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One of the central issues in evolutionary developmental biology is how we can formulate the relationships between evolutionary and developmental processes. Two major models have been proposed: the 'funnel-like' model, in which the earliest embryo shows the most conserved morphological pattern, followed by diversifying later stages, and the 'hourglass' model, in which constraints are imposed to conserve organogenesis stages, which is called the phylotypic period. Here we perform a quantitative comparative transcriptome analysis of several model vertebrate embryos and show that the pharyngula stage is most conserved, whereas earlier and later stages are rather divergent. These results allow us to predict approximate developmental timetables between different species, and indicate that pharyngula embryos have the most conserved gene expression profiles, which may be the source of the basic body plan of vertebrates. The conservation of embryonic development across species is of great interest in evolutionary biology. Here, using transcriptome analysis, the authors show that the pharyngula stage of development—in mid-embryogenesis—is conserved between mice, chickens, frogs and zebrafish.

The anterior end of the mammalian face is characteristically composed of a semimotile nose, not the upper jaw as in other tetrapods. Thus, the therian nose is covered ventrolaterally by the “premaxilla,” and the osteocranium possesses only a single nasal aperture because of the absence of medial bony elements. This stands in contrast to those in other tetrapods in whom the premaxilla covers the rostral terminus of the snout, providing a key to understanding the evolution of the mammalian face. Here, we show that the premaxilla in therian mammals (placentals and marsupials) is not entirely homologous to those in other amniotes; the therian premaxilla is a composite of the septomaxilla and the palatine remnant of the premaxilla of nontherian amniotes (including monotremes). By comparing topographical relationships of craniofacial primordia and nerve supplies in various tetrapod embryos, we found that the therian premaxilla is predominantly of the maxillary prominence origin and associated with mandibular arch. The rostral-most part of the upper jaw in nonmammalian tetrapods corresponds to the motile nose in therian mammals. During development, experimental inhibition of primordial growth demonstrated that the entire mammalian upper jaw mostly originates from the maxillary prominence, unlike other amniotes. Consistently, cell lineage tracing in transgenic mice revealed a mammalian-specific rostral growth of the maxillary prominence. We conclude that the mammalian-specific face, the muzzle, is an evolutionary novelty obtained by overriding ancestral developmental constraints to establish a novel topographical framework in craniofacial mesenchyme.

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 shoulder muscles of an early jawed vertebrate represent an intermediate evolutionary state. [Also see Report by Trinajstic et al. ] Most living vertebrates, from sharks to shrews and from hummingbirds to humans, are “jawed vertebrates,” distinguished by their possession of a jaw. These animals share other traits as well, such as two sets of paired appendages, shoulder girdles, and dual nostrils, revealing the basic anatomical architecture inherited from a common ancestor. Another group of vertebrates, the cyclostomes, comprises the two modern jawless vertebrates, lampreys and hagfish. These animals lack not only a jaw but also paired fins and shoulder girdles, showing that an even more ancient ancestor of vertebrates that gave rise to both the cyclostomes and jawed vertebrates also lacked these features. On page 160 this issue, Trinajstic et al. ( 1 ) systematically describe the muscle anatomy of three fossil animals from the earliest jawed vertebrate group, the placoderms, which evolved soon after the acquisition of the jaw.

The turtle body plan, with its solid shell, deviates radically from those of other tetrapods. The dorsal part of the turtle shell, or the carapace, consists mainly of costal and neural bony plates, which are continuous with the underlying thoracic ribs and vertebrae, respectively. Because of their superficial position, the evolutionary origins of these costo-neural elements have long remained elusive. Here we show, through comparative morphological and embryological analyses, that the major part of the carapace is derived purely from endoskeletal ribs. We examine turtle embryos and find that the costal and neural plates develop not within the dermis, but within deeper connective tissue where the rib and intercostal muscle anlagen develop. We also examine the fossils of an outgroup of turtles to confirm that the structure equivalent to the turtle carapace developed independently of the true osteoderm. Our results highlight the hitherto unravelled evolutionary course of the turtle shell. The evolutionary origins of the costal and neural bony plates of the turtle shell have long remained elusive. Here the authors show, through comparative morphological and embryological analyses, that the most of the carapace is derived from endoskeletal ribs.

Palaeospondylus gunni , from the Middle Devonian period, is one of the most enigmatic fossil vertebrates, and its phylogenetic position has remained unclear since its discovery in Scotland in 1890 (ref.  1 ). The fossil’s strange set of morphological features has made comparisons with known vertebrate morphotype diversity difficult. Here we use synchrotron radiation X-ray micro-computed tomography to show that Palaeospondylus was a sarcopterygian, and most probably a stem-tetrapod. The skeleton of Palaeospondylus consisted solely of endoskeletal elements in which hypertrophied chondrocyte cell lacunae, osteoids and a small fraction of perichondral bones developed. Despite the complete lack of teeth and dermal bones, the neurocranium of Palaeospondylus resembles those of stem-tetrapod Eusthenopteron 2 and Panderichthys 3 , and phylogenetic analyses place Palaeospondylus in between them. Because the unique features of Palaeospondylus , such as the cartilaginous skeleton and the absence of paired appendages, are present in the larva of crown tetrapods, our study highlights an unanticipated heterochronic evolution at the root of tetrapods. Detailed structural analysis of Palaeospondylus gunni from the Middle Devonian period shows strong resemblance to Eusthenopteron and Panderichthys , indicating that it was a sarcopterygian and most probably a stem-tetrapod.

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.

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.

Two major skeletal systems—the endoskeleton and exoskeleton—are recognized in vertebrate evolution. Here, we propose that these two systems are distinguished primarily by their relative positions, not by differences in embryonic histogenesis or cell lineage of origin. Comparative embryologic analyses have shown that both types of skeleton have changed their mode of histogenesis during evolution. Although exoskeletons were thought to arise exclusively from the neural crest, recent experiments in teleosts have shown that exoskeletons in the trunk are mesodermal in origin. The enameloid and dentine-coated postcranial exoskeleton seen in many vertebrates does not appear to represent an ancestral condition, as previously hypothesized, but rather a derived condition, in which the enameloid and dentine tissues became accreted to bones. Recent data from placoderm fossils are compatible with this scenario. In contrast, the skull contains neural crest-derived bones in its rostral part. Recent developmental studies suggest that the boundary between neural crest- and mesoderm-derived bones may not be consistent throughout evolution. Rather, the relative positions of bony elements may be conserved, and homologies of bony elements have been retained, with opportunistic changes in the mechanisms and cell lineages of development.

Modern cartilaginous fishes are divided into elasmobranchs (sharks, rays and skates) and chimaeras, and the lack of established whole-genome sequences for the former has prevented our understanding of early vertebrate evolution and the unique phenotypes of elasmobranchs. Here we present de novo whole-genome assemblies of brownbanded bamboo shark and cloudy catshark and an improved assembly of the whale shark genome. These relatively large genomes (3.8–6.7 Gbp) contain sparse distributions of coding genes and regulatory elements and exhibit reduced molecular evolutionary rates. Our thorough genome annotation revealed Hox C genes previously hypothesized to have been lost, as well as distinct gene repertories of opsins and olfactory receptors that would be associated with adaptation to unique underwater niches. We also show the early establishment of the genetic machinery governing mammalian homoeostasis and reproduction at the jawed vertebrate ancestor. This study, supported by genomic, transcriptomic and epigenomic resources, provides a foundation for the comprehensive, molecular exploration of phenotypes unique to sharks and insights into the evolutionary origins of vertebrates. Genomic resources for cartilaginous fishes are scarce. Here, the authors sequence the genome of three sharks and provide insights on the molecular basis of adaptation to underwater lifestyle and the evolutionary origins of vertebrates.