Abstract
BackgroundEcological 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.MethodsWe 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.ResultsWe 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.
Highlights
The Cretaceous terrestrial revolution and the Cretaceous-Paleogene (K-Pg) mass extinction event are often viewed as milestones in placental mammal evolution (Meredith et al, 2011)
In C. didactylus and T. tetradactyla the volumes estimated from the mass were smaller than those
We argue that the lateral orientation of the coronoid process (Figs. 3B, 3A, 11F –11H) and the M. temporalis superficialis medial line of action in the pygmy anteater (Fig. 11H) are the basis for the temporalis-led medial roll of the dorsal margin of the mandibular body
Summary
The Cretaceous terrestrial revolution and the Cretaceous-Paleogene (K-Pg) mass extinction event are often viewed as milestones in placental mammal evolution (Meredith et al, 2011). Despite the homogeneity of the main complexes of the masticatory apparatus among placental mammals, muscular architecture and proportions vary largely (e.g., Parsons, 1896; Toldt, 1905; Turnbull, 1970). This suggests a wide range of functional disparity associated with both phylogenetic constraints and ecological specialization (Samuels, 2009; Hautier, Lebrun & Cox, 2012; Fabre et al, 2017; Ginot, Claude & Hautier, 2018; Kohli & Rowe, 2019). 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
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