Fast drum strokes: Novel and convergent features of sonic muscle ultrastructure, innervation, and motor neuron organization in the pyramid butterflyfish (hemitaurichthys polylepis)

Abstract

Sound production that is mediated by intrinsic or extrinsic swim bladder musculature has evolved multiple times in teleost fishes. Sonic muscles must contract rapidly and synchronously to compress the gas-filled bladder with sufficient velocity to produce sound. Muscle modifications that may promote rapid contraction include small fiber diameter, elaborate sarcoplasmic reticulum (SR), triads at the A-I boundary, and cores of sarcoplasm. The diversity of innervation patterns indicate that sonic muscles have independently evolved from different trunk muscle precursors. The analysis of sonic motor pathways in distantly related fishes is required to determine the relationships between sonic muscle evolution and function in acoustic signaling. We examined the ultrastructure of sonic and adjacent hypaxial muscle fibers and the distribution of sonic motor neurons in the coral reef Pyramid Butterflyfish (Chaetodontidae: Hemitaurichthys polylepis) that produces sound by contraction of extrinsic sonic muscles near the anterior swim bladder. Relative to adjacent hypaxial fibers, sonic muscle fibers were sparsely arranged among the endomysium, smaller in cross-section, had longer sarcomeres, a more elaborate SR, wider t-tubules, and more radially arranged myofibrils. Both sonic and non-sonic muscle fibers possessed triads at the Z-line, lacked sarcoplasmic cores, and had mitochondria among the myofibrils and concentrated within the peripheral sarcoplasm. Sonic muscles of this derived eutelost possess features convergent with other distant vocal taxa (other euteleosts and non-euteleosts): small fiber diameter, a well-developed SR, and radial myofibrils. In contrast with some sonic fishes, however, Pyramid Butterflyfish sonic muscles lack sarcoplasmic cores and A-I triads. Retrograde nerve label experiments show that sonic muscle is innervated by central and ventrolateral motor neurons associated with spinal nerves 1-3. This restricted distribution of sonic motor neurons in the spinal cord differs from many euteleosts and likely reflects the embryological origin of sonic muscles from hypaxial trunk precursors rather than occipital somites.

Vocal Behavior and Vocal Central Pattern Generator Organization Diverge among Toadfishes

“…Sound production in fishes does not exhibit a similar dependency on respiration and often involves the vibration of either a gas-filled swim bladder or other skeletal structures such as part of the pectoral girdle [Ladich and Fine, 2006;Bass and Ladich, 2008]. While anatomical investigations have identified a sonic or vocal motor nucleus (VMN) in several groups of distantly related teleost fishes [for reviews, see Bass and Baker, 1991;Onuki and Somiya, 2007;Bass and Ladich, 2008;Boyle et al, 2013;Bass et al, in press], most neurophysiological studies of the vocal motor system have been on toadfishes, a single order (Batrachoidiformes) and family (Batrachoididae) that includes species commonly known as midshipman and toadfish [Greenfield et al, 2008].…”

Sound production mechanism inGobius paganellus(Gobiidae)

“…Two different kinds of observation support the hypothesis the goby sounds result from the contraction of the levator pectoralis. This muscle has many characteristics of fast contracting muscles (Ono and Poss, 1982;Bass and Marchaterre, 1989;Fine et al, 1993;Loesser et al, 1997;Ladich, 2001;Boyle et al, 2013): mitochondria in the core, numerous peripheral mitochondria, ribbon-like disposition of myofibrils and well-developed sarcoplasmic reticulum tubules. Sonic diameter is quite high on average (54μm) in comparison to that of other sonic muscles (Parmentier and Diogo, 2006) but is also highly variable (from 20 to 94μm).…”

“…Despite these differences, sonic systems are quite easy to identify because they have distinct sonic muscles associated with the swimbladder. It is not always the case: sounds in tilapia (Oreochromis niloticus), pennant bannerfish (Heniochus chrysostomus) and pyramid butterflyfish (Hemitaurichthys polylepis) also employ the physoclistous swimbladder, but they do not show any apparent distinct specialized muscle (Longrie et al, 2009;Parmentier et al, 2011b;Boyle et al, 2013).…”

Sound production inOnuxodon fowleri(Carapidae) and its amplification by the host shell

“…In addition, the myofibrils do not reach the sarcolemma: the periphery is mostly filled with high concentrations of mitochondria and extension of the sarcoplasmic reticulum. Such fibers are generally considered to be adapted for fast contractions (Rome and Lindstedt, 1998;Boyle et al, 2013). A pulse of O. fowleri sounds most probably results from a single twitch of the PSM (see below).…”