The rise of predation in Jurassic lampreys.

Lampreys, one of two living lineages of jawless vertebrates, are always intriguing for their feeding behavior via the toothed suctorial disc and life cycle comprising the ammocoete, metamorphic, and adult stages. However, they left a meager fossil record, and their evolutionary history remains elusive. Here we report two superbly preserved large lampreys from the Middle-Late Jurassic Yanliao Biota of North China and update the interpretations of the evolution of the feeding apparatus, the life cycle, and the historic biogeography of the group. These fossil lampreys' extensively toothed feeding apparatus differs radically from that of their Paleozoic kin but surprisingly resembles the Southern Hemisphere pouched lamprey, which foreshadows an ancestral flesh-eating habit for modern lampreys. Based on the revised petromyzontiform timetree, we argued that modern lampreys' three-staged life cycle might not be established until the Jurassic when they evolved enhanced feeding structures, increased body size and encountered more penetrable host groups. Our study also places modern lampreys' origin in the Southern Hemisphere of the Late Cretaceous, followed by an early Cenozoic anti-tropical disjunction in distribution, hence challenging the conventional wisdom of their biogeographical pattern arising from a post-Cretaceous origin in the Northern Hemisphere or the Pangean fragmentation in the Early Mesozoic.

Neurocranial development of the coelacanth and the evolution of the sarcopterygian head.

The neurocranium of sarcopterygian fishes was originally divided into an anterior (ethmosphenoid) and posterior (otoccipital) portion by an intracranial joint, and underwent major changes in its overall geometry before fusing into a single unit in lungfishes and early tetrapods1. Although the pattern of these changes is well-documented, the developmental mechanisms that underpin variation in the form of the neurocranium and its associated soft tissues during the evolution of sarcopterygian fishes remain poorly understood. The coelacanth Latimeria is the only known living vertebrate that retains an intracranial joint2,3. Despite its importance for understanding neurocranial evolution, the development of the neurocranium of this ovoviviparous fish remains unknown. Here we investigate the ontogeny of the neurocranium and brain in Latimeria chalumnae using conventional and synchrotron X-ray micro-computed tomography as well as magnetic resonance imaging, performed on an extensive growth series for this species. We describe the neurocranium at the earliest developmental stage known for Latimeria, as well as the major changes that the neurocranium undergoes during ontogeny. Changes in the neurocranium are associated with an extreme reduction in the relative size of the brain along with an enlargement of the notochord. The development of the notochord appears to have a major effect on the surrounding cranial components, and might underpin the formation of the intracranial joint. Our results shed light on the interplay between the neurocranium and its adjacent soft tissues during development in Latimeria, and provide insights into the developmental mechanisms that are likely to have underpinned the evolution of neurocranial diversity in sarcopterygian fishes.

The homology and function of the lung plates in extant and fossil coelacanths.

The presence of a pulmonary organ that is entirely covered by true bone tissue and fills most of the abdominal cavity is hitherto unique to fossil actinistians. Although small hard plates have been recently reported in the lung of the extant coelacanth Latimeria chalumnae, the homology between these hard structures in fossil and extant forms remained to be demonstrated. Here, we resolve this question by reporting the presence of a similar histological pattern-true cellular bone with star-shaped osteocytes, and a globular mineralisation with radiating arrangement-in the lung plates of two fossil coelacanths (Swenzia latimerae and Axelrodichthys araripensis) and the plates that surround the lung of the most extensively studied extant coelacanth species, L. chalumnae. The point-for-point structural similarity of the plates in extant and fossil coelacanths supports their probable homology and, consequently, that of the organ they surround. Thus, this evidence questions the previous interpretations of the fatty organ as a component of the pulmonary complex of Latimeria.

Allometric growth in the extant coelacanth lung during ontogenetic development.

Coelacanths are lobe-finned fishes known from the Devonian to Recent that were long considered extinct, until the discovery of two living species in deep marine waters of the Mozambique Channel and Sulawesi. Despite extensive studies, the pulmonary system of extant coelacanths has not been fully investigated. Here we confirm the presence of a lung and discuss its allometric growth in Latimeria chalumnae, based on a unique ontogenetic series. Our results demonstrate the presence of a potentially functional, well-developed lung in the earliest known coelacanth embryo, and its arrested growth at later ontogenetic stages, when the lung is clearly vestigial. The parallel development of a fatty organ for buoyancy control suggests a unique adaptation to deep-water environments. Furthermore, we provide the first evidence for the presence of small, hard, flexible plates around the lung in L. chalumnae, and consider them homologous to the plates of the 'calcified lung' of fossil coelacanths.

Facts and fancies about early fossil chordates and vertebrates.

The interrelationships between major living vertebrate, and even chordate, groups are now reasonably well resolved thanks to a large amount of generally congruent data derived from molecular sequences, anatomy and physiology. But fossils provide unexpected combinations of characters that help us to understand how the anatomy of modern groups was progressively shaped over millions of years. The dawn of vertebrates is documented by fossils that are preserved as either soft-tissue imprints, or minute skeletal fragments, and it is sometimes difficult for palaeontologists to tell which of them are reliable vertebrate remains and which merely reflect our idea of an ancestral vertebrate.

Duplications of hox gene clusters and the emergence of vertebrates.

The vertebrate body plan is characterized by an increased complexity relative to that of all other chordates and large-scale gene amplifications have been associated with key morphological innovations leading to their remarkable evolutionary success. Here, we use compound full Hox clusters deletions to investigate how Hox genes duplications may have contributed to the emergence of vertebrate-specific innovations. We show that the combined deletion of HoxA and HoxB leads to an atavistic heart phenotype, suggesting that the ancestral HoxA/B cluster was co-opted to help in diversifying the complex organ in vertebrates. Other phenotypic effects observed seem to illustrate the resurgence of ancestral (plesiomorphic) features. This indicates that the duplications of Hox clusters were associated with the recruitment or formation of novel cis-regulatory controls, which were key to the evolution of many vertebrate features and hence to the evolutionary radiation of this group.

The buccohypophyseal canal is an ancestral vertebrate trait maintained by modulation in sonic hedgehog signaling.

BACKGROUND: The pituitary gland is formed by the juxtaposition of two tissues: neuroectoderm arising from the basal diencephalon, and oral epithelium, which invaginates towards the central nervous system from the roof of the mouth. The oral invagination that reaches the brain from the mouth is referred to as Rathke's pouch, with the tip forming the adenohypophysis and the stalk disappearing after the earliest stages of development. In tetrapods, formation of the cranial base establishes a definitive barrier between the pituitary and oral cavity; however, numerous extinct and extant vertebrate species retain an open buccohypophyseal canal in adulthood, a vestige of the stalk of Rathke's pouch. Little is currently known about the formation and function of this structure. Here we have investigated molecular mechanisms driving the formation of the buccohypophyseal canal and their evolutionary significance. RESULTS: We show that Rathke's pouch is located at a boundary region delineated by endoderm, neural crest-derived oral mesenchyme and the anterior limit of the notochord, using CD1, R26R-Sox17-Cre and R26R-Wnt1-Cre mouse lines. As revealed by synchrotron X-ray microtomography after iodine staining in mouse embryos, the pouch has a lobulated three-dimensional structure that embraces the descending diencephalon during pituitary formation. Polaris(fl/fl); Wnt1-Cre, Ofd1(-/-) and Kif3a(-/-) primary cilia mouse mutants have abnormal sonic hedgehog (Shh) signaling and all present with malformations of the anterior pituitary gland and midline structures of the anterior cranial base. Changes in the expressions of Shh downstream genes are confirmed in Gas1(-/-) mice. From an evolutionary perspective, persistence of the buccohypophyseal canal is a basal character for all vertebrates and its maintenance in several groups is related to a specific morphology of the midline that can be related to modulation in Shh signaling. CONCLUSION: These results provide insight into a poorly understood ancestral vertebrate structure. It appears that the opening of the buccohypophyseal canal depends upon Shh signaling and that modulation in this pathway most probably accounts for its persistence in phylogeny.

The giant cretaceous Coelacanth (Actinistia, Sarcopterygii) Megalocoelacanthus dobiei Schwimmer, Stewart & Williams, 1994, and its bearing on Latimerioidei interrelationships.

We present a redescription of Megalocoelacanthus dobiei, a giant fossil coelacanth from Upper Cretaceous strata of North America. Megalocoelacanthus has been previously described on the basis of composite material that consisted of isolated elements. Consequently, many aspects of its anatomy have remained unknown as well as its phylogenetic relationships with other coelacanths. Previous studies have suggested that Megalocoelacanthus is closer to Latimeria and Macropoma than to Mawsonia. However, this assumption was based only on the overall similarity of few anatomical features, rather than on a phylogenetic character analysis. A new, and outstandingly preserved specimen from the Niobrara Formation in Kansas allows the detailed description of the skull of Megalocoelacanthus and elucidation of its phylogenetic relationships with other coelacanths. Although strongly flattened, the skull and jaws are well preserved and show many derived features that are shared with Latimeriidae such as Latimeria, Macropoma and Libys. Notably, the parietonasal shield is narrow and flanked by very large, continuous vacuities forming the supraorbital sensory line canal. Such an unusual morphology is also known in Libys. Some other features of Megalocoelacanthus, such as its large size and the absence of teeth are shared with the mawsoniid genera Mawsonia and Axelrodichthys. Our cladistic analysis supports the sister-group relationship of Megalocoelacanthus and Libys within Latimeriidae. This topology suggests that toothless, large-sized coelacanths evolved independently in both Latimeriidae and Mawsoniidae during the Mesozoic. Based on previous topologies and on ours, we then review the high-level taxonomy of Latimerioidei and propose new systematic phylogenetic definitions.

A new paleozoic Symmoriiformes (Chondrichthyes) from the late Carboniferous of Kansas (USA) and cladistic analysis of early chondrichthyans.

BACKGROUND: The relationships of cartilaginous fishes are discussed in the light of well preserved three-dimensional Paleozoic specimens. There is no consensus to date on the interrelationship of Paleozoic chondrichthyans, although three main phylogenetic hypotheses exist in the current literature: 1. the Paleozoic shark-like chondrichthyans, such as the Symmoriiformes, are grouped along with the modern sharks (neoselachians) into a clade which is sister group of holocephalans; 2. the Symmoriiformes are related to holocephalans, whereas the other Paleozoic shark-like chondrichthyans are related to neoselachians; 3. many Paleozoic shark-like chondrichthyans, such as the Symmoriiformes, are stem chondrichthyans, whereas stem and crown holocephalans are sister group to the stem and crown neoselachians in a crown-chondrichthyan clade. This third hypothesis was proposed recently, based mainly on dental characters. METHODOLOGY/PRINCIPAL FINDINGS: On the basis of two well preserved chondrichthyan neurocrania from the Late Carboniferous of Kansas, USA, we describe here a new species of Symmoriiformes, Kawichthys moodiei gen. et sp. nov., which was investigated by means of computerized X-ray synchrotron microtomography. We present a new phylogenetic analysis based on neurocranial characters, which supports the third hypothesis and corroborates the hypothesis that crown-group chondrichthyans (Holocephali+Neoselachii) form a tightly-knit group within the chondrichthyan total group, by providing additional, non dental characters. CONCLUSIONS/SIGNIFICANCE: Our results highlight the importance of new well preserved Paleozoic fossils and new techniques of observation, and suggest that a new look at the synapomorphies of the crown-group chondrichthyans would be worthwhile in terms of understanding the adaptive significance of phylogenetically important characters.

Comparative anatomy: all vertebrates do have vertebrae.

In contrast to lampreys and jawed vertebrates, hagfishes were thought to lack vertebrae. Now, long overlooked vertebral rudiments have been analysed in hagfish, suggesting that vertebrae existed in the last common ancestor of all vertebrates.

Fossil jawless fish from China foreshadows early jawed vertebrate anatomy.

Most living vertebrates are jawed vertebrates (gnathostomes), and the living jawless vertebrates (cyclostomes), hagfishes and lampreys, provide scarce information about the profound reorganization of the vertebrate skull during the evolutionary origin of jaws. The extinct bony jawless vertebrates, or 'ostracoderms', are regarded as precursors of jawed vertebrates and provide insight into this formative episode in vertebrate evolution. Here, using synchrotron radiation X-ray tomography, we describe the cranial anatomy of galeaspids, a 435-370-million-year-old 'ostracoderm' group from China and Vietnam. The paired nasal sacs of galeaspids are located anterolaterally in the braincase, and the hypophyseal duct opens anteriorly towards the oral cavity. These three structures (the paired nasal sacs and the hypophyseal duct) were thus already independent of each other, like in gnathostomes and unlike in cyclostomes and osteostracans (another 'ostracoderm' group), and therefore have the condition that current developmental models regard as prerequisites for the development of jaws. This indicates that the reorganization of vertebrate cranial anatomy was not driven deterministically by the evolutionary origin of jaws but occurred stepwise, ultimately allowing the rostral growth of ectomesenchyme that now characterizes gnathostome head development.

Teeth before jaws? Comparative analysis of the structure and development of the external and internal scales in the extinct jawless vertebrate Loganellia scotica.

Traditional hypotheses posit that teeth evolved from dermal scales, through the expansion of odontogenetically competent ectoderm into the mouth of jawless vertebrates. The discovery of tooth-like scales inside thelodonts, an extinct group of jawless vertebrates, led to the alternative hypothesis that teeth evolved from endodermal derivatives and that there exists a fundamental developmental and phylogenetic distinction between oral/pharyngeal and external odontodes. We set out a test of this latter hypothesis, examining the development of scales of the thelodont Loganellia scotica using synchrotron radiation X-ray tomographic microscopy (SRXTM). We reveal that the internal scales are organized into fused patches and rows, a key distinction from the discrete dermal scales. The pattern of growth of oral scale patches is polarized, but not along a particular vector, whereas pharyngeal scale rows grew along a vector. Our test of the phylogenetic distribution of oral and pharyngeal scales and teeth in vertebrates indicates that odontodes are first expressed in an external position. Internal scales, where present, are always located near to external orifices; the sequential development of pharyngeal scales in Loganellia is peculiar among thelodonts and other stem gnathostomes. It represents a convergence on, rather than the establishment of, the developmental pattern underpinning tooth replacement in jawed vertebrates. The available evidence suggests that internal odontodes evolved through the expansion of odontogenic competence from external to internal epithelia.

Large colonial organisms with coordinated growth in oxygenated environments 2.1 Gyr ago.

The evidence for macroscopic life during the Palaeoproterozoic era (2.5-1.6 Gyr ago) is controversial. Except for the nearly 2-Gyr-old coil-shaped fossil Grypania spiralis, which may have been eukaryotic, evidence for morphological and taxonomic biodiversification of macroorganisms only occurs towards the beginning of the Mesoproterozoic era (1.6-1.0 Gyr). Here we report the discovery of centimetre-sized structures from the 2.1-Gyr-old black shales of the Palaeoproterozoic Francevillian B Formation in Gabon, which we interpret as highly organized and spatially discrete populations of colonial organisms. The structures are up to 12 cm in size and have characteristic shapes, with a simple but distinct ground pattern of flexible sheets and, usually, a permeating radial fabric. Geochemical analyses suggest that the sediments were deposited under an oxygenated water column. Carbon and sulphur isotopic data indicate that the structures were distinct biogenic objects, fossilized by pyritization early in the formation of the rock. The growth patterns deduced from the fossil morphologies suggest that the organisms showed cell-to-cell signalling and coordinated responses, as is commonly associated with multicellular organization. The Gabon fossils, occurring after the 2.45-2.32-Gyr increase in atmospheric oxygen concentration, may be seen as ancient representatives of multicellular life, which expanded so rapidly 1.5 Gyr later, in the Cambrian explosion.