A shark-inspired general model of tooth morphogenesis unveils developmental asymmetries in phenotype transitions.

Developmental complexity stemming from the dynamic interplay between genetic and biomechanic factors canalizes the ways genotypes and phenotypes can change in evolution. As a paradigmatic system, we explore how changes in developmental factors generate typical tooth shape transitions. Since tooth development has mainly been researched in mammals, we contribute to a more general understanding by studying the development of tooth diversity in sharks. To this end, we build a general, but realistic, mathematical model of odontogenesis. We show that it reproduces key shark-specific features of tooth development as well as real tooth shape variation in small-spotted catsharks Scyliorhinus canicula. We validate our model by comparison with experiments in vivo. Strikingly, we observe that developmental transitions between tooth shapes tend to be highly degenerate, even for complex phenotypes. We also discover that the sets of developmental parameters involved in tooth shape transitions tend to depend asymmetrically on the direction of that transition. Together, our findings provide a valuable base for furthering our understanding of how developmental changes can lead to both adaptive phenotypic change and trait convergence in complex, phenotypically highly diverse, structures.

A Unitary Association-based conodont biozonation of the Smithian-Spathian boundary (Early Triassic) and associated biotic crisis from South China.

The Smithian-Spathian boundary (SSB) crisis played a prominent role in resetting the evolution and diversity of the nekton (ammonoids and conodonts) during the Early Triassic recovery. The late Smithian nektonic crisis culminated at the SSB, ca. 2.7 Myr after the Permian-Triassic boundary mass extinction. An accurate and high-resolution biochronological frame is needed for establishing patterns of extinction and re-diversification of this crisis. Here, we propose a new biochronological frame for conodonts that is based on the Unitary Associations Method (UAM). In this new time frame, the SSB can thus be placed between the climax of the extinction and the onset of the re-diversification. Based on the study of new and rich conodont collections obtained from five sections (of which four are newly described here) in the Nanpanjiang Basin, South China, we have performed a thorough taxonomical revision and described one new genus and 21 new species. Additionally, we have critically reassessed the published conodont data from 16 other sections from South China, and we have used this new, standardized dataset to construct the most accurate, highly resolved, and laterally reproducible biozonation of the Smithian to early Spathian interval for South China. The resulting 11 Unitary Association Zones (UAZ) are intercalibrated with lithological and chemostratigraphical (δ13Ccarb) markers, as well as with ammonoid zones, thus providing a firm basis for an evolutionary meaningful and laterally consistent definition of the SSB. Our UAZ8, which is characterized by the occurrence of Icriospathodus ex gr. crassatus, Triassospathodus symmetricus and Novispathodus brevissimus, is marked by a new evolutionary radiation of both conodonts and ammonoids and is within a positive peak in the carbon isotope record. Consequently, we propose to place the SSB within the separation interval intercalated between UAZ7 and UAZ8 thus leaving some flexibility for future refinement and updating. Supplementary Information: The online version contains supplementary material available at 10.1186/s13358-022-00259-x.

Temperature-driven heterochrony as a main evolutionary response to climate changes in conodonts.

Can we predict the evolutionary response of organisms to climate changes? The direction of greatest intraspecific phenotypic variance is thought to correspond to an 'evolutionary line of least resistance', i.e. a taxon's phenotype is expected to evolve along that general direction, if not constrained otherwise. In particular, heterochrony, whereby the timing or rate of developmental processes are modified, has often been invoked to describe evolutionary trajectories and it may be advantageous to organisms when rapid adaptation is critical. Yet, to date, little is known empirically as to which covariation patterns, whether static allometry, as measured in adult forms only, or ontogenetic allometry, the basis for heterochrony, may be prevalent in what circumstances. Here, we quantify the morphology of segminiplanate conodont elements during two distinct time intervals separated by more than 130 Myr: the Devonian-Carboniferous boundary and the Carnian-Norian boundary (Late Triassic). We evidence that the corresponding species share similar patterns of intraspecific static allometry. Yet, during both crises, conodont evolution was decoupled from this common evolutionary line of least resistance. Instead, it followed heterochrony-like trajectories that furthermore appear as driven by ocean temperature. This may have implications for our interpretation of conodonts' and past marine ecosystems' response to environmental perturbations.

Hide and seek shark teeth in Random Forests: machine learning applied to Scyliorhinus canicula populations.

Shark populations that are distributed alongside a latitudinal gradient often display body size differences at sexual maturity and vicariance patterns related to their number of tooth files. Previous works have demonstrated that Scyliorhinus canicula populations differ between the northeastern Atlantic Ocean and the Mediterranean Sea based on biological features and genetic analysis. In this study, we sample more than 3,000 teeth from 56 S. canicula specimens caught incidentally off Roscoff and Banyuls-sur-Mer. We investigate population differences based on tooth shape and form by using two approaches. Classification results show that the classical geometric morphometric framework is outperformed by an original Random Forests-based framework. Visually, both S. canicula populations share similar ontogenetic trends and timing of gynandric heterodonty emergence but the Atlantic population has bigger, blunter teeth, and less numerous accessory cusps than the Mediterranean population. According to the models, the populations are best differentiated based on their lateral tooth edges, which bear accessory cusps, and the tooth centroid sizes significantly improve classification performances. The differences observed are discussed in light of dietary and behavioural habits of the populations considered. The method proposed in this study could be further adapted to complement DNA analyses to identify shark species or populations based on tooth morphologies. This process would be of particular interest for fisheries management and identification of shark fossils.

Exceptional fossil assemblages confirm the existence of complex Early Triassic ecosystems during the early Spathian.

The mass extinction characterizing the Permian/Triassic boundary (PTB; ~ 252 Ma) corresponds to a major faunal shift between the Palaeozoic and the Modern evolutionary fauna. The temporal, spatial, environmental, and ecological dynamics of the associated biotic recovery remain highly debated, partly due to the scarce, or poorly-known, Early Triassic fossil record. Recently, an exceptionally complex ecosystem dated from immediately after the Smithian/Spathian boundary (~ 3 myr after the PTB) was reported: the Paris Biota (Idaho, USA). However, the spatiotemporal representativeness of this unique assemblage remained questionable as it was hitherto only reported from a single site. Here we describe three new exceptionally diverse assemblages of the same age as the Paris Biota, and a fourth younger one. They are located in Idaho and Nevada, and are taxonomic subsets of the Paris Biota. We show that the latter covered a region-wide area and persisted at least partially throughout the Spathian. The presence of a well-established marine fauna such as the Paris Biota, as soon as the early Spathian, indicates that the post-PTB biotic recovery and the installation of complex ecosystems probably took place earlier than often assumed, at least at a regional scale.

The intraspecific diversity of tooth morphology in the large-spotted catshark Scyliorhinus stellaris: insights into the ontogenetic cues driving sexual dimorphism.

Teeth in sharks are shed and replaced throughout their lifetime. Morphological dental changes through ontogeny have been identified in several species and have been correlated with shifts in diet and the acquisition of sexual maturity. However, these changes were rarely quantified in detail along multiple ontogenetic stages, which makes it difficult to infer the developmental processes responsible for the observed plasticity. In this work, we use micro-computed tomography and 3D geometric morphometrics to describe and analyze the tooth size and shape diversity across three ontogenetic stages (hatchling, juvenile, and sexually mature) in the large-spotted catshark Scyliorhinus stellaris (Linnaeus, 1758). We first describe the intra-individual variation of tooth form for each sex at each ontogenetic stage. We provide a tooth morphospace for palatoquadrate and Meckelian teeth and identify dental features, such as relative size and number of cusps, involved in the range of variation of the observed morphologies. We then use these shape data to draw developmental trajectories between ontogenetic stages and for each tooth position within the jaw to characterize ontogenetic patterns of sexual dimorphism. We highlight the emergence of gynandric heterodonty between the juvenile and mature ontogenetic stages, with mature females having tooth morphologies more similar to juveniles' than mature males that display regression in the number of accessory cusps. From these data, we speculate on the developmental processes that could account for such developmental plasticity in S. stellaris.

Learning from beautiful monsters: phylogenetic and morphogenetic implications of left-right asymmetry in ammonoid shells.

BACKGROUND: Many pathologies that modify the shell geometry and ornamentation of ammonoids are known from the fossil record. Since they may reflect the developmental response of the organism to a perturbation (usually a sublethal injury), their study is essential for exploring the developmental mechanisms of these extinct animals. Ammonoid pathologies are also useful to assess the value of some morphological characters used in taxonomy, as well as to improve phylogenetic reconstructions and evolutionary scenarios. RESULTS: We report on the discovery of an enigmatic pathological middle Toarcian (Lower Jurassic) ammonoid specimen from southern France, characterized by a pronounced left-right asymmetry in both ornamentation and suture lines. For each side independently, the taxonomic interpretations of ornamentation and suture lines are congruent, suggesting a Hildoceras semipolitum species assignment for the left side and a Brodieia primaria species assignment for the right side. The former exhibits a lateral groove whereas the second displays sinuous ribs. This specimen, together with the few analogous cases reported in the literature, lead us to erect a new forma-type pathology herein called "forma janusa" for specimens displaying a left-right asymmetry in the absence of any clear evidence of injury or parasitism, whereby the two sides match with the regular morphology of two distinct, known species. CONCLUSIONS: Since "forma janusa" specimens reflect the underlying developmental plasticity of the ammonoid taxa, we hypothesize that such specimens may also indicate unsuspected phylogenetic closeness between the two displayed taxa and may even reveal a direct ancestor-descendant relationship. This hypothesis is not, as yet, contradicted by the stratigraphical data at hand: in all studied cases the two distinct taxa correspond to contemporaneous or sub-contemporaneous taxa. More generally, the newly described specimen suggests that a hitherto unidentified developmental link may exist between sinuous ribs and lateral grooves. Overall, we recommend an integrative approach for revisiting aberrant individuals that illustrate the intricate links among shell morphogenesis, developmental plasticity and phylogeny.

Unexpected Early Triassic marine ecosystem and the rise of the Modern evolutionary fauna.

In the wake of the end-Permian mass extinction, the Early Triassic (~251.9 to 247 million years ago) is portrayed as an environmentally unstable interval characterized by several biotic crises and heavily depauperate marine benthic ecosystems. We describe a new fossil assemblage-the Paris Biota-from the earliest Spathian (middle Olenekian, ~250.6 million years ago) of the Bear Lake area, southeastern Idaho, USA. This highly diversified assemblage documents a remarkably complex marine ecosystem including at least seven phyla and 20 distinct metazoan orders, along with algae. Most unexpectedly, it combines early Paleozoic and middle Mesozoic taxa previously unknown from the Triassic strata, among which are primitive Cambrian-Ordovician leptomitid sponges (a 200-million year Lazarus taxon) and gladius-bearing coleoid cephalopods, a poorly documented group before the Jurassic (~50 million years after the Early Triassic). Additionally, the crinoid and ophiuroid specimens show derived anatomical characters that were thought to have evolved much later. Unlike previous works that suggested a sluggish postcrisis recovery and a low diversity for the Early Triassic benthic organisms, the unexpected composition of this exceptional assemblage points toward an early and rapid post-Permian diversification for these clades. Overall, it illustrates a phylogenetically diverse, functionally complex, and trophically multileveled marine ecosystem, from primary producers up to top predators and potential scavengers. Hence, the Paris Biota highlights the key evolutionary position of Early Triassic fossil ecosystems in the transition from the Paleozoic to the Modern marine evolutionary fauna at the dawn of the Mesozoic era.

Synchrotron-aided reconstruction of the conodont feeding apparatus and implications for the mouth of the first vertebrates.

The origin of jaws remains largely an enigma that is best addressed by studying fossil and living jawless vertebrates. Conodonts were eel-shaped jawless animals, whose vertebrate affinity is still disputed. The geometrical analysis of exceptional three-dimensionally preserved clusters of oro-pharyngeal elements of the Early Triassic Novispathodus, imaged using propagation phase-contrast X-ray synchrotron microtomography, suggests the presence of a pulley-shaped lingual cartilage similar to that of extant cyclostomes within the feeding apparatus of euconodonts ("true" conodonts). This would lend strong support to their interpretation as vertebrates and demonstrates that the presence of such cartilage is a plesiomorphic condition of crown vertebrates.

Allometries and the morphogenesis of the molluscan shell: a quantitative and theoretical model.

This article explores the close relationships between growth rate and allometries of molluscan shells. After reviewing the previous theoretical approaches devoted to the understanding of shell form and its morphogenesis, we present a free-form vector model which can simulate apertural shape changes and nonlinear allometries. Shell morphology is generated by iteratively adding a growth increment onto the last computed aperture. The first growth increment defines so-called growth vectors which are assumed to be constant in direction (relative to the last computed aperture position) during a simulation of a shell (ontogeny). These growth vectors are uniformly scaled at each time step according to various growth rate curves that are used to simulate the mantle growth over time. From the model, we derive morphometric variables that illustrate the ontogenetic trajectories in time-size-shape space. We investigate the effects of changing the growth curves types, growth rate parameters and growth vector maps on the direction, speed and patterns of ontogenetic allometries. Because this model focuses the issue on time, it highlights a plausible effect of growth rate on shell shape and illustrates some fundamental geometrical properties of the logarithmic spiral, in particular the close relationship between the size and the geometry of growth increments. This model could be used to develop a mathematically data-driven approach where experimentally obtained growth curves could be used as inputs in the model. More generally, our study recalls the role of growth rates in the generation of allometries.

Growth-dependent phenotypic variation of molluscan shells: implications for allometric data interpretation.

In recent years, developmental plasticity has received increasing attention. Specifically, some studies highlighted a possible association between shell shape and growth rates in intertidal gastropods. We use a growth vector model to study how hypothetical growth processes could underlie developmental plasticity in molluscs. It illustrates that variation in instantaneous shell growth rate can induce variability in allometric curves. Consequently, morphological variation is time-dependent. Basing our model parameters on a study documenting the results of transplants experiments of three gastropods ecomorphs, we reproduce the main aspects of the variation in size, shape, and growth rates among populations when bred in their own habitat or transplanted to another ecotype habitat. In agreement with empirical results, our simulation shows that a flatter growth profile corresponds to conditions of rapid growth. The model also allows the comparison of allometric slopes using different subdata sets that correspond to static and ontogenetic allometry. Our model highlights that depending on subdata sets, the "main effects" could be attributed to source population or environment. In addition, convergence or divergence of allometric slopes is observed depending on the subdata sets. Although there is evidence that shell shape in gastropods is to some extent growth rate dependent, gaining a general overview of the issue is challenging, in particular because of the scarcity of studies referring to allometry. We argue that the dynamics of development at the "phenotypic level" constitute a non-reducible level of investigation if one seeks to relate the observed amount of phenotypic variation to variability in the underlying factors.

Good genes and good luck: ammonoid diversity and the end-Permian mass extinction.

The end-Permian mass extinction removed more than 80% of marine genera. Ammonoid cephalopods were among the organisms most affected by this crisis. The analysis of a global diversity data set of ammonoid genera covering about 106 million years centered on the Permian-Triassic boundary (PTB) shows that Triassic ammonoids actually reached levels of diversity higher than in the Permian less than 2 million years after the PTB. The data favor a hierarchical rather than logistic model of diversification coupled with a niche incumbency hypothesis. This explosive and nondelayed diversification contrasts with the slow and delayed character of the Triassic biotic recovery as currently illustrated for other, mainly benthic groups such as bivalves and gastropods.

Theoretical investigations on dual-beam illumination electronic speckle pattern interferometry.

Contrary to what is found in most of the existing scientific literature, where a specific frame is developed, the theory of speckle interferometry is (conveniently) presented here as a particular case of the more general theory of holographic interferometry. In addition to the intellectual benefit of dealing with a single unified theory, this brings about many advantages when it comes to discuss fundamental topics such as the three-dimensional evolution of the complex amplitude of the diffuse optical wavefronts, the degree of approximation of the leading formulas, the loss of fringe contrast, the decorrelation effects, the real influence of the terms generally neglected in out-of-focus regions. In the same way, the statistical properties of the speckle fields, usually treated as a separate subject matter, are also integrated in the theory, thus providing a comprehensive knowledge of the qualitative features of speckle interferometry methods, otherwise difficult to understand.

Application of dynamic phase shifting with wavelet analysis to electronic speckle contouring.

Dynamic phase shifting is a temporal phase unwrapping method, i.e., a method in which a sequence of speckle patterns is analyzed along the time axis. Each pixel can thus be considered as an independent detector, which is of particular interest for the study of complex surfaces. I report the application of this technique, which is based on a wavelet analysis, to contouring measurements with a dual-beam illumination electronic speckle pattern interferometry setup. I present a new, more general geometric model of the setup. I also investigate the possibility of enhancing the accuracy by using the intermediate phase values. Tests are performed on a simply described object and compared with coordinate measuring machine measurements.