dlx and ParaHox) and other gene families that would serve as landmarks for genome duplications. Including these new sequences, we performed a molecular phylogenetic census using the maximum likelihood method for 55 gene families. In most of these gene families, we detected many more gene duplications before the cyclostome-gnathostome split, than after. Many of these gene families (e.g., visual opsins, RAR, Notch) have multiple paralogs in conserved, syntenic genomic regions that must have been generated by large-scale duplication events. Taken together, this indicates that the genome duplications occurred before the cyclostome-gnathostome split. We propose that the redundancy in gene repertoires possessed by all vertebrates, including hagfishes and lampreys, was introduced primarily by genome duplications. Apart from subsequent lineage-specific modifications, these ancient genome duplication events might serve generally to distinguish vertebrates from invertebrates at the genomic level. [PUBLICATION ABSTRACT]

Background Hagfishes are fascinating creatures that typically inhabit the deep sea. The deep sea is characterized by its lack of sunlight, primary productivity, and diminishing biomass with increasing ocean depth. Therefore, hagfishes living in this environment must develop effective survival strategies to adapt to the limited food supply. Deep-sea hagfishes have been observed to survive without food intake for up to one year. In this study, we have assembled a high-quality somatic genome of the deep-sea hagfish ( Eptatretus okinoseanus ) captured below 1,000 m. We compared the genome of E. okinoseanus with the genomes of inshore hagfish, lampreys, and other related species to investigate the genetic factors underlying the deep-sea hagfish adaptations to the environment. Results The E. okinoseanus somatic genome was estimated to be 1.89 Gb and assembled into 17 pseudochromosomes. Phylogenetic analysis showed that shallow-sea and deep-sea hagfishes diverged approximately 58.8 million years ago. We found Perilipin gene family was significantly expanded in deep sea E. okinoseanus , which promotes triacylglycerol storage. Furthermore, a series of genes involved in fatty acid synthesis and metabolism, blood glucose regulation, and metabolic rate regulation were also expanded, rapid evolution or positive selection, and these changes contribute to their efficiency in energy utilization. Among these genes, the positively selected gene JNK may play an important role in energy metabolism. In addition, the olfactory receptors of the deep-sea hagfish were significantly expanded to 86, and three conserved motifs present only in hagfishes olfactory receptors were identified, which may facilitate the rapid localization of carrion. Conclusions This study provides valuable genomic resources for insights into the survival strategies of deep-sea hagfishes in oligotrophic environments.

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.

Jawed vertebrates (gnathostomes) have been the dominant lineage of deuterostomes for nearly three hundred fifty million years. Only a few lineages of jawless vertebrates remain in comparison. Composed of lampreys and hagfishes (cyclostomes), these jawless survivors are important systems for understanding the evolution of vertebrates. One focus of cyclostome research has been head skeleton development, as its evolution has been a driver of vertebrate morphological diversification. Recent work has identified hyaline-like cartilage in the oral cirri of the invertebrate chordate amphioxus, making cyclostomes critical for understanding the stepwise acquisition of vertebrate chondroid tissues. Our knowledge of cyclostome skeletogenesis, however, has lagged behind gnathostomes due to the difficulty of manipulating lamprey and hagfish embryos. In this review, we discuss and compare the regulation and histogenesis of cyclostome and gnathostome skeletal tissues. We also survey differences in skeletal morphology that we see amongst cyclostomes, as few elements can be confidently homologized between them. A recurring theme is the heterogeneity of skeletal morphology amongst living vertebrates, despite conserved genetic regulation. Based on these comparisons, we suggest a model through which these mesenchymal connective tissues acquired distinct histologies and that histological flexibility in cartilage existed in the last common ancestor of modern vertebrates.