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

Abstract 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

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

Biomechanics of <i>Machaeracanthus</i> pectoral fin spines provide evidence for distinctive spine function and lifestyle among early chondrichthyans

Acanthodians are a major group of Paleaozoic jawed vertebrates that constitute a paraphyletic assemblage of stem-chondrichthyans (Brazeau and Friedman, 2015). Representatives of this group are characterized, among other traits, by the presence of bony spines in front of all paired and median fins except the caudal (Denison, 1979), which has given rise to their colloquial name of 'spiny sharks'. The occurrence of pectoral fin spines is recognized as a potential gnathostome synapomorphy (Miller et al., 2003) or symplesiomorphy (Coates, 2003), being also present in other major groups of Paleaozoic jawed vertebrates, including placoderms (Young, 2010), 'non-acanthodian' chondrichthyans (Miller et al., 2003), and osteichthyans (Zhu et al., 1999). However, this trait was independently lost in the later evolutionary history of these lineages and is absent in most living representatives (Coates, 2003; Miller et al., 2003), with the exception of catfishes (Siluriformes), that acquired pectoral fin spines as an evolutionary reversion (Price et al., 2015). As a consequence, the paucity of living analogsue precludes deriving functional interpretations of those structures and the role that they fulfilled in life remains unclear, despite this having the potential to enrich our understanding on the ecologies and lifestyles of groups of early jawed vertebrates. Machaeracanthus constitutes a genus of acanthodians that ranged from the Late Silurian to the Middle Devonian, which is known from fin spines, scales, and a few endoskeletal remains (Burrow et al., 2010; Botella et al., 2012). The spines of this genus differ from the fin spines of all other acanthodians and sharks in presenting a marked cross-sectional asymmetry and a totally enclosed central canal, which is usually open along the proximal end of the trailing edge in other taxa (Burrow et al., 2010). The description of wear patterns at the tips of pectoral fin spines of Machaeracanthus and their peculiar arrangement in pairs has led some authors to propose that these elements could have been used as 'snow-shoes' to lay on and prevent sinking into the substrate below or even to propel itself along the bottom (Südkamp and Burrow, 2007). Here, we test this hypothesis through beam theory analyses and provide evidence that the biomechanical properties of Machaeracanthus pectoral fin spines are compatible with this interpretation, thus shedding light on the diversity of the functions of these intriguing anatomical structures and the lifestyles of some of the earliest jawed vertebrates

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

Vascular structure of the earliest shark teeth

Here we use synchrotron tomography to characterise dental vasculature in the oldest known tooth-bearing sharks, Leonodus carlsi Mader, 1986 and Celtiberina maderi Wang, 1993. Three dimensional reconstruction of the vascular system and microstructure of both taxa revealed a complex and dense network of canals, including horizontal, ascending and secondary bifurcated canals, as well as histological features consistent with an osteodont histotype. However, L. carlsi and C. maderi also exhibit significant morphological differences, showing Leonodus a typical diplodont tooth morphology with a linguo-labially elongated base, that contrast with Celtiberina’s teeth that show a single conical cusp curved lingually with a week developed flat base mesio-distally extended, perhaps reflecting distant relationship. These data are compatible with a pre-Devonian diversification of the two main tooth types traditionally recognised in Palaeozoic sharks (i.e., “cladodont” vs “diplodont”). Finally, our data demonstrate that existing dental classification schemes based on styles of vascularisation are over-simplified, especially when Palaeozoic taxa are considered

Categorical versus geometric morphometric approaches to characterizing the evolution of morphological disparity in Osteostraci (Vertebrata, stem Gnathostomata)

Morphological variation (disparity) tends to be evaluated through two non-mutually exclusive approaches: (i) quantitatively, through geometric morphometrics, and (ii) in terms of discrete, ‘cladistic’, or categorical characters. Uncertainty over the comparability of these approaches diminishes the potential to obtain nomothetic insights into the evolution of morphological disparity, and the few benchmarking studies conducted so far show contrasting results. Here, we apply both approaches to characterising morphology in the stem-gnathostome vertebrate clade Osteostraci, in order to assess congruence between these alternative methods as well as to explore the evolutionary patterns of the group in terms of temporal disparity and the influence of phylogenetic relationships and habitat on morphospace occupation. Our results suggest that both approaches yield similar results in morphospace occupation and clustering, but also some differences indicating that these metrics may capture different aspects of morphology. Phylomorphospaces reveal important convergence towards a generalised ‘horseshoe’-shaped cranial morphology and two strong branching trends involving different major groups of osteostracans (benneviaspidids and thyestiids), which probably reflect adaptations to different lifestyles. Temporal patterns of disparity recorded by categorical and morphometric approaches differ considerably, capturing disparity maxima at very different times of the evolutionary history of the group. Disparity patterns recorded by the categorical approach parallel taxonomic diversity dynamics, likely reflecting a bias in facies representation rather than a real biological signal. This work provides evidence supporting that categorical and continuous data do not always capture morphological disparity in equivalent ways and that discrepancies reflect differences in the potential of each data type for characterizing more or less inclusive aspects of overall phenotype

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

Identification of a Nidovirales Orf1a N7-guanine cap Methyltransferase signature- sequence as a genetic marker of large genome Tobaniviridae Running title: RNA cap N7-guanine Methyltransferase in Tobaniviridae Orf1a

Members of the Nidoviralesorder have (+)RNA genomes amongstthe largest in size in the RNA virus world. Expression of their genes is promoted through reading of genomic RNA and mRNA transcripts by the ribosome of the infected cell. The 5'-end of these RNAs is supposedly protected by an RNA-cap structure (m7GpppNm) whose most synthesis steps remain elusive. In Eukaryotes, the RNA-cap structure is methylated by RNA methyltransferases (MTases) at the RNA-cap N7-guanine position as well as the 2'-O methyl position of the first transcribed nucleotide. In Coronaviridae, two separate enzymes (nsp14 and nsp16) perform the N7-guanine and the 2'-OH methylation, respectively. One salient feature of the Nidovirales N7-guanine MTase nsp14 is that it is the only example of non-Rossman fold viral MTase known so far. Conversely, all other Nidoviralesnsp16-like MTases have a canonical Rossman fold. Many Nidoviralesmembers lack either any RNA MTase signature sequence (e.g., Arteriviridae), or lack a N7-guanine MTase signature sequence (e.g., Tobaniviridae, Euroniviridae, Roniviridae, Medioniviridae). Both nsp14-and nsp16-like enzyme genes are usually located in Orf1b encoding for the replication machinery. Here, we report the discovery of a putative Rossman fold RNA MTase in the Orf1a of ten Tobaniviridaemembers. Multiple sequence alignments and structural analyses identify this novel gene as a typical RNA-cap N7-guanine MTase with substrate specificity and active-site organization similar to the canonical eukaryotic RNA-cap N7-guanine MTase