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Comparative masticatory myology in anteaters and its implications for interpreting morphological convergence in myrmecophagous placentals.

ABSTRACT: Background:Ecological adaptations of mammals are reflected in the morphological diversity of their feeding apparatus, which includes differences in tooth crown morphologies, variation in snout size, or changes in muscles of the feeding apparatus. The adaptability of their feeding apparatus allowed them to optimize resource exploitation in a wide range of habitats. The combination of computer-assisted X-ray microtomography (µ-CT) with contrast-enhancing staining protocols has bolstered the reconstruction of three-dimensional (3D) models of muscles. This new approach allows for accurate descriptions of muscular anatomy, as well as the quick measurement of muscle volumes and fiber orientation. Ant- and termite-eating (myrmecophagy) represents a case of extreme feeding specialization, which is usually accompanied by tooth reduction or complete tooth loss, snout elongation, acquisition of a long vermiform tongue, and loss of the zygomatic arch. Many of these traits evolved independently in distantly-related mammalian lineages. Previous reports on South American anteaters (Vermilingua) have shown major changes in the masticatory, intermandibular, and lingual muscular apparatus. These changes have been related to a functional shift in the role of upper and lower jaws in the evolutionary context of their complete loss of teeth and masticatory ability. Methods:We used an iodine staining solution (I2KI) to perform contrast-enhanced µ-CT scanning on heads of the pygmy (Cyclopes didactylus), collared (Tamandua tetradactyla) and giant (Myrmecophaga tridactyla) anteaters. We reconstructed the musculature of the feeding apparatus of the three extant anteater genera using 3D reconstructions complemented with classical dissections of the specimens. We performed a description of the musculature of the feeding apparatus in the two morphologically divergent vermilinguan families (Myrmecophagidae and Cyclopedidae) and compared it to the association of morphological features found in other myrmecophagous placentals. Results:We found that pygmy anteaters (Cyclopes) present a relatively larger and architecturally complex temporal musculature than that of collared (Tamandua) and giant (Myrmecophaga) anteaters, but shows a reduced masseter musculature, including the loss of the deep masseter. The loss of this muscle concurs with the loss of the jugal bone in Cyclopedidae. We show that anteaters, pangolins, and aardvarks present distinct anatomies despite morphological and ecological convergences.

SUBMITTER: Ferreira-Cardoso S

PROVIDER: S-EPMC7491420 | biostudies-literature | 2020

REPOSITORIES: biostudies-literature

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Comparative masticatory myology in anteaters and its implications for interpreting morphological convergence in myrmecophagous placentals.

Ferreira-Cardoso Sérgio S Fabre Pierre-Henri PH de Thoisy Benoit B Delsuc Frédéric F Hautier Lionel L

PeerJ 20200903

<h4>Background</h4>Ecological adaptations of mammals are reflected in the morphological diversity of their feeding apparatus, which includes differences in tooth crown morphologies, variation in snout size, or changes in muscles of the feeding apparatus. The adaptability of their feeding apparatus allowed them to optimize resource exploitation in a wide range of habitats. The combination of computer-assisted X-ray microtomography (µ-CT) with contrast-enhancing staining protocols has bolstered th ...[more]

PMID: 32983632

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Project description:Background and aimsPatterns of morphological evolution at levels above family rank remain underexplored in the ferns. The present study seeks to address this gap through analysis of 79 morphological characters for 81 taxa, including representatives of all ten families of eupolypod II ferns. Recent molecular phylogenetic studies demonstrate that the evolution of the large eupolypod II clade (which includes nearly one-third of extant fern species) features unexpected patterns. The traditional 'athyrioid' ferns are scattered across the phylogeny despite their apparent morphological cohesiveness, and mixed among these seemingly conservative taxa are morphologically dissimilar groups that lack any obvious features uniting them with their relatives. Maximum-likelihood and maximum-parsimony character optimizations are used to determine characters that unite the seemingly disparate groups, and to test whether the polyphyly of the traditional athyrioid ferns is due to evolutionary stasis (symplesiomorphy) or convergent evolution. The major events in eupolypod II character evolution are reviewed, and character and character state concepts are reappraised, as a basis for further inquiries into fern morphology.MethodsCharacters were scored from the literature, live plants and herbarium specimens, and optimized using maximum-parsimony and maximum-likelihood, onto a highly supported topology derived from maximum-likelihood and Bayesian analysis of molecular data. Phylogenetic signal of characters were tested for using randomization methods and fitdiscrete.Key resultsThe majority of character state changes within the eupolypod II phylogeny occur at the family level or above. Relative branch lengths for the morphological data resemble those from molecular data and fit an ancient rapid radiation model (long branches subtended by very short backbone internodes), with few characters uniting the morphologically disparate clades. The traditional athyrioid ferns were circumscribed based upon a combination of symplesiomorphic and homoplastic characters. Petiole vasculature consisting of two bundles is ancestral for eupolypods II and a synapomorphy for eupolypods II under deltran optimization. Sori restricted to one side of the vein defines the recently recognized clade comprising Rhachidosoraceae through Aspleniaceae, and sori present on both sides of the vein is a synapomorphy for the Athyriaceae sensu stricto. The results indicate that a chromosome base number of x =41 is synapomorphic for all eupolypods, a clade that includes over two-thirds of extant fern species.ConclusionsThe integrated approach synthesizes morphological studies with current phylogenetic hypotheses and provides explicit statements of character evolution in the eupolypod II fern families. Strong character support is found for previously recognized clades, whereas few characters support previously unrecognized clades. Sorus position appears to be less complicated than previously hypothesized, and linear sori restricted to one side of the vein support the clade comprising Aspleniaceae, Diplaziopsidaceae, Hemidictyaceae and Rachidosoraceae - a lineage only recently identified. Despite x =41 being a frequent number among extant species, to our knowledge it has not previously been demonstrated as the ancestral state. This is the first synapomorphy proposed for the eupolypod clade, a lineage comprising 67 % of extant fern species. This study provides some of the first hypotheses of character evolution at the family level and above in light of recent phylogenetic results, and promotes further study in an area that remains open for original observation.

Dataset Information

Comparative masticatory myology in anteaters and its implications for interpreting morphological convergence in myrmecophagous placentals.

Publications

Comparative masticatory myology in anteaters and its implications for interpreting morphological convergence in myrmecophagous placentals.

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