Author Correction: Elpistostege and the origin of the vertebrate hand.

An amendment to this paper has been published and can be accessed via a link at the top of the paper.

Elpistostege and the origin of the vertebrate hand.

The evolution of fishes to tetrapods (four-limbed vertebrates) was one of the most important transformations in vertebrate evolution. Hypotheses of tetrapod origins rely heavily on the anatomy of a few tetrapod-like fish fossils from the Middle and Late Devonian period (393-359 million years ago)1. These taxa-known as elpistostegalians-include Panderichthys2, Elpistostege3,4 and Tiktaalik1,5, none of which has yet revealed the complete skeletal anatomy of the pectoral fin. Here we report a 1.57-metre-long articulated specimen of Elpistostege watsoni from the Upper Devonian period of Canada, which represents-to our knowledge-the most complete elpistostegalian yet found. High-energy computed tomography reveals that the skeleton of the pectoral fin has four proximodistal rows of radials (two of which include branched carpals) as well as two distal rows that are organized as digits and putative digits. Despite this skeletal pattern (which represents the most tetrapod-like arrangement of bones found in a pectoral fin to date), the fin retains lepidotrichia (fin rays) distal to the radials. We suggest that the vertebrate hand arose primarily from a skeletal pattern buried within the fairly typical aquatic pectoral fin of elpistostegalians. Elpistostege is potentially the sister taxon of all other tetrapods, and its appendages further blur the line between fish and land vertebrates.

Whole-body variational modularity in the zebrafish: an inside-out story of a model species.

Actinopterygians are the most diversified clade of extant vertebrates. Their impressive morphological disparity bears witness to tremendous ecological diversity. Modularity, the organization of biological systems into quasi-independent anatomical/morphological units, is thought to increase evolvability of organisms and facilitate morphological diversification. Our study aims to quantify patterns of variational modularity in a model actinopterygian, the zebrafish (Danio rerio), using three-dimensional geometric morphometrics on osteological structures isolated from micro-CT scans. A total of 72 landmarks were digitized along cranial and postcranial ossified regions of 30 adult zebrafishes. Two methods were used to test modularity hypotheses, the covariance ratio and the distance matrix approach. We find strong support for two modules, one comprised paired fins and the other comprised median fins, that are best explained by functional properties of subcarangiform swimming. While the skull is tightly integrated with the rest of the body, its intrinsic integration is relatively weak supporting previous findings that the fish skull is a modular structure. Our results provide additional support for the recognition of similar hypotheses of modularity identified based on external morphology in various teleosts, and at least two variational modules are proposed. Thus, our results hint at the possibility that internal and external modularity patterns may be congruent.

Phenotypic regionalization of the vertebral column in the thorny skate Amblyraja radiata: Stability and variation.

Regionalization of the vertebral column occurred early during vertebrate evolution and has been extensively investigated in mammals. However, less data are available on vertebral regions of crown gnathostomes. This is particularly true for batoids (skates, sawfishes, guitarfishes, and rays) whose vertebral column has long been considered to be composed of the same two regions as in teleost fishes despite the presence of a synarcual. However, the numerous vertebral units in chondrichthyans may display a more complex regionalization pattern than previously assumed and the intraspecific variation of such pattern deserves a thorough investigation. In this study, we use micro-computed tomography (µCT) scans of vertebral columns of a growth series of thorny skates Amblyraja radiata to provide the first fine-scale morphological description of vertebral units in a batoids species. We further investigate axial regionalization using a replicable clustering analysis on presence/absence of vertebral elements to decipher the regionalization of the vertebral column of A. radiata. We identify four vertebral regions in this species. The two anteriormost regions, named synarcual and thoracic, may undergo strong developmental or functional constraints because they display stable patterns of shapes and numbers of vertebral units across all growth stages. The third region, named hemal transitional, is characterized by high inter-individual morphological variation and displays a transition between the monospondylous (one centrum per somite) to diplospondylous (two centra per somite) conditions. The posteriormost region, named caudal, is subdivided into three sub-regions with shapes changing gradually along the anteroposterior axis. These regionalized patterns are discussed in light of ecological habits of skates.

A microanatomical and histological study of the scales of the Devonian sarcopterygian Miguashaia bureaui and the evolution of the squamation in coelacanths.

Coelacanths have traditionally been described as morphologically conservative throughout their long evolutionary history, which spans more than 400 million years. After an initial burst during the Devonian, a morphological stasis was long thought to have prevailed since the Carboniferous, as shown by the extant Latimeria. New fossil discoveries have challenged this view, with punctual and sometimes unusual departures from the general coelacanth Bauplan. The dermal skeleton is considered to represent one, if not the main, example of morphological stasis in coelacanth evolution and as a consequence, has remained poorly surveyed. The lack of palaeohistological data on the dermoskeleton has resulted in a poor understanding of the early establishment and evolution of the coelacanth squamation. Here we describe the scales of Miguashaia bureaui from the Upper Devonian of Miguasha, Québec (Canada), revealing histological data for a Palaeozoic coelacanth in great detail and adding to our knowledge on the dermal skeleton of sarcopterygians. Miguashaia displays rounded scales ornamented by tubercules and narrow ridges made of dentine and capped with enamel. At least two generations of superimposed odontodes occur, which is reminiscent of the primitive condition of stem osteichthyans like Andreolepis or Lophosteus, and onychodonts like Selenodus. The middle vascular layer is well developed and shows traces of osteonal remodelling. The basal plate consists of a fully mineralised lamellar bone with a repetitive rotation pattern every five layers indicating a twisted plywood-like arrangement of the collagen plies. Comparisons with the extant Latimeria and other extinct taxa show that these features are consistently conserved across coelacanth evolution with only minute changes in certain taxa. The morphological and histological features displayed in the scales of Miguashaia enable us to draw a comprehensive picture of the onset of the coelacanth squamation and to propose and discuss evolutionary scenarios for the coelacanth dermoskeleton.

Loss in the making: absence of pelvic fins and presence of paedomorphic pelvic girdles in a Late Devonian antiarch placoderm (jawed stem-gnathostome).

Within jawed vertebrates, pelvic appendages have been modified or lost repeatedly, including in the most phylogenetically basal, extinct, antiarch placoderms. One Early Devonian basal antiarch, Parayunnanolepis, possessed pelvic girdles, suggesting the presence of pelvic appendages at the origin of jawed vertebrates; their absence in more derived antiarchs implies a secondary loss. Recently, paired female genital plates were identified in the Late Devonian antiarch, Bothriolepis canadensis, in the position of pelvic girdles in other placoderms. We studied these putative genital plates along an ontogenetic series of B. canadensis; ontogenetic changes in their morphology, histology and elemental composition suggest they represent endoskeletal pelvic girdles composed of perichondral and endochondral bone. We suggest that pelvic fins of derived antiarchs were lost, while pelvic girdles were retained, but reduced, relative to Parayunnanolepis This indicates developmental plasticity and evolutionary lability in pelvic appendages, shortly after these elements evolved at the origin of jawed vertebrates.

Fin modules: an evolutionary perspective on appendage disparity in basal vertebrates.

BACKGROUND: Fishes are extremely speciose and also highly disparate in their fin configurations, more specifically in the number of fins present as well as their structure, shape, and size. How they achieved this remarkable disparity is difficult to explain in the absence of any comprehensive overview of the evolutionary history of fish appendages. Fin modularity could provide an explanation for both the observed disparity in fin configurations and the sequential appearance of new fins. Modularity is considered as an important prerequisite for the evolvability of living systems, enabling individual modules to be optimized without interfering with others. Similarities in developmental patterns between some of the fins already suggest that they form developmental modules during ontogeny. At a macroevolutionary scale, these developmental modules could act as evolutionary units of change and contribute to the disparity in fin configurations. This study addresses fin disparity in a phylogenetic perspective, while focusing on the presence/absence and number of each of the median and paired fins. RESULTS: Patterns of fin morphological disparity were assessed by mapping fin characters on a new phylogenetic supertree of fish orders. Among agnathans, disparity in fin configurations results from the sequential appearance of novel fins forming various combinations. Both median and paired fins would have appeared first as elongated ribbon-like structures, which were the precursors for more constricted appendages. Among chondrichthyans, disparity in fin configurations relates mostly to median fin losses. Among actinopterygians, fin disparity involves fin losses, the addition of novel fins (e.g., the adipose fin), and coordinated duplications of the dorsal and anal fins. Furthermore, some pairs of fins, notably the dorsal/anal and pectoral/pelvic fins, show non-independence in their character distribution, supporting expectations based on developmental and morphological evidence that these fin pairs form evolutionary modules. CONCLUSIONS: Our results suggest that the pectoral/pelvic fins and the dorsal/anal fins form two distinct evolutionary modules, and that the latter is nested within a more inclusive median fins module. Because the modularity hypotheses that we are testing are also supported by developmental and variational data, this constitutes a striking example linking developmental, variational, and evolutionary modules.

Building blocks of a fish head: Developmental and variational modularity in a complex system.

Evolution of the vertebrate skull is developmentally constrained by the interactions among its anatomical systems, such as the dermatocranium and the sensory system. The interaction between the dermal bones and lateral line canals has been debated for decades but their morphological integration has never been tested. An ontogenetic series of 97 juvenile and adult Amia calva (Actinopterygii) was used to describe the patterning and modularity of sensory lateral line canals and their integration with supporting cranial bones. Developmental modules were tested for the otic canal and supratemporal commissure by computing correlations in the branching sequence of groups of pores. Landmarks were digitized on 25 specimens to test a priori hypotheses of variational and developmental modularity at the level of canals and dermal bones. Branching sequence suggests a specific patterning supported by significant positive correlations in the sequence of appearance of branches between bilateral sides. Differences in patterning between the otic canal and the supratemporal commissure and tests of modularity with geometric morphometrics suggest that both canals form distinct modules. The integration between bones and canals was insufficient to detect a module. However, both components were not independent. Groups of pores tended to disappear without affecting other groups of pores suggesting that they are quasi-independent units acting as modules. This study provides evidence of a hierarchical organization for the modular sensory system that could explain variation of pattern of canals among species and their association with dermal bones.

The revival of a so-called rotten fish: the ontogeny of the Devonian acanthodian Triazeugacanthus.

Since its original description as a chordate, the Late Devonian Scaumenella mesacanthi has been interpreted alternately as a prochordate, a larval ostracoderm and an immature acanthodian. For the past 30 years, these minute specimens were generally considered as decayed acanthodians, most of them belonging to Triazeugacanthus affinis. Among the abundant material of 'Scaumenella', we identified a size series of 188 specimens of Triazeugacanthus based on otolith characteristics. Despite taphonomic alteration, we describe proportional growth and progressive appearance of skeletal elements through size increase. Three ontogenetic stages are identified based on squamation extent, ossification completion and allometric growth. We demonstrate that what has been interpreted previously as various degrees of decomposition corresponds to ontogenetic changes.

Dynamic skeletogenesis in fishes: insight of exercise training on developmental plasticity.

BACKGROUND: Through developmental and evolutionary time, organisms respond variably to their environment not only in terms of size and shape but also in terms of timing. Developmental plasticity can potentially act on various aspects of the timing of developmental events (i.e., appearance, cessation, duration, sequence). In this study, we address the developmental plasticity of median fin endoskeleton by using exercise training on newly-hatched Arctic charr (Salvelinus alpinus). RESULTS: Developmental progress of cartilage formation (i.e., chondrification) in all fins is less influenced than ossification by an increase of water velocity. The most responsive elements, meaning those elements with greater onset plasticity owing to a water velocity increase, differ in terms of early versus late developmental events. The most responsive elements are those that chondrify and to a greater extent ossify later in the development. CONCLUSIONS: Plasticity is documented for the timing of appearance (i.e., onset) and the timing of transition from cartilage to bone (i.e., transitions of skeletal states) rather than the order of events within a sequence. Similarities of plastic response in developmental patterns could be used as a powerful criterion to strengthen the identification of phenotypic modules.

Evolution of median fin patterning and modularity in living and fossil osteichthyans.

Morphological and developmental similarities, and interactions among developing structures are interpreted as evidences of modularity. Such similarities exist between the dorsal and anal fins of living actinopterygians, on the anteroposterior axis: (1) both fins differentiate in the same direction [dorsal and anal fin patterning module (DAFPM)], and (2) radials and lepidotrichia differentiate in the same direction [endoskeleton and exoskeleton module (EEM)]. To infer the evolution of these common developmental patternings among osteichthyans, we address (1) the complete description and quantification of the DAFPM and EEM in a living actinopterygian (the rainbow trout Oncorhynchus mykiss) and (2) the presence of these modules in fossil osteichthyans (coelacanths, lungfishes, porolepiforms and 'osteolepiforms'). In Oncorhynchus, sequences of skeletal elements are determined based on (1) apparition (radials and lepidotrichia), (2) chondrification (radials), (3) ossification (radials and lepidotrichia), and (4) segmentation plus bifurcation (lepidotrichia). Correlations are then explored between sequences. In fossil osteichthyans, sequences are determined based on (1) ossification (radials and lepidotrichia), (2) segmentation, and (3) bifurcation of lepidotrichia. Segmentation and bifurcation patterns were found crucial for comparisons between extant and extinct osteichthyan taxa. Our data suggest that the EEM is plesiomorphic at least for actinopterygians, and the DAFPM is plesiomorphic for osteichthyans, with homoplastic dissociation. Finally, recurrent patterns suggest the presence of a Lepidotrichia Patterning Module (LPM).

Life history and ossification patterns in Miguashaia bureaui reveal the early evolution of osteogenesis in coelacanths.

The study of development is critical for revealing the evolution of major vertebrate lineages. Coelacanths have one of the longest evolutionary histories among osteichthyans, but despite access to extant representatives, the onset of their weakly ossified endoskeleton is still poorly understood. Here we present the first palaeohistological and skeletochronological study of Miguashaia bureaui from the Upper Devonian of Canada, pivotal for exploring the palaeobiology and early evolution of osteogenesis in coelacanths. Cross sections of the caudal fin bones show that the cortex is made of layers of primary bone separated by lines of arrested growth, indicative of a cyclical growth. The medullary cavity displays remnants of calcified cartilage associated with bony trabeculae, characteristic of endochondral ossification. A skeletochronological analysis indicates that rapid growth during a short juvenile period was followed by slower growth in adulthood. Our new analysis highlights the life history and palaeoecology of Miguashaia bureaui and reveals that, despite differences in size and habitat, the poor endoskeletal ossification known in the extant Latimeria chalumnae can be traced back at least 375 million years ago.

Morphometric analysis of lungfish endocasts elucidates early dipnoan palaeoneurological evolution.

The lobe-finned fish, lungfish (Dipnoi, Sarcoptergii), have persisted for ~400 million years from the Devonian Period to present day. The evolution of their dermal skull and dentition is relatively well understood, but this is not the case for the central nervous system. While the brain has poor preservation potential and is not currently known in any fossil lungfish, substantial indirect information about it and associated structures (e.g. labyrinths) can be obtained from the cranial endocast. However, before the recent development of X-ray tomography as a palaeontological tool, these endocasts could not be studied non-destructively, and few detailed studies were undertaken. Here, we describe and illustrate the endocasts of six Palaeozoic lungfish from tomographic scans. We combine these with six previously described digital lungfish endocasts (4 fossil and 2 recent taxa) into a 12-taxon dataset for multivariate morphometric analysis using 17 variables. We find that the olfactory region is more highly plastic than the hindbrain, and undergoes significant elongation in several taxa. Further, while the semicircular canals covary as an integrated module, the utriculus and sacculus vary independently of each other. Functional interpretation suggests that olfaction has remained a dominant sense throughout lungfish evolution, and changes in the labyrinth may potentially reflect a change from nektonic to near-shore environmental niches. Phylogenetic implications show that endocranial form fails to support monophyly of the 'chirodipterids'. Those with elongated crania similarly fail to form a distinct clade, suggesting these two paraphyletic groups have converged towards either head elongation or truncation driven by non-phylogenetic constraints.

A late-surviving stem-ctenophore from the Late Devonian of Miguasha (Canada).

Like other soft-bodied organisms, ctenophores (comb jellies) produce fossils only under exceptional taphonomic conditions. Here, we present the first record of a Late Devonian ctenophore from the Escuminac Formation from Miguasha in eastern Canada. Based on the 18-fold symmetry of this disc-shaped fossil, we assign it to the total-group Ctenophora. Our phylogenetic analyses suggest that the new taxon Daihuoides jakobvintheri gen. et sp. nov. falls near Cambrian stem ctenophores such as 'dinomischids' and 'scleroctenophorans'. Accordingly, Daihuoides is a Lazarus-taxon, which post-dates its older relatives by over 140 million years, and overlaps temporally with modern ctenophores, whose oldest representatives are known from the Early Devonian. Our analyses also indicate that the fossil record of ctenophores does not provide strong evidence for or against the phylogenomic hypothesis that ctenophores are sister to all other metazoans.

A fresh look at Cladarosymblema narrienense, a tetrapodomorph fish (Sarcopterygii: Megalichthyidae) from the Carboniferous of Australia, illuminated via X-ray tomography.

BACKGROUND: The megalichthyids are one of several clades of extinct tetrapodomorph fish that lived throughout the Devonian-Permian periods. They are advanced "osteolepidid-grade" fishes that lived in freshwater swamp and lake environments, with some taxa growing to very large sizes. They bear cosmine-covered bones and a large premaxillary tusk that lies lingually to a row of small teeth. Diagnosis of the family remains controversial with various authors revising it several times in recent works. There are fewer than 10 genera known globally, and only one member definitively identified from Gondwana. Cladarosymblema narrienense Fox et al. 1995 was described from the Lower Carboniferous Raymond Formation in Queensland, Australia, on the basis of several well-preserved specimens. Despite this detailed work, several aspects of its anatomy remain undescribed. METHODS: Two especially well-preserved 3D fossils of Cladarosymblema narrienense, including the holotype specimen, are scanned using synchrotron or micro-computed tomography (µCT), and 3D modelled using specialist segmentation and visualisation software. New anatomical detail, in particular internal anatomy, is revealed for the first time in this taxon. A novel phylogenetic matrix, adapted from other recent work on tetrapodomorphs, is used to clarify the interrelationships of the megalichthyids and confirm the phylogenetic position of C. narrienense. RESULTS: Never before seen morphological details of the palate, hyoid arch, basibranchial skeleton, pectoral girdle and axial skeleton are revealed and described. Several additional features are confirmed or updated from the original description. Moreover, the first full, virtual cranial endocast of any tetrapodomorph fish is presented and described, giving insight into the early neural adaptations in this group. Phylogenetic analysis confirms the monophyly of the Megalichthyidae with seven genera included (Askerichthys, Cladarosymblema, Ectosteorhachis, Mahalalepis, Megalichthys, Palatinichthys, and Sengoerichthys). The position of the megalichthyids as sister group to canowindrids, crownward of "osteolepidids" (e.g.,Osteolepis and Gogonasus), but below "tristichopterids" such as Eusthenopteron is confirmed, but our findings suggest further work is required to resolve megalichthyid interrelationships.

Developmental plasticity in fish exposed to a water velocity gradient: a complex response.

Developmental plasticity plays a major role in evolution and provides an excellent context for unravelling the ecological implication of variation in abiotic factors to which developing fish are subjected. Water velocity has been known to induce plasticity in salmonids, but the ontogenetic component of these changes is poorly documented. Newly hatched specimens of rainbow trout (Oncorhynchus mykiss) were reared in four constant water velocity treatments (0.4, 0.8, 1.6 and 3.2 cm/sec) for a period of 100 days. Traditional and geometric morphometrics were used complementarily to characterize morphological changes among treatments throughout ontogeny and demonstrated early and complex developmental plasticity in O. mykiss. Certain traits display a constant direction of change, whereas other traits present a break point at 20-25 mm ( approximately 40-60 dph) indicating a modification in the nature of changes between developmental stages. Plasticity in response to water velocity was detected from very early on (15-20 mm; approximately 20-40 dph) and concerned mostly fin-related traits. Body-related traits did not respond conformingly to functional expectations as fishes reared in the fastest velocity treatment show a robust body shape more comparable to that of fish from the slowest treatment than do fish from the intermediate velocity. The noncongruence between treatment and response gradient suggests that different combinations of water velocity have the potential to lead to diverging interpretation of plasticity, both in an ecological and evolutionary context. Overall, the complex shape changes observed in O. mykiss stress the importance of paying better attention to actual functional requirements and adaptations that occur at levels other than hydrodynamics.

The oldest articulated chondrichthyan from the Early Devonian period.

Chondrichthyans (including living sharks, skates, rays and chimaeras) have a fossil record of scales and dermal denticles perhaps dating back to the Late Ordovician period, about 455 million years ago. Their fossil tooth record extends to the earliest Devonian period, almost 418 million years ago, whereas the oldest known articulated shark remains date from the Early Devonian period, about 394 million years ago. Here we report the discovery of an articulated shark that is almost 409 million years old from the Early Devonian (early Emsian) period of New Brunswick, Canada. The specimen, identified as Doliodus problematicus (Woodward), sheds light on the earliest chondrichthyans and their interrelationships with basal jawed vertebrates. This species has been truly problematic. Previously known only from isolated teeth, it has been identified as an acanthodian and a chondrichthyan. This specimen is the oldest shark showing the tooth families in situ, and preserves one of the oldest chondrichthyan braincases. More notably, it shows the presence of paired pectoral fin-spines, previously unknown in cartilaginous fishes.

Morphological integration and developmental progress during fish ontogeny in two contrasting habitats.

Morphological integration can respond to environmental conditions, a response that may be dynamic through ontogeny. Among fishes, brook charrs (Salvelinus fontinalis) display a trophic polymorphism that makes it a good species for analyzing the ontogeny of morphological integration. To better understand the processes regulating variation and integration, we assess the ontogenetic dynamics of covariances and developmental progress for populations of S. fontinalis from two habitats that differ in water velocity; lake and stream. Geometric morphometrics and developmental progress were evaluated on 751 and 198 specimens, respectively. In both habitats, most ossification events occur before the transition from alevin to juvenile. This threshold defines two distinct periods. During the first period representing free-embryos and alevins, there are important shape changes and rapid ossification, integration tends to be relatively low and decreasing and the variance of shape drastically decreases. During the juvenile period, the rate of shape change decreases and the onset of ossification is nearly complete, plus integration increases and shape variance stabilizes. While we find two distinct developmental periods, we nonetheless find a notable stability underlying the ontogenetic dynamics of variability as well as gradual change in the structure of covariation within each habitat. Our results imply that the variability of juvenile body shape does not seem to retain signals of variability determined early in ontogeny and warrants caution in using juvenile as guides to the earlier causes of variability. Overall, this study highlights the difficulty of inferring causes of integration from studies of static covariance.

Modularity promotes morphological divergence in ray-finned fishes.

Modularity is considered a prerequisite for the evolvability of biological systems. This is because in theory, individual modules can follow quasi-independent evolutionary trajectories or evolve at different rates compared to other aspects of the organism. This may influence the potential of some modules to diverge, leading to differences in disparity. Here, we investigated this relationship between modularity, rates of morphological evolution and disparity using a phylogenetically diverse sample of ray-finned fishes. We compared the support for multiple hypotheses of evolutionary modularity and asked if the partitions delimited by the best-fitting models were also characterized by the highest evolutionary rate differentials. We found that an evolutionary module incorporating the dorsal, anal and paired fins was well supported by the data, and that this module evolves more rapidly and consequently generates more disparity than other modules. This suggests that modularity may indeed promote morphological disparity through differences in evolutionary rates across modules.