Three-dimensional structure of the basketweave Z-band in midshipman fish sonic muscle

Striated muscle enables movement in all animals by the contraction of myriads of sarcomeres joined end to end by the Z-bands. The contraction is due to tension generated in each sarcomere between overlapping arrays of actin and myosin filaments. At the Z-band, actin filaments from adjoining sarcomeres overlap and are cross-linked in a regular pattern mainly by the protein α-actinin. The Z-band is dynamic, reflected by the 2 regular patterns seen in transverse section electron micrographs; the so-called small-square and basketweave forms. Although these forms are attributed, respectively, to relaxed and actively contracting muscles, the basketweave form occurs in certain relaxed muscles as in the muscle studied here. We used electron tomography and subtomogram averaging to derive the 3D structure of the Z-band in the swimbladder sonic muscle of type I male plainfin midshipman fish (Porichthys notatus), into which we docked the crystallographic structures of actin and α-actinin. The α-actinin links run diagonally between connected pairs of antiparallel actin filaments and are oriented at an angle of about 25° away from the actin filament axes. The slightly curved and flattened structure of the α-actinin rod has a distinct fit into the map. The Z-band model provides a detailed understanding of the role of α-actinin in transmitting tension between actin filaments in adjoining sarcomeres.

Sound production to electric discharge: sonic muscle evolution in progress in Synodontis spp. catfishes (Mochokidae)

Elucidating the origins of complex biological structures has been one of the major challenges of evolutionary studies. Within vertebrates, the capacity to produce regular coordinated electric organ discharges (EODs) has evolved independently in different fish lineages. Intermediate stages, however, are not known. We show that, within a single catfish genus, some species are able to produce sounds, electric discharges or both signals (though not simultaneously). We highlight that both acoustic and electric communication result from actions of the same muscle. In parallel to their abilities, the studied species show different degrees of myofibril development in the sonic and electric muscle. The lowest myofibril density was observed in Synodontis nigriventris , which produced EODs but no swim bladder sounds, whereas the greatest myofibril density was observed in Synodontis grandiops , the species that produced the longest sound trains but did not emit EODs. Additionally, S. grandiops exhibited the lowest auditory thresholds. Swim bladder sounds were similar among species, while EODs were distinctive at the species level. We hypothesize that communication with conspecifics favoured the development of species-specific EOD signals and suggest an evolutionary explanation for the transition from a fast sonic muscle to electrocytes.

Variability in the sonic muscles of the Lusitanian toadfish (Halobatrachus didactylus): acoustic signals may reflect individual quality

Animal vocalizations are good examples of signals that have been shaped by sexual selection and often contribute to resolve contests or the choice of mates. We relate the mass of the sound-producing muscles of a highly vocal fish species, the Lusitanian toadfish ( Halobatrachus didactylus (Bloch and Schneider, 1801)), with the sender’s physical features, such as body size, and reproductive and body condition. In this species, both sexes are known to emit sounds during agonistic interactions and males rely on their mate attraction vocalizations to reproduce. Sonic muscles were highly variable among males (CV = 40%) and females (CV = 33%) and showed sexual dimorphism. Regression analysis showed that variability in the sonic muscles was best explained by total length and fish condition in males and females. Liver mass in both genders, and the mass of the testes accessory glands, also explained sonic muscle variability. These variables explained 96% and 91% of the sonic muscle mass variability in males and females, respectively. As in teleost fishes sonic muscle mass correlates to particular sound acoustic features, we propose that in the Lusitanian toadfish sounds can inform the receiver about the sender’s quality, such as body size and condition, which are critical information in contests and mate choice.