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.

Flexible conservatism in the skull modularity of convergently evolved myrmecophagous placental mammals

“…We show that the absence of a module including a complete zygomatic arch is a frequent pattern among myrmecophagous placentals (Table 3). Such absence is concordant with the evolution of adduction-less mandibular motion in anteaters and probably pangolins too [95], which contrasts with some previous studies on mammalian modularity [31,80]. Although masticatory function appears to explain part of the variation of the zygomatic region, it is hardly the sole explanatory variable justifying the presence/absence of a zygomatic-pterygoid module with a complete zygomatic arch.…”

“…Therefore, the association of the maxillo-palatal region landmarks with those of the naso-frontal region could be the result of facial prominences outgrowth and fusion [3]. In addition, the loss of mastication in myrmecophagous placentals [60,95] likely reduces the mechanical stress applied to the molar region during adduction. Such reduced strain might have also reduced covariances generated by bone remodelling as a response to masticatory stress [96].…”

“…Another major feature of the convergent skulls of anteaters and pangolins is the absence of an ossified zygomatic arch (e.g., [95,97]). Mandibular adductor muscles, like the masseter [98], apply significant mechanical strain, increasing the rate of periosteal deposition [99,100] and generating mastication-induced osteogenesis [3].…”

Transcriptomic data reveal divergent paths of chitinase evolution underlying dietary convergence in anteaters and pangolins

“…This highly-specialized diet has indeed independently evolved in five placental orders: armadillos (Cingulata), anteaters (Pilosa), aardvarks (Tubulidentata), pangolins (Pholidota), and aardwolves (Carnivora). As a consequence of foraging for small-sized prey (Redford 1987), similar morphological adaptations have evolved in these mammalian species such as powerful claws used to dig into ant and termite nests, tooth reduction culminating in complete tooth loss in anteaters and pangolins (Ferreira-Cardoso et al 2019), an elongated muzzle with an extensible tongue (Ferreira-Cardoso et al 2020), and viscous saliva produced by hypertrophied salivary glands (Reiss 2001). Due to strong energetic constraints imposed by a nutritionally poor diet, myrmecophagous mammals also share relatively low metabolic rates and might thus require specific adaptations to extract nutrients from the chitinous exoskeletons of their prey (McNab 1984).…”

Hind foot drumming: Volumetric micro‐computed tomography investigation of the hind limb musculature of three African mole‐rat species (Bathyergidae)

“…Additionally, diceCT scanning has been used to digitally dissect the masticatory and facial muscles of several primate species including the blue‐eyed black lemur ( Eulemur flavifrons ; Dickinson et al, 2020a), the common marmoset ( Callithrix jacchus ; Dickinson et al, 2019) and the Aye‐Aye ( Daubentonia madagascariensis ; Dickinson et al, 2020b). Several studies have comparatively studied the masticatory musculature of African mole‐rats (Bathyergidae; Cox & Faulkes, 2014; Cox et al, 2020), bats (Santana, 2018) and anteaters (Ferreira‐Cardoso et al, 2020), however no statistical analysis comparing the species was performed in these studies as they compared only one individual per species. Locomotory studies on the limbs of crocodilians (Klinkhamer et al, 2017; Wiseman et al, 2021), frogs (Collings & Richards, 2019) and birds (Bishop et al, 2021; Sullivan et al, 2019) have also employed diceCT scanning.…”