Cephalic muscle development in the Australian lungfish,Neoceratodus forsteri

Abstract

Lungfishes are the extant sister group of tetrapods. As such, they are important for the study of evolutionary processes involved in the water to land transition of vertebrates. The evolution of a true neck, that is, the complete separation of the pectoral girdle from the cranium, is one of the most intriguing morphological transitions known among vertebrates. Other salient changes involve new adaptations for terrestrial feeding, which involves both the cranium and its associated musculature. Historically, the cranium has been extensively investigated, but the development of the cranial muscles much less so. Here, we present a detailed study of cephalic muscle development in the Australian lungfish, Neoceratodus forsteri, which is considered to be the sister taxon to all other extant lungfishes. Neoceratodus shows several developmental patterns previously described in other taxa; the tendency of muscles to develop from anterior to posterior, from their region of origin toward insertion, and from lateral to ventral/medial (outside-in), at least in the branchial arches. The m.protractor pectoralis appears to develop as an extension of the most posterior m.levatores arcuum branchialium, supporting the hypothesis that the m.cucullaris and its derivatives (protractor pectoralis, levatores arcuum branchialium) are branchial muscles. We present a new hypothesis regarding the homology of the ventral branchial arch muscles (subarcualis recti and obliqui, transversi ventrales) in lungfishes and amphibians. Moreover, the morphology and development of the cephalic muscles confirms that extant lungfishes are neotenic and have been strongly influenced via paedomorphosis during their evolutionary history.

Neural crest and the patterning of vertebrate craniofacial muscles

“…These become subdivided first into three pairings: dorsal and ventral recti, medial and lateral recti, and the two obliques. Pairing of lateral and medial recti has been described also in salamanders (Duellman & Trueb, ), Rana viridis (Edgeworth, ), and the shark Squalus acanthias (Goldschmid, ), but spatially separate origins occur in lungfish (Ziermann, Clement, et al, ) as well as humans (Sevel, ). In most cases these descriptions are based on the appearance of myogenic condensations, and the prior histories of the myoblasts have not been defined.…”

“…Comparable movements of EOM precursors have been described in zebrafish (Lin et al, 2006), which also has a comparatively large optic vesicle. In Xenopus, broad bands of putative EOM precursors are present (Ziermann, Clement, Ericsson, & Olsson, 2017). These become subdivided first into three pairings: dorsal and ventral recti, medial and lateral recti, and the two obliques.…”

Pattern of nitrergic cells and fibers organization in the central nervous system of the Australian lungfish,Neoceratodus forsteri(Sarcopterygii: Dipnoi)

“…The importance of the nitrergic system, formed by the networks of neurons containing NOS, in the control of other "classical" neurotransmitter systems has been established. Thus, the NO-mediated signal can modulate glutamatergic (Garthwaite, 1991;Lawrence & Jarrott, 1993;Neitz, Mergia, Eysel, Koesling, & Mittmann, 2011;Raju et al, 2015;Rudkouskaya et al, 2010) and dopaminergic (Bugnon, Schaad, & Schorderet, 1994;Chaparro-Huerta, Beas-Zarate, Guerrero, & Feria-Velasco, 1997;Kiss, Zsilla, & Vizi, 2004;Zhu & Luo, 1992) neurotransmission, via presynaptic regulation of neurotransmitter release and/or postsynaptic regulation of signal action. In addition, NO also acts on GABAergic synaptic transmission (Gasulla & Calvo, 2015;Maggesissi et al, 2009;Tarasenko, Krupko, & Himmelreich, 2014;Yamamoto, Takei, Koyanagi, Koshikawa, & Kobayashi, 2015;Yang, Chen, Li, & Pan, 2007), by reduction of the strength of inhibition, which allows the fine-tuning of information processing (Yassin et al, 2014).…”

Morphofunctional Categories and Ontogenetic Origin of Temporal Skull Openings in Amniotes

“…This is not the case in most extant non-amniotes, in which larvae hatch and have to feed (Figure 1A). For that, jaw (and branchial) musculature inserts primarily to the embryonic neurocranium (chondrocranium), as dermatocranial bones are not yet well-developed ( Figure 1A ′ , A ′′ ) (Edgeworth, 1935;De Beer, 1937;Ziermann et al, 2018). As such, compared to amniotes, the primordial cartilaginous skull is highly functional.…”

“…As such, compared to amniotes, the primordial cartilaginous skull is highly functional. Dermatocranial and temporal skull bones are later influenced developmentally by the functional jaw musculature near the neurocranium and are incorporated to the feeding apparatus as further attachment sites (Figure 1A ′′ , B ′ ) (Ziermann et al, 2018). Furthermore, in non-tetrapods, opercle bones also contribute to the dermatocranial armor to protect gill arches, to regulate gill ventilation, and to form a natural and broad edge of the temporal region ( Figure 1A ′ : dotted line) (Goodrich, 1930;De Beer, 1937;Kemp, 1999).…”