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

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

Pre-Messinian ecological diversity of Mediterranean sharks revealed by the study of their dermal denticles

The Messinian salinity crisis (~5.59 Ma) is regarded as one of the most determining events for the recent evolutionary and palaeobiogeographic history of the Mediterranean biota. The impact of such episode has usually been assessed by evaluating the associated taxonomic turnover, however its consequences have rarely been interpreted from an ecological perspective. Here we assess the functional diversity of shark dermal denticles in a Serravallian locality from southeast Spain, providing a primary view into the pre-Messinian ecological diversity of shark communities from the Western Mediterranean. Our results reveal a high diversity of functional types of dermal denticles including dermal denticles that prevent the settlement of ectoparasites and epibiontes, abrasion resistant dermal denticles, drag reduction dermal denticles and dermal denticles with less specific, or more generalized, functions. This variety of dermal denticles supports the presence of several ecological groups of sharks such as schooling and strong swimming species and, possibly, demersal species, slow sharks of the open water bioluminescent taxa. Therefore, the application of this methodology to Pliocene and Pleistocene fossiliferous sites will be crucial for unravelling the impact of Messinian salinity crisis and other recent geological events from an ecological perspective, allowing us to understand the shark communitycompositionand diversityof the current Mediterranean Sea

Testing hypotheses of pteraspid heterostracan feeding using computational fluid dynamics

The ecological context of early vertebrate evolution has been characterized as a gradual shift from passive to more active feeding modes. This evolutionary scenario has been based largely on poorly constrained inferences of the feeding ecology of extinct stem-gnathostomes, among which heterostracans are the earliest. Pteraspidiform heterostracans possessed a feeding apparatus composed of rod-like oral plates with rows of rostrally facing denticles, previously interpreted as an adaptation for suspension feeding. Here, we test this hypothesis using computational fluid dynamics. We simulate water flow around 2D models consisting of rows of denticles both rostrally facing and reversed, to assess whether these orientations create recirculation patterns that are a hydrodynamic adaptation to suspension feeding. All tested models, independent of denticle orientation, show similar flow, velocity, and vorticity patterns. Recirculation patterns, highest velocity, and vorticity develop directly on top of the denticles and in spaces between the denticles. Therefore, we reject the hypothesis that denticle orientation is an adaptation for recirculation linked to suspension feeding. The denticles may instead have served to prevent material from lodging between the plates