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Mechanics unlocks the morphogenetic puzzle of interlocking bivalved shells.

ABSTRACT: Brachiopods and mollusks are 2 shell-bearing phyla that diverged from a common shell-less ancestor more than 540 million years ago. Brachiopods and bivalve mollusks have also convergently evolved a bivalved shell that displays an apparently mundane, yet striking feature from a developmental point of view: When the shell is closed, the 2 valve edges meet each other in a commissure that forms a continuum with no gaps or overlaps despite the fact that each valve, secreted by 2 mantle lobes, may present antisymmetric ornamental patterns of varying regularity and size. Interlocking is maintained throughout the entirety of development, even when the shell edge exhibits significant irregularity due to injury or other environmental influences, which suggests a dynamic physical process of pattern formation that cannot be genetically specified. Here, we derive a mathematical framework, based on the physics of shell growth, to explain how this interlocking pattern is created and regulated by mechanical instabilities. By close consideration of the geometry and mechanics of 2 lobes of the mantle, constrained both by the rigid shell that they secrete and by each other, we uncover the mechanistic basis for the interlocking pattern. Our modeling framework recovers and explains a large diversity of shell forms and highlights how parametric variations in the growth process result in morphological variation. Beyond the basic interlocking mechanism, we also consider the intricate and striking multiscale-patterned edge in certain brachiopods. We show that this pattern can be explained as a secondary instability that matches morphological trends and data.

SUBMITTER: Moulton DE

PROVIDER: S-EPMC6955362 | biostudies-literature | 2020 Jan

REPOSITORIES: biostudies-literature

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Mechanics unlocks the morphogenetic puzzle of interlocking bivalved shells.

Moulton Derek E DE Goriely Alain A Chirat Régis R

Proceedings of the National Academy of Sciences of the United States of America 20191216 1

Brachiopods and mollusks are 2 shell-bearing phyla that diverged from a common shell-less ancestor more than 540 million years ago. Brachiopods and bivalve mollusks have also convergently evolved a bivalved shell that displays an apparently mundane, yet striking feature from a developmental point of view: When the shell is closed, the 2 valve edges meet each other in a commissure that forms a continuum with no gaps or overlaps despite the fact that each valve, secreted by 2 mantle lobes, may pre ...[more]

PMID: 31843921

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Project description: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.

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Mechanics unlocks the morphogenetic puzzle of interlocking bivalved shells.

Publications

Mechanics unlocks the morphogenetic puzzle of interlocking bivalved shells.

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