Postcranial disparity of galeaspids and the evolution of swimming speeds in stem-gnathostomes.

Galeaspids are extinct jawless relatives of living jawed vertebrates whose contribution to understanding the evolutionary assembly of the gnathostome bodyplan has been limited by absence of postcranial remains. Here, we describe Foxaspis novemura gen. et sp. nov., based on complete articulated remains from a newly discovered Konservat-Lagerstätte in the Early Devonian (Pragian, ∼410 Ma) of Guangxi, South China. F. novemura had a broad, circular dorso-ventrally compressed headshield, slender trunk and strongly asymmetrical hypochordal tail fin comprised of nine ray-like scale-covered digitations. This tail morphology contrasts with the symmetrical hypochordal tail fin of Tujiaaspis vividus, evidencing disparity in galeaspid postcranial anatomy. Analysis of swimming speed reveals galeaspids as moderately fast swimmers, capable of achieving greater cruising swimming speeds than their more derived jawless and jawed relatives. Our analyses reject the hypothesis of a driven trend towards increasingly active food acquisition which has been invoked to characterize early vertebrate evolution.

A new Meckel's cartilage from the Devonian Hangenberg black shale in Morocco and its position in chondrichthyan jaw morphospace.

Fossil chondrichthyan remains are mostly known from their teeth, scales or fin spines only, whereas their cartilaginous endoskeletons require exceptional preservational conditions to become fossilized. While most cartilaginous remains of Famennian (Late Devonian) chondrichthyans were found in older layers of the eastern Anti-Atlas, such fossils were unknown from the Hangenberg black shale (HBS) and only a few chondrichthyan teeth had been found therein previously. Here, we describe a Meckel's cartilage from the Hangenberg black shale in Morocco, which is the first fossil cartilage from these strata. Since no teeth or other skeletal elements have been found in articulation, we used elliptical Fourier (EFA), principal component (PCA), and hierarchical cluster (HCA) analyses to morphologically compare it with 41 chondrichthyan taxa of different size and age and to evaluate its possible systematic affiliation. PCA and HCA position the new specimen closest to some acanthodian and elasmobranch jaws. Accordingly, a holocephalan origin was excluded. The jaw shape as well as the presence of a polygonal pattern, typical for tessellated calcified cartilage, suggest a ctenacanth origin and we assigned the new HBS Meckel's cartilage to the order Ctenacanthiformes with reservations.

Galeaspid anatomy and the origin of vertebrate paired appendages.

Paired fins are a major innovation1,2 that evolved in the jawed vertebrate lineage after divergence from living jawless vertebrates3. Extinct jawless armoured stem gnathostomes show a diversity of paired body-wall extensions, ranging from skeletal processes to simple flaps4. By contrast, osteostracans (a sister group to jawed vertebrates) are interpreted to have the first true paired appendages in a pectoral position, with pelvic appendages evolving later in association with jaws5. Here we show, on the basis of articulated remains of Tujiaaspis vividus from the Silurian period of China, that galeaspids (a sister group to both osteostracans and jawed vertebrates) possessed three unpaired dorsal fins, an approximately symmetrical hypochordal tail and a pair of continuous, branchial-to-caudal ventrolateral fins. The ventrolateral fins are similar to paired fin flaps in other stem gnathostomes, and specifically to the ventrolateral ridges of cephalaspid osteostracans that also possess differentiated pectoral fins. The ventrolateral fins are compatible with aspects of the fin-fold hypothesis for the origin of vertebrate paired appendages6-10. Galeaspids have a precursor condition to osteostracans and jawed vertebrates in which paired fins arose initially as continuous pectoral-pelvic lateral fins that our computed fluid-dynamics experiments show passively generated lift. Only later in the stem lineage to osteostracans and jawed vertebrates did pectoral fins differentiate anteriorly. This later differentiation was followed by restriction of the remaining field of fin competence to a pelvic position, facilitating active propulsion and steering.

Evolutionary analysis of swimming speed in early vertebrates challenges the 'New Head Hypothesis'.

The ecological context of early vertebrate evolution is envisaged as a long-term trend towards increasingly active food acquisition and enhanced locomotory capabilities culminating in the emergence of jawed vertebrates. However, support for this hypothesis has been anecdotal and drawn almost exclusively from the ecology of living taxa, despite knowledge of extinct phylogenetic intermediates that can inform our understanding of this formative episode. Here we analyse the evolution of swimming speed in early vertebrates based on caudal fin morphology using ancestral state reconstruction and evolutionary model fitting. We predict the lowest and highest ancestral swimming speeds in jawed vertebrates and microsquamous jawless vertebrates, respectively, and find complex patterns of swimming speed evolution with no support for a trend towards more active lifestyles in the lineage leading to jawed groups. Our results challenge the hypothesis of an escalation of Palaeozoic marine ecosystems and shed light into the factors that determined the disparate palaeobiogeographic patterns of microsquamous versus macrosquamous armoured Palaeozoic jawless vertebrates. Ultimately, our results offer a new enriched perspective on the ecological context that underpinned the assembly of vertebrate and gnathostome body plans, supporting a more complex scenario characterized by diverse evolutionary locomotory capabilities reflecting their equally diverse ecologies.

Grouping behaviour impacts on the parasitic pressure and squamation of sharks.

The evolution of grouping behaviour involves a complex trade-off of benefits and costs. Among the latter, an increase in the risk of parasitic transmission is a well-documented phenomenon that has likely promoted the evolution of defensive mechanisms in aquatic vertebrates. Here, we explore the relationship between grouping behaviour, parasitic richness (∼parasitic pressure), and the evolution of potential defensive traits in the squamation of sharks through phylogenetic, standard and zero-inflation regression models. Our results demonstrate that sharks that frequently aggregate show increased parasitic pressure, which may constitute an agent of selection. Accordingly, their squamation is characterized by large-scale crown insertion angles and low-scale coverage, which are interpreted as traits that compromise parasite attachment and survival. These traits are less evident in regions of the body and ecological groups that are subjected to high abrasive stress or increased drag. Thus, the squamation of sharks responds to a compromise between various functions, where protective and hydrodynamic roles prevail over the rest (e.g. ectoparasitic defence and bioluminescence aiding). This work establishes a quantitative framework for inferring parasitic pressure and social interaction from squamation traits and provides an empirical basis from which to explore these phenomena through early vertebrate and chondrichthyan evolution.

Body-axis organization in tetrapods: a model-system to disentangle the developmental origins of convergent evolution in deep time.

Convergent evolution is a central concept in evolutionary theory but the underlying mechanism has been largely debated since On the Origin of Species. Previous hypotheses predict that developmental constraints make some morphologies more likely to arise than others and natural selection discards those of the lowest fitness. However, the quantification of the role and strength of natural selection and developmental constraint in shaping convergent phenotypes on macroevolutionary timescales is challenging because the information regarding performance and development is not directly available. Accordingly, current knowledge of how embryonic development and natural selection drive phenotypic evolution in vertebrates has been extended from studies performed at short temporal scales. We propose here the organization of the tetrapod body-axis as a model system to investigate the developmental origins of convergent evolution over hundreds of millions of years. The quantification of the primary developmental mechanisms driving body-axis organization (i.e. somitogenesis, homeotic effects and differential growth) can be inferred from vertebral counts, and recent techniques of three-dimensional computational biomechanics have the necessary potential to reveal organismal performance even in fossil forms. The combination of both approaches offers a novel and robust methodological framework to test competing hypotheses on the functional and developmental drivers of phenotypic evolution and evolutionary convergence.

Biomechanical insights into the dentition of megatooth sharks (Lamniformes: Otodontidae).

The evolution of gigantism in extinct otodontid sharks was paralleled by a series of drastic modifications in their dentition including widening of the crowns, loss of lateral cusplets, and acquisition of serrated cutting edges. These traits have generally been interpreted as key functional features that enabled the transition from piscivory to more energetic diets based on marine mammals, ultimately leading to the evolution of titanic body sizes in the most recent forms (including the emblematic Otodus megalodon). To investigate this hypothesis, we evaluate the biomechanics of the anterior, lateral, and posterior teeth of five otodontid species under different loading conditions by using two-dimensional finite element analysis. Stress distribution patterns are remarkably similar among all models under puncture and draw (i.e., when subjected to vertical and lateral forces, respectively). Contrary to expectation, higher average stress values are detected under both loading scenarios in more recent species. Altogether, this suggests little correlation between tooth morphology and key aspects of biomechanical behaviour in otodontids, making it difficult to frame the morphological trend of their dentitions within an adaptive scenario. We propose that this pattern most likely emerged as a non-functional by-product of heterochronic processes driven by selection towards larger body sizes.

Functional assessment of morphological homoplasy in stem-gnathostomes.

Osteostraci and Galeaspida are stem-gnathostomes, occupying a key phylogenetic position for resolving the nature of the jawless ancestor from which jawed vertebrates evolved more than 400 million years ago. Both groups are characterized by the presence of rigid headshields that share a number of common morphological traits, in some cases hindering the resolution of their interrelationships and the exact nature of their affinities with jawed vertebrates. Here, we explore the morphological and functional diversity of osteostracan and galeaspid headshields using geometric morphometrics and computational fluid dynamics to constrain the factors that promoted the evolution of their similar morphologies and informing on the ecological scenario under which jawed vertebrates emerged. Phylomorphospace, Mantel analysis and Stayton metrics demonstrate a high degree of homoplasy. Computational fluid dynamics reveals similar hydrodynamic performance among morphologically convergent species, indicating the independent acquisition of the same morphofunctional traits and, potentially, equivalent lifestyles. These results confirm that a number of the characters typically used to infer the evolutionary relationships among galeaspids, osteostracans and jawed vertebrates are convergent in nature, potentially obscuring understanding of the assembly of the gnathostome bodyplan. Ultimately, our results reveal that while the jawless relatives of the earliest jawed vertebrates were ecologically diverse, widespread convergence on the same hydrodynamic adaptations suggests they had reached the limits of their potential ecological diversity-overcome by jawed vertebrates and their later innovations.

Use of nursery areas by the extinct megatooth shark Otodus megalodon (Chondrichthyes: Lamniformes).

Nursery areas are fundamental for the success of many marine species, particularly for large, slow-growing taxa with low fecundity and high age of maturity. Here, we examine the population size-class structure of the extinct gigantic shark Otodus megalodon in a newly described middle Miocene locality from Northeastern Spain, as well as in eight previously known formations (Temblor, Calvert, Pisco, Gatún, Chucunaque, Bahía Inglesa, Yorktown and Bone Valley). In all cases, body lengths of all individuals were inferred from dental parameters and the size-class structure was estimated from kernel probability density functions and Gaussian mixture models. Our analyses support the presence of five potential nurseries ranging from the Langhian (middle Miocene) to the Zanclean (Pliocene), with higher densities of individuals with estimated body lengths within the typical range of neonates and young juveniles. These results reveal, for the first time, that nursery areas were commonly used by O. megalodon over large temporal and spatial scales, reducing early mortality and playing a key role in maintaining viable adult populations. Ultimately, the presumed reliance of O. megalodon on the presence of suitable nursery grounds might have also been determinant in the demise of this iconic top predatory shark.

Computational Fluid Dynamics Suggests Ecological Diversification among Stem-Gnathostomes.

The evolutionary assembly of the vertebrate bodyplan has been characterized as a long-term ecological trend toward increasingly active and predatory lifestyles, culminating in jawed vertebrates that dominate modern vertebrate biodiversity [1-8]. This contrast is no more stark than between the earliest jawed vertebrates and their immediate relatives, the extinct jawless, dermal armor-encased osteostracans, which have conventionally been interpreted as benthic mud-grubbers with poor swimming capabilities and low maneuverability [9-12]. Using computational fluid dynamics, we show that osteostracan headshield morphology is compatible with a diversity of hydrodynamic efficiencies including passive control of water flow around the body; these could have increased versatility for adopting diverse locomotor strategies. Hydrodynamic performance varies with morphology, proximity to the substrate, and angle of attack (inclination). Morphotypes with dorsoventrally oblate headshields are hydrodynamically more efficient when swimming close to the substrate, whereas those with dorsoventrally more prolate headshields exhibit maximum hydrodynamic efficiency when swimming free from substrate effects. These results suggest different hydrofoil functions among osteostracan headshield morphologies, compatible with ecological diversification and undermining the traditional view that jawless stem-gnathostomes were ecologically constrained [9-12] with the origin of jaws as the key innovation that precipitated the ecological diversification of the group [13, 14].

Body dimensions of the extinct giant shark Otodus megalodon: a 2D reconstruction.

Inferring the size of extinct animals is fraught with danger, especially when they were much larger than their modern relatives. Such extrapolations are particularly risky when allometry is present. The extinct giant shark †Otodus megalodon is known almost exclusively from fossilised teeth. Estimates of †O. megalodon body size have been made from its teeth, using the great white shark (Carcharodon carcharias) as the only modern analogue. This can be problematic as the two species likely belong to different families, and the position of the †Otodus lineage within Lamniformes is unclear. Here, we infer †O. megalodon body dimensions based on anatomical measurements of five ecologically and physiologically similar extant lamniforms: Carcharodon carcharias, Isurus oxyrinchus, Isurus paucus, Lamna ditropis and Lamna nasus. We first assessed for allometry in all analogues using linear regressions and geometric morphometric analyses. Finding no evidence of allometry, we made morphological extrapolations to infer body dimensions of †O. megalodon at different sizes. Our results suggest that a 16 m †O. megalodon likely had a head ~ 4.65 m long, a dorsal fin ~ 1.62 m tall and a tail ~ 3.85 m high. Morphometric analyses further suggest that its dorsal and caudal fins were adapted for swift predatory locomotion and long-swimming periods.

Ecomorphological inferences in early vertebrates: reconstructing Dunkleosteus terrelli (Arthrodira, Placodermi) caudal fin from palaeoecological data.

Our knowledge about the body morphology of many extinct early vertebrates is very limited, especially in regard to their post-thoracic region. The prompt disarticulation of the dermo-skeletal elements due to taphonomic processes and the lack of a well-ossified endoskeleton in a large number of groups hinder the preservation of complete specimens. Previous reconstructions of most early vertebrates known from partial remains have been wholly based on phylogenetically closely related taxa. However, body design of fishes is determined, to a large extent, by their swimming mode and feeding niche, making it possible to recognise different morphological traits that have evolved several times in non-closely related groups with similar lifestyles. Based on this well-known ecomorphological correlation, here we propose a useful comparative framework established on extant taxa for predicting some anatomical aspects in extinct aquatic vertebrates from palaeoecological data and vice versa. For this, we have assessed the relationship between the locomotory patterns and the morphological variability of the caudal region in extant sharks by means of geometric morphometrics and allometric regression analysis. Multivariate analyses reveal a strong morphological convergence in non-closely related shark species that share similar modes of life, enabling the characterization of the caudal fin morphology of different ecological subgroups. In addition, interspecific positive allometry, affecting mainly the caudal fin span, has been detected. This phenomenon seems to be stronger in sharks with more pelagic habits, supporting its role as a compensation mechanism for the loss of hydrodynamic lift associated with the increase in body size, as previously suggested for many other living and extinct aquatic vertebrates. The quantification of shape change per unit size in each ecological subgroup has allowed us to establish a basis for inferring not only qualitative aspects of the caudal fin morphology of extinct early vertebrates but also to predict absolute values of other variables such as the fin span or the hypocercal and heterocercal angles. The application of this ecomorphological approach to the specific case of Dunkleosteus terrelli has led to a new reconstruction of this emblematic placoderm. Our proposal suggests a caudal fin with a well-developed ventral lobe, narrow peduncle and wide span, in contrast to classical reconstructions founded on the phylogenetic proximity with much smaller placoderms known from complete specimens. Interestingly, this prediction gains support with the recent discovery of fin distal elements (ceratotrichia) in a well preserved D. terrelli, which suggests a possible greater morphological variability in placoderm caudal fins than previously thought.

Regional endothermy as a trigger for gigantism in some extinct macropredatory sharks.

Otodontids include some of the largest macropredatory sharks that ever lived, the most extreme case being Otodus (Megaselachus) megalodon. The reasons underlying their gigantism, distribution patterns and extinction have been classically linked with climatic factors and the evolution, radiation and migrations of cetaceans during the Paleogene. However, most of these previous proposals are based on the idea of otodontids as ectothermic sharks regardless of the ecological, energetic and body size constraints that this implies. Interestingly, a few recent studies have suggested the possible existence of endothermy in these sharks thus opening the door to a series of new interpretations. Accordingly, this work proposes that regional endothermy was present in otodontids and some closely related taxa (cretoxyrhinids), playing an important role in the evolution of gigantism and in allowing an active mode of live. The existence of regional endothermy in these groups is supported here by three different approaches including isotopic-based approximations, swimming speed inferences and the application of a novel methodology for assessing energetic budget and cost of swimming in extinct taxa. In addition, this finding has wider implications. It calls into question some previous paleotemperature estimates based partially on these taxa, suggests that the existing hypothesis about the evolution of regional endothermy in fishes requires modification, and provides key evidence for understanding the evolution of gigantism in active macropredators.

Squamation and ecology of thelodonts.

Thelodonts are an enigmatic group of Paleozoic jawless vertebrates that have been well studied from taxonomical, biostratigraphic and paleogeographic points of view, although our knowledge of their ecology and mode of life is still scant. Their bodies were covered by micrometric scales whose morphology, histology and the developmental process are extremely similar to those of extant sharks. Based on these similarities and on the well-recognized relationship between squamation and ecology in sharks, here we explore the ecological diversity and lifestyles of thelodonts. For this we use classic morphometrics and discriminant analysis to characterize the squamation patterns of a significant number of extant shark species whose ecology is well known. Multivariate analyses have defined a characteristic squamation pattern for each ecological group, thus establishing a comparative framework for inferring lifestyles in thelodonts. We then use this information to study the squamation of the currently described 147 species of thelodonts, known from both articulated and disarticulated remains. Discriminant analysis has allowed recognizing squamation patterns comparable to those of sharks and links them to specific ecological groups. Our results suggest a remarkable ecological diversity in thelodonts. A large number of them were probably demersal species inhabiting hard substrates, within caves and crevices in rocky environments or reefs, taking advantage of the flexibility provided by their micromeric squamations. Contrary to classical interpretations, only few thelodonts were placed among demersal species inhabiting sandy and muddy substrates. Schooling species with defensive scales against ectoparasites could be also abundant suggesting that social interactions and pressure of ectoparasites were present in vertebrates as early the Silurian. The presence of species showing scales suggestive of low to moderate speed and a lifestyle presumably associated with open water environments indicates adaptation of thelodonts to deep water habitats. Scale morphology suggests that some other thelodonts were strong-swimming pelagic species, most of them radiating during the Early Devonian in association with the Nekton Revolution.