Tetrapod Evolution Research Articles

Musculoskeletal anatomical changes that accompany limb reduction in lizards.

Muscles, bones, and tendons in the adult tetrapod limb are intimately integrated, both spatially and functionally. However, muscle and bone evolution do not always occur hand in hand. We asked, how does the loss of limb bones affect limb muscle anatomy, and do these effects vary among different lineages? To answer these questions, we compared limb muscular and skeletal anatomy among gymnophthalmid lizards, which exhibit a remarkable variation in limb morphology and different grades of digit and limb reduction. We mapped the characters onto a phylogeny of the group to assess the likelihood that they were acquired independently. Our results reveal patterns of reduction of muscle and bone elements that did not always coincide and examples of both, convergent and lineage-specific non-pentadactyl musculoskeletal morphologies. Among lineages in which non-pentadactyly evolved independently, the degree of convergence seems to depend on the number of digits still present. Most tetradactyl and tridactyl limbs exhibited profound differences in pattern and degree of muscle loss/reduction, and recognizable morphological convergence occurred only in extremely reduced morphologies (e.g., spike-like appendix). We also found examples of muscles that persisted although the bones to which they plesiomorphically attach had been lost, and examples of muscles that had been lost although their normal bony attachments persisted. Our results demonstrate that muscle anatomy in reduced limbs cannot be predicted from bone anatomy alone, meaning that filling the gap between osteological and myological data is an important step toward understanding this recurrent phenomenon in the evolution of tetrapods.

Stratigraphy and depositional environments of the Late Famennian (Late Devonian) of Southern Belgium and characterization of the Strud locality

AbstractThe Famennian (Upper Devonian,c. 372 to 359 Ma) strata of Belgium have recently received much attention after the discoveries of early tetrapod remains and outstandingly preserved continental arthropods. The Strud locality has yielded a diverse flora and fauna including seed-plants, tetrapods, various placoderm, actinopterygian, acanthodian and sarcopterygian fishes, crustaceans (anostracans, notostracans, conchostracans and decapods) and a putative complete insect. This fossil assemblage is one of the oldest continental – probably fresh-water – ecosystems with a considerable vertebrate and invertebrate diversity. The study of the palaeoenvironment of the Strud locality is crucial because it records one of the earliest and most important phases of tetrapod evolution that took place after their emergence but before their terrestrialization. It raises the question of environmental and ecological conditions for the Devonian aquatic ecosystem and the selection pressures occurring at the onset of tetrapod terrestrialization. The present study characterized the fluvial facies of the Upper Famennian sedimentary rocks of Strud and the surrounding areas. The exceptional preservation of arthropods and plants in the main fossiliferous layers is explained by rapid burial in the fine-grained sediment of the quiet and confined flood plain environment. Newly investigated fossiliferous sections in the Meuse–Samson area led to the description and correlation of key sections (Strud, Wierde and Jausse sections, complemented by the less continuous Haltinne, Huy and Coutisse sections). Moreover, the investigated sections allowed a review of the age of the fossiliferous horizon, which is now definitely considered to be Late Famennian in age.

Hox cluster characterization of Banna caecilian (Ichthyophis bannanicus) provides hints for slow evolution of its genome.

BackgroundCaecilians, with a discrete lifestyle, are the least explored group of amphibians. Though with distinct traits, many aspects of their biology are poorly investigated. Obtaining the caecilian genomic sequences will offer new perspectives and aid the fundamental studies in caecilian biology. The caecilian genomic sequences are also important and practical in the comparative genomics of amphibians. Currently, however, only sparse genomic sequences of caecilians are available. Hox genes, an old family of transcription factors playing central roles in the establishment of metazoan body plan. Understanding their structure and genomic organization may provide insights into the animal’s genome, which is valuable for animals without a sequenced genome.ResultsWe sequenced and characterized the Hox clusters of Banna caecilian (Ichthyophis bannanicus) with a strategy combining long range PCR and genome walking. We obtained the majority of the four caecilian Hox clusters and identified 39 Hox genes, 5 microRNA genes and 1 pseudogene (ψHoxD12). There remained seven intergenic gaps we were unable to fill. From the obtained sequences, the caecilian Hox clusters contained less repetitive sequences and more conserved noncoding elements (CNEs) than the frog counterparts. We found that caecilian and coelacanth shared many more CNEs than frog and coelacanth did. Relative rate of sequence evolution showed that caecilian Hox genes evolved significantly more slowly than the other tetrapod species used in this study and were comparable to the slowly evolving coelacanth Hox genes. Phylogenetic tree of the four Hox clusters also revealed shorter branch length especially for the caecilian HoxA, HoxB and HoxD clusters. These features of the caecilian Hox clusters suggested a slowly evolving genome, which was supported by further analysis of a large orthologous protein dataset.ConclusionsOur analyses greatly extended the knowledge about the caecilian Hox clusters from previous PCR surveys. From the obtained Hox sequences and the orthologous protein dataset, the caecilian Hox loci and its genome appear evolving comparatively slowly. As the basal lineage of amphibians and land vertebrate, this characteristic of the caecilian genome is valuable in the study concerning the genome biology and evolution of amphibians and early tetrapods.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-015-1684-0) contains supplementary material, which is available to authorized users.

Turn (on) Your Head and “Cough”: Evolution of Lung Breathing from a Lungless Primitive Vertebrate

Air breathing was critical to the terrestrial radiation and evolution of tetrapods and arose in fish. The origins of the vertebrate lung stem from primitive boney fish. The origin of the neural substrates, which are sensitive to metabolically produced CO2 and which rhythmically activating respiratory muscles to produce lung ventilation to match ventilation to metabolic demand, is enigmatic. We have found that a distinct periodic centrally generated rhythm, described as “cough” and occurring in lamprey in vivo and in vitro, is modulated by central sensitivity to CO2. This suggests that elements critical for the evolution of breathing in tetrapods, were present in the most basal vertebrate ancestors prior to the evolution of the lung. We propose that the evolution of breathing in all vertebrates occurred through exaptations derived from these critical basal elements.

Embryonic Origin and Patterning of Cranial Muscle in the Mexican Axolotl ( Ambystoma mexicanum )

Cranial muscles play critical roles in numerous and diverse functions, including feeding, respiration, facial expression and (in some groups) vocalization. Despite the conservation of their basic structure in vertebrate evolution, cranial muscles have also played a significant role in evolutionary transitions among species. Here, we employ embryonic transplantations, using GFP-transgenic axolotls as donors, to determine the mesodermal contribution to cranial bone, cartilage and muscle. Expression patterns of cranial mesoderm markers are also analyzed within developing muscles. We define the axial level where unsegmented mesoderm can contribute to head muscles in the axolotl. Analysis of the posterior limit of unsegmented myogenic mesoderm indicates close overlap with the head-trunk boundary in the somites. This may help explain some of the differences in fate maps for muscles of birds and amphibians in the posterior head. Finally, gene expression analysis reveals markers for muscle groups important to the evolution of early tetrapods, including the gill levators.

Amelotin: an enamel matrix protein that experienced distinct evolutionary histories in amphibians, sauropsids and mammals.

BackgroundAmelotin (AMTN) is an ameloblast-secreted protein that belongs to the secretory calcium-binding phosphoprotein (SCPP) family, which originated in early vertebrates. In rodents, AMTN is expressed during the maturation stage of amelogenesis only. This expression pattern strongly differs from the spatiotemporal expression of other ameloblast-secreted SCPPs, such as the enamel matrix proteins (EMPs). Furthermore, AMTN was characterized in rodents only. In this study, we applied various approaches, including in silico screening of databases, PCRs and transcriptome sequencing to characterize AMTN sequences in sauropsids and amphibians, and compared them to available mammalian and coelacanth sequences.ResultsWe showed that (i) AMTN is tooth (enamel) specific and underwent pseudogenization in toothless turtles and birds, and (ii) the AMTN structure changed during tetrapod evolution. To infer AMTN function, we studied spatiotemporal expression of AMTN during amelogenesis in a salamander and a lizard, and compared the results with available expression data from mouse. We found that AMTN is expressed throughout amelogenesis in non-mammalian tetrapods, in contrast to its expression limited to enamel maturation in rodents.ConclusionsTaken together our findings suggest that AMTN was primarily an EMP. Its functions were conserved in amphibians and sauropsids while a change occurred early in the mammalian lineage, modifying its expression pattern during amelogenesis and its gene structure. These changes likely led to a partial loss of AMTN function and could have a link with the emergence of prismatic enamel in mammals.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-015-0329-x) contains supplementary material, which is available to authorized users.

Positional strategy of trunk muscles among aquatic, semi-aquatic and terrestrial species in Urodela

Clarification of the trunk structure in Urodela is important in understanding the locomotive evolution of basal tetrapods. The components of the muscular trunk wall among Urodela using different modes of locomotion were compared. Since the whole trunk may be used for swimming and the effect of limbs may be small in the more aquatic species, they showed smaller differences in the trunk muscles among anterior, middle and posterior sections of the trunk. By contrast, in the more terrestrial species, the dorsal and abdominal muscles are larger in the middle section than those in the anterior and posterior sections. High compressive stresses occur in the supporting limbs and their insertion at the trunk on the ventral side, and spread from the forelimbs along the back to the supporting hindlimbs on the dorsal side. Tensile stresses occur in the middle ventral part. The components of the trunk muscles among the three sections may reflect differences in stresses occurring in the trunk of the more terrestrial species. The findings also suggest that in the middle section, larger dorsal muscles for stiffening the back to maintain posture and larger abdominal muscles are responsible for balancing the body weight while it is supported by the limbs in the more terrestrial species.

Molecular genomic- and transcriptional-aspects of a teleost TRAF6 homolog: Possible involvement in immune responses of Oplegnathus fasciatus against pathogens

Tumor necrosis factor receptor (TNFR)-associated factor 6 (TRAF6) is a crucial docking molecule for TNFR superfamily and Interleukin-1 receptor/Toll-like receptor (IL-1R/TLR) superfamily. As an adaptor protein in pathogen-induced signaling cascades, TRAF6 modulates both adaptive- and innate-immunity. In order to understand the immune responses of teleost TRAF6, Oplegnathus fasciatus TRAF6-like gene (OfTRAF6) was identified and characterized. Genomic length of OfTRAF6 (4 kb), obtained by means of a genomic BAC library, spanned seven exons which represented a putative coding sequence of 1716 bp and encoded 571 amino acids (aa) with an estimated molecular weight of 64 kDa. This putative protein demonstrated the classical tetra-domain architecture composed of a zinc finger RING-type profile, two zinc finger TRAF-type profiles, a coiled-coil region and a MATH domain. While the sequence similarity with human TRAF6 was 66.5%, OfTRAF6 shared a higher overall similarity with teleost homologs (∼75–92%). Phylogeny of TRAF-family was examined and TRAF6-subfamily appeared to be the precursor of other subfamilies. In addition, the clustering pattern confirmed that OfTRAF6 is a novel member of TRAF6subfamily. Based on comparative genomic analysis, we found that vertebrate TRAF6 exhibits two distinct structures in teleost and tetrapod lineages. An intron-loss event has probably occurred in TRAF6 gene during the evolution of tetrapods from teleosts. Inspection of putative OfTRAF6 promoter revealed the presence of several immune responsive transcription factor binding sites. Real-time qPCR assay detected OfTRAF6 transcripts in eleven juvenile fish tissues with higher levels in peripheral blood cells followed by liver. Putative role of OfTRAF6 in response to flagellin, LPS, poly I:C, pathogenic bacteria (Edwardsiella tarda and Streptococcus iniae) and rock bream iridovirus (RBIV) was profiled in different tissues and OfTRAF6 revealed up-regulated transcript levels. Altogether, these findings implicate that OfTRAF6 is not only involved in flagellin-induced signaling cascade, but also contributes to the antibacterial- and antiviral-responses.

First Occurrence of Tetrapod Footprints from Westphalian Strata of the Sidi Kassem Basin, Central Morocco

The Sidi Kassem Basin is the only limnic basin of Westphalian age in Morocco. It is built up of 1,250 m of alluvio-fluvial to lacustrine deposits that have so far yielded plant fossils and invertebrate remains only. Recent exploration for fossil tetrapod footprints in floodplain-deposits of the basin revealed a moderately diverse vertebrate ichnofauna composed of tracks assigned to cf. Batrachichnus Woodworth, 1900; cf. Hylopus Dawson, 1882; Dimetropus Romer and Price, 1940; and Notalacerta Butts, 1891. The tracks can be referred to temnospondyl, anamniote reptiliomorph, non-therapsid synapsid (pelycosaur), and captorhinomorph trackmakers. The described ichnoassemblage is important in at least three aspects: (1) It suggests an Early to mid-Pennsylvanian age for the footprint-bearing strata of the study area. (2) It is the oldest association of tetrapod footprints from Africa. (3) It is the first evidence of the relatively rare ichnogenera cf. Hylopus and Notalacerta outside of North America and Europe. Judged from the variety of tetrapod tracks and previously collected floral remains, the Sidi Kassem Basin must have represented a well-established continental ecosystem during Pennsylvanian time. Further exploration for trace and body fossils of Palaeozoic vertebrates in this basin may be important for the reconstruction of early tetrapod evolution.

Coevolution of Mucosal Immunoglobulins and the Polymeric Immunoglobulin Receptor: Evidence That the Commensal Microbiota Provided the Driving Force

Immunoglobulins (Igs) in mucosal secretions contribute to immune homeostasis by limiting access of microbial and environmental antigens to the body proper, maintaining the integrity of the epithelial barrier and shaping the composition of the commensal microbiota. The emergence of IgM in cartilaginous fish represented the primordial mucosal Ig, which is expressed in all higher vertebrates. Expansion and diversification of the mucosal Ig repertoire led to the emergence of IgT in bony fishes, IgX in amphibians, and IgA in reptiles, birds, and mammals. Parallel evolution of cellular receptors for the constant (Fc) regions of Igs provided mechanisms for their transport and immune effector functions. The most ancient of these Fc receptors is the polymeric Ig receptor (pIgR), which first appeared in an ancestor of bony fishes. The pIgR transports polymeric IgM, IgT, IgX, and IgA across epithelial cells into external secretions. Diversification and refinement of the structure of mucosal Igs during tetrapod evolution were paralleled by structural changes in pIgR, culminating in the multifunctional secretory IgA complex in mammals. In this paper, evidence is presented that the mutualistic relationship between the commensal microbiota and the vertebrate host provided the driving force for coevolution of mucosal Igs and pIgR.

Current and historical perspectives on the completeness of the fossil record of pelycosaurian-grade synapsids

Understanding of the early evolution of tetrapods may have been influenced by the effects of geological and anthropogenic sampling biases, as suggested by previous studies. Here we make a thorough assessment of how these and other biases affect the record of pelycosaurian-grade synapsids, a group of tetrapods that dominated the terrestrial realm during the late Carboniferous and early Permian. Modified versions of the character and skeletal completeness metrics are used to assess the completeness of the known specimens, while a recently published supertree of basal synapsids is tested for congruence between the stratigraphic and phylogenetic hypotheses. A historical analysis is also applied to the record in order to show how the biases in the study of this group over the past centuries may have influenced the current record. The results show that the completeness of basal synapsid specimens shows very little variation throughout the Early Permian. A peak in skeletal and character completeness metric values in the Middle Permian (Wordian) is attributed to exceptional preservation of the Mezen fauna. A significant negative correlation is found between the skeletal completeness metric and a taxic diversity curve of pelycosaurs, implying a tendency to name many species based on poor material. The lack of correlation between the character completeness metric and diversity is attributed to the history of discovery in the group: the majority of pelycosaur species were named between the 1930s and 1960s, when character based assignments were secondary to size, location and stratigraphy. A strong correspondence between the phylogeny and stratigraphy implies a reliable phylogenetic hypothesis, but the low relative completeness index score suggests that a great deal of the fossil record is missing. While the relative completeness index has improved over the past century, the rate of improvement has slowed in the last two decades, and the slowing rate of discovery of new species suggests that the limit of what the fossil record of pelycosaurs has to offer is being approached. A consistent shape of diversity curves over the past century implies that the same biases which affected the record in the past are still affecting it now. This study highlights the need for sampling correction methods to be employed in studies of early synapsids.

A Footnote to the Evolution of Digits

A Footnote to the Evolution of Digits

Identification, characterization, and expression of dentin matrix protein 1 gene inXenopus laevis

Dentin matrix protein 1 (DMP1) is an acidic extracellular matrix protein expressed mainly in bone and dentin, and is a member of the small integrin-binding ligand N-linked glycoprotein (SIBLING) family. The DMP1 gene, however, appears to evolve rapidly in comparison with other SIBLING genes, even though such functionally important molecules usually evolve more slowly than less important ones. The purpose of this study was to identify and characterize an ortholog of the DMP1 gene in an amphibian (Xenopus laevis; X. laevis) to clarify molecular evolutionary alterations in DMP1 associated with calcified tissues in tetrapods. Furthermore, we analyzed the mRNA expression of this gene to elucidate its functional change in bone and developing tooth germ in comparison with amniote DMP1s. The similarities of the deduced amino acid sequence of X. laevis DMP1 to that of the corresponding amniote proteins were low, although they did share several unique features specific to DMP1 and have similar properties. Expression of X. laevis DMP1 mRNA was predominant in osteocytes and odontoblasts, but only transiently observed in ameloblasts, as in amniotes. These results suggest that DMP1 has conserved several functions during tetrapod evolution. This indicates that continuity of biochemical properties has been more important in maintaining DMP1 functionality than that of the sequence of amino acid residues, which has undergone change over the course of molecular evolution.

Dimorphisms of the proteasome subunit beta type 8 gene (PSMB8) of ectothermic tetrapods originated in multiple independent evolutionary events

The proteasome subunit beta type 8 gene (PSMB8) encodes one of the beta subunits of the immunoproteasome responsible for the generation of peptides presented by major histocompatibility complex class I molecules. Dimorphic alleles of the PSMB8 gene, termed A and F types, based on the deduced 31st amino acid residue of the mature protein have been reported from various vertebrates. Phylogenetic analysis revealed the presence of dichotomous ancient lineages, one comprising the F-type PSMB8 of basal ray-finned fishes, and the other comprising the A-type PSMB8 of these animals and both the F- and A-type PSMB8 of Xenopus and acanthopterygians, indicating that evolutionary history of the PSMB8 dimorphism was not straightforward. We analyzed the PSMB8 gene of five reptile and one amphibian species and found both the A and F types from all six. Phylogenetic analysis indicated that the PSMB8 F type was apparently regenerated from the PSMB8 A type at least five times independently during tetrapod evolution. Genomic typing of wild individuals of geckos and newts indicated that the frequencies of the A- and F-type alleles are not highly biased in these species. Phylogenetic analysis of each exon of the reptile PSMB8 gene suggested interallelic sequence homogenization as a possible evolutionary mechanism for the apparent recurrent regeneration of PSMB8 dimorphism in tetrapods. An extremely strong balancing selection acting on PSMB8 dimorphism was implicated in an unprecedented pattern of allele evolution.

Analysis of the transcriptome of the Indonesian coelacanth Latimeria menadoensis

BackgroundLatimeria menadoensis is a coelacanth species first identified in 1997 in Indonesia, at 10,000 Km of distance from its African congener. To date, only six specimens have been caught and just a very limited molecular data is available. In the present work we describe the de novo transcriptome assembly obtained from liver and testis samples collected from the fifth specimen ever caught of this species.ResultsThe deep RNA sequencing performed with Illumina technologies generated 145,435,156 paired-end reads, accounting for ~14 GB of sequence data, which were de novo assembled using a Trinity/CLC combined strategy. The assembly output was processed and filtered producing a set of 66,308 contigs, whose quality was thoroughly assessed. The comparison with the recently sequenced genome of the African congener Latimeria chalumnae and with the available genomic resources of other vertebrates revealed a good reconstruction of full length transcripts and a high coverage of the predicted full coelacanth transcriptome.The RNA-seq analysis revealed remarkable differences in the expression profiles between the two tissues, allowing the identification of liver- and testis-specific transcripts which may play a fundamental role in important biological processes carried out by these two organs.ConclusionGiven the high genomic affinity between the two coelacanth species, the here described de novo transcriptome assembly can be considered a valuable support tool for the improvement of gene prediction within the genome of L. chalumnae and a valuable resource for investigation of many aspects of tetrapod evolution.

ANALYSIS OF TRIASSIC ARCHOSAURIFORM TRACKWAYS: DIFFERENCE IN STRIDE/FOOT RATIO BETWEEN DINOSAUROMORPHS AND OTHER ARCHOSAURIFORMS

Fossilized trackways have rarely been analyzed quantitatively to examine major trends and patterns in evolution despite their potential utility, especially in understanding locomotory evolution. In the present study, trackways of Triassic archosauriforms were analyzed. The analyses showed foot and stride lengths of archosauriforms increased from the Early to Middle Triassic, especially those of dinosauromorphs, which tripled. Dinosauromorphs were much smaller in foot length and stride length compared to other archosauriforms during the Early Triassic. They reached similar stride length compared with other archosauriforms during the Middle Triassic and similar foot length in the Late Triassic. Stride/foot ratio is significantly higher in dinosauromorphs compared to other archosauriforms throughout the Triassic. This relatively long stride length of dinosauromorphs is attributed to either faster speed or higher relative hip height that was probably caused by their digitigrade foot posture. Analyses of trackway data sets, especially in combination with precise trackmaker assignment and age determination, would bring us more thorough knowledge about locomotory evolution of tetrapods that complements body fossil evidence.

Congenital Malformations of the Vertebral Column in Ancient Amphibians

Temnospondyls, the largest group of Palaeozoic and Mesozoic amphibians, primitively possess rhachitomous vertebrae with multipartite centra (consisting of one horse-shoe-shaped inter- and paired pleurocentra). In a group of temnospondyls, the stereospondyls, the intercentra became pronounced and disc-like, whereas the pleurocentra were reduced. We report the presence of congenital vertebral malformations (hemi, wedge and block vertebrae) in Permian and Triassic temnospondyls, showing that defects of formation and segmentation in the tetrapod vertebral column represent a fundamental failure of somitogenesis that can be followed throughout tetrapod evolution. This is irrespective of the type of affected vertebra, that is, rhachitomous or stereospondylous, and all components of the vertebra can be involved (intercentrum, pleurocentrum and neural arch), either together or independently on their own. This is the oldest known occurrence of wedge vertebra and congenital block vertebra described in fossil tetrapods. The frequency of vertebral congenital malformations in amphibians appears unchanged from the Holocene.

The African coelacanth genome provides insights into tetrapod evolution

It was a zoological sensation when a living specimen of the coelacanth was first discovered in 1938, as this lineage of lobe-finned fish was thought to have gone extinct 70 million years ago. The modern coelacanth looks remarkably similar to many of its ancient relatives, and its evolutionary proximity to our own fish ancestors provides a glimpse of the fish that first walked on land. Here we report the genome sequence of the African coelacanth, Latimeria chalumnae. Through a phylogenomic analysis, we conclude that the lungfish, and not the coelacanth, is the closest living relative of tetrapods. Coelacanth protein-coding genes are significantly more slowly evolving than those of tetrapods, unlike other genomic features . Analyses of changes in genes and regulatory elements during the vertebrate adaptation to land highlight genes involved in immunity, nitrogen excretion and the development of fins, tail, ear, eye, brain, and olfaction. Functional assays of enhancers involved in the fin-to-limb transition and in the emergence of extra-embryonic tissues demonstrate the importance of the coelacanth genome as a blueprint for understanding tetrapod evolution.

Conservation of Amelogenin Gene Expression During Tetrapod Evolution

Well studied in mammals, amelogenesis is less known at the molecular level in reptiles and amphibians. In the course of extensive studies of enamel matrix protein (EMP) evolution in tetrapods, we look for correlation between changes in protein sequences and temporospatial protein gene expression during amelogenesis, using an evo-devo approach. Our target is the major EMP, amelogenin (AMEL) that plays a crucial role in enamel structure. We focused here our attention to an amphibian, the salamander Pleurodeles waltl. RNAs were extracted from the lower jaws of a juvenile P. waltl and the complete AMEL sequence was obtained using PCR and RACE PCR. The alignment of P. waltl AMEL with other tetrapodan (frogs, reptiles and mammals) sequences revealed residue conservation in the N- and C-terminal regions, and a highly variable central region. Using sense and anti-sense probes synthetized from the P. waltl AMEL sequence, we performed in situ hybridization on sections during amelogenesis in larvae, juveniles, and adults. We demonstrated that (i) AMEL expression was always found to be restricted to ameloblasts, (ii) the expression pattern was conserved through ontogeny, even in larvae where enameloid is present in addition to enamel, and (iii) the processes are similar to those described in lizards and mammals. These findings indicate that high variations in the central region of AMEL have not modified its temporospatial expression during amelogenesis for 360 million years of tetrapod evolution.

Gaining ground: the origin and evolution of tetrapods

Preface Acknowledgments One Introduction Two Skulls and Skeletons in Transition Three Relationships and Relatives: The Lobe-Fin Family Four Setting the Scene: The Devonian World Five The First Feet: Tetrapods of the Famennian Six From Fins to Feet: Transformation and Transition Seven Emerging into the Carboniferous: The First Phase Eight East Kirkton and the Roots of the Modern Family Tree Nine The Late Carboniferous: Expanding Horizons Ten Gaining Ground: The Evolution of Terrestriality References Index