Evolution of the strikingly diverse submandibular muscles in Anura

Abstract

The most ventral muscles of the head (the mm. submentalis, intermandibularis, and interhyoideus) provide support to the gular region and lift the buccal floor during ventilation and feeding. These muscles show limited variation in most gnathostomes, but in Anura they exhibit a surprising diversity. The few studies that have explored this character system highlighted its potential as a source of phylogenetic information. In this paper we explored the diversity of this character system studying specimens of 567 anuran species and reviewing published data to cover a total of 1321 species, belonging to 53 of the 54 currently recognized anuran families, as well as caudates and caecilians. We defined 27 discrete characters including the number of muscle bellies, supplementary layers, hypertrophy and diversity of elastic fibres, and pigmentation, among others, and optimized them on a comprehensive phylogenetic hypothesis. We recognized 223 unambiguously optimized synapomorphies for numerous clades on different scales, including three for Anura and many for suprafamiliar clades with poor phenotypic support. Finally, we discussed the evolution of this highly diverse character system, including homology, development, and its functional role in vocalization and feeding. Interestingly, the striking levels of variation in some structures contrast with the amount of phylogenetic inertia, allowing us to recognize several general patterns. Supplementary elements of the m. intermandibularis evolved first as broad layers occuring in more than half of extant anuran species and then concentrated forming discreet bellies in several clades. The anterior portion of the gular region is not sexually dimorphic, and is likely related to ventilation and tongue protraction. Conversely, the diversity of the m. interhyoideus is strongly linked to vocal sacs, which are present only in adult males, suggesting the presence of two independent modules.

Vocal Repertoire of Two Bokermannohyla (Anura: Hylidae) Species, with an Overview of Advertisement Call Diversity in the Genus

“…Rather, males of B. caramaschii lack a vocal sac, and one of their submandibular muscles (m. interhyoideus) is not as expanded as in other Bokermannohyla species in which this muscle forms an expanded pouch (Fig. 4A, B; Elias-Costa et al, 2021). One of the functions of the vocal sac is to radiate sound via coupling of the sound energy produced by the frog and the surrounding air (Bradbury and Vehrencamp, 1998;Pauly et al, 2006;Starnberger et al, 2014).…”

Treefrog Diversity in the Neotropics: Phylogenetic Relationships of Scinaxini (Anura: Hylidae: Hylinae)

“…The terminology employed follows Duellman (1970a) for adult external morphology, Trueb (1973, 1993) for cranial and postcranial osteology, Fabrezi (1992, 1993) for carpal and tarsal osteology, Trewavas (1933) for laryngeal morphology, Jurgens (1971) for nasal cartilage morphology, Blotto et al (2020) for hand and foot myology, Tyler (1971), Trewavas (1933), Horton (1982), and Elias-Costa et al (2021) for submandibular myology, Diogo et al (2008) for neck and head myology, Engelkes et al (2021) for shoulder joint myology, Gaupp (1896) and Duellman and Trueb (1986) for abdominal myology, Luna et al (2018) for nuptial pad morphology, Altig and McDiarmid (1999) for larval external morphology, and Wassersug (1976) for larval internal oral morphology. Throughout the text, hand digits were numbered II–V following Fabrezi and Alberch (1996); following Altig and McDiarmid (1999) the labial tooth rows are considered A (anterior) and P (posterior).…”

“…Elias-Costa et al (2021) described the diversity of the subgular morphology of the m. interhyoideus as five states in their ch. 19.…”

“…76). Indeed, in species with a posterolaterally expanded m. interhyoideus, this expansion is independent of its development in the subgular region, and results from an increase in muscle mass on the post-tympanic region behind the angle of the jaws (Elias-Costa et al, 2021) or from a large lateral expansion of the muscle that forms a posterodorsally oriented lobe (see Elias-Costa et al, 2021: ch. 18, fig.…”

First description of buccopharyngeal anatomy in Pelodryadinae larvae: Morphological comparison and systematic implications (Anura: Hylidae: Pelodryadinae: Litoria rubella and Ranoidea caerulea)

“…This clade has been consistently considered sister to the Neotropical subfamily Phyllomedusinae (e.g., Faivovich et al, 2005Faivovich et al, , 2010Frost et al, 2006;Jetz & Pyron, 2018), but taxonomy and internal relationships are far from being stable (Faivovich et al, 2005(Faivovich et al, , 2010. Although the sister relationship of Pelodryadinae and Phyllomedusinae appears to be well supported by molecular and phenotypic evidence (e.g., Elias-Costa et al, 2021;Faivovich et al, 2010), the poor taxon sampling and the lack of data of pelodryadins precludes the optimization and the understanding of the evolution of many phenotypic characters.…”