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Increasing morphological disparity and decreasing optimality for jaw speed and strength during the radiation of jawed vertebrates.

ABSTRACT: The Siluro-Devonian adaptive radiation of jawed vertebrates, which underpins almost all living vertebrate biodiversity, is characterized by the evolutionary innovation of the lower jaw. Multiple lines of evidence have suggested that the jaw evolved from a rostral gill arch, but when the jaw took on a feeding function remains unclear. We quantified the variety of form in the earliest jaws in the fossil record from which we generated a theoretical morphospace that we then tested for functional optimality. By drawing comparisons with the real jaw data and reconstructed jaw morphologies from phylogenetically inferred ancestors, our results show that the earliest jaw shapes were optimized for fast closure and stress resistance, inferring a predatory feeding function. Jaw shapes became less optimal for these functions during the later radiation of jawed vertebrates. Thus, the evolution of jaw morphology has continually explored previously unoccupied morphospace and accumulated disparity through time, laying the foundation for diverse feeding strategies and the success of jawed vertebrates.

SUBMITTER: Deakin WJ

PROVIDER: S-EPMC8932669 | biostudies-literature | 2022 Mar

REPOSITORIES: biostudies-literature

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Increasing morphological disparity and decreasing optimality for jaw speed and strength during the radiation of jawed vertebrates.

Deakin William J WJ Anderson Philip S L PSL den Boer Wendy W Smith Thomas J TJ Smith Thomas J TJ Hill Jennifer J JJ Rücklin Martin M Donoghue Philip C J PCJ Rayfield Emily J EJ

Science advances 20220318 11

The Siluro-Devonian adaptive radiation of jawed vertebrates, which underpins almost all living vertebrate biodiversity, is characterized by the evolutionary innovation of the lower jaw. Multiple lines of evidence have suggested that the jaw evolved from a rostral gill arch, but when the jaw took on a feeding function remains unclear. We quantified the variety of form in the earliest jaws in the fossil record from which we generated a theoretical morphospace that we then tested for functional opt ...[more]

PMID: 35302857

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Project description:BackgroundThe Dlx gene family encodes transcription factors involved in the development of a wide variety of morphological innovations that first evolved at the origins of vertebrates or of the jawed vertebrates. This gene family expanded with the two rounds of genome duplications that occurred before jawed vertebrates diversified. It includes at least three bigene pairs sharing conserved regulatory sequences in tetrapods and teleost fish, but has been only partially characterized in chondrichthyans, the third major group of jawed vertebrates. Here we take advantage of developmental and molecular tools applied to the shark Scyliorhinus canicula to fill in the gap and provide an overview of the evolution of the Dlx family in the jawed vertebrates. These results are analyzed in the theoretical framework of the DDC (Duplication-Degeneration-Complementation) model.ResultsThe genomic organisation of the catshark Dlx genes is similar to that previously described for tetrapods. Conserved non-coding elements identified in bony fish were also identified in catshark Dlx clusters and showed regulatory activity in transgenic zebrafish. Gene expression patterns in the catshark showed that there are some expression sites with high conservation of the expressed paralog(s) and other expression sites with events of paralog sub-functionalization during jawed vertebrate diversification, resulting in a wide variety of evolutionary scenarios within this gene family.ConclusionDlx gene expression patterns in the catshark show that there has been little neo-functionalization in Dlx genes over gnathostome evolution. In most cases, one tandem duplication and two rounds of vertebrate genome duplication have led to at least six Dlx coding sequences with redundant expression patterns followed by some instances of paralog sub-functionalization. Regulatory constraints such as shared enhancers, and functional constraints including gene pleiotropy, may have contributed to the evolutionary inertia leading to high redundancy between gene expression patterns.

Dataset Information

Increasing morphological disparity and decreasing optimality for jaw speed and strength during the radiation of jawed vertebrates.

Publications

Increasing morphological disparity and decreasing optimality for jaw speed and strength during the radiation of jawed vertebrates.

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