Anatomy, function, and evolution of jaw and hyobranchial muscles in cryptobranchoid salamander larvae

Abstract

Larval salamanders (Lissamphibia: Caudata) are known to be effective suction feeders in their aquatic environments, although they will eventually transform into terrestrial tongue feeding adults during metamorphosis. Early tetrapods may have had a similar biphasic life cycle and this makes larval salamanders a particularly interesting model to study the anatomy, function, development, and evolution of the feeding apparatus in terrestrial vertebrates. Here, we provide a description of the muscles that are involved in the feeding strike in salamander larvae of the Hynobiidae and compare them to larvae of the paedomorphic Cryptobranchidae. We provide a functional and evolutionary interpretation for the observed muscle characters. The cranial muscles in larvae from species of the Hynobiidae and Cryptobranchidae are generally very similar. Most notable are the differences in the presence of the m. hyomandibularis, a muscle that connects the hyobranchial apparatus with the lower jaw. We found this muscle only in Onychodactylus japonicus (Hynobiidae) but not in other hynobiid or cryptobranchid salamanders. Interestingly, the m. hyomandibularis in O. japonicus originates from the ceratobranchial I and not the ceratohyal, and thus exhibits what was previously assumed to be the derived condition. Finally, we applied a biomechanical model to simulate suction feeding in larval salamanders. We provide evidence that a flattened shape of the hyobranchial apparatus in its resting position is beneficial for a fast and successful suction feeding strike.

A New Basal Salamandroid (Amphibia, Urodela) from the Late Jurassic of Qinglong, Hebei Province, China

“…It has been documented that basibranchial II provides the attachment for three muscles: M. geniohyoideus, M. rectus cervicis, and M. subarcualis oblique [ 118 – 121 ]. In those salamanders lacking basibranchial II (e.g., Onychodactylus japonicus and cryptobranchids), M. geniohyoideus is continuous with M. rectus cervicis, whereas M. subarcualis oblique inserts on the adjacent fascia of M. rectus cervicis [ 118 , 119 , 121 ]. In Qinglongtriton , the complex structure of basibranchial II may have strengthened the attachment of these muscles, thus enhancing the ability to control the hyobranchial apparatus during feeding and respiration.…”

Musculoskeletal architecture of the prey capture apparatus in salamandrid newts with multiphasic lifestyle: does anatomy change during the seasonal habitat switches?

“…In salamander larvae, the M. geniohyoideus runs from the lower jaw posteriorly and attaches on the urohyal: the posterior‐most hyobranchial skeletal element that is attached to the rest of the hyobranchial system (Drüner, ; Reilly, ; Reilly & Lauder, ; Deban & Wake, ; Kleinteich et al. ). During metamorphosis in salamandrids, the urohyal loses its connection with the hyobranchial system or is completely lost in some salamandrids (Francis, ) along with the origin of the M. geniohyoideus.…”

“…However, in metamorphosed newts, though the M. geniohyoideus insertion on the lower jaw remains in place, its origin and accordingly its course differ substantially from other tetrapods. In salamander larvae, the M. geniohyoideus runs from the lower jaw posteriorly and attaches on the urohyal: the posterior-most hyobranchial skeletal element that is attached to the rest of the hyobranchial system (Dr€ uner, 1902;Reilly, 1987;Reilly & Lauder, 1990;Kleinteich et al 2014). During metamorphosis in salamandrids, the urohyal loses its connection with the hyobranchial system or is completely lost in some salamandrids (Francis, 1934) along with the origin of the M. geniohyoideus.…”

Ontogenetic plasticity in cranial morphology is associated with a change in the food processing behavior in Alpine newts

“…The 3D muscle morphology is considered but the main function of each muscle is assessed from a lateral perspective (i.e., simplified to a 2D movement). More complex inter-hyobranchial movements are likely to occur due to the 3D orientation of the hyobranchial apparatus and its muscles (see for example [53]). The hyobranchial system of all morphotypes forms the attachment site for several major muscles (i.e., six in the LLM and MMM, and five in the PMM).…”