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Development of the ultrastructure of sonic muscles: a kind of neoteny?

Millot S, Parmentier E - BMC Evol. Biol. (2014)

Bottom Line: Interestingly, some characters of sonic muscles can also be found in the trunk muscles of newly hatched larvae that are able to maintain tail beat frequencies up to 100 Hz.Call, pulse and period durations increased significantly with the fish size, but the call dominant frequencies decreased, and the number of pulses and the call amplitude formed a bell curve.This hypothesis has the advantage that it could easily explain why high-speed sonic muscles have evolved so many times in different lineages.

View Article: PubMed Central - HTML - PubMed

Affiliation: Laboratoire de Morphologie Fonctionnelle et Evolutive, Institut de Chimie, B6C, 4000 Liège, Belgium. E.Parmentier@ulg.ac.be.

ABSTRACT

Background: Drumming muscles of some sound-producing fish are 'champions' of contraction speed, their rate setting the fundamental frequency. In the piranha, contraction of these muscles at 150 Hz drives a sound at the same frequency. Drumming muscles of different not closely related species show evolutionary convergences. Interestingly, some characters of sonic muscles can also be found in the trunk muscles of newly hatched larvae that are able to maintain tail beat frequencies up to 100 Hz. The aim of this work was to study the development of sound production and sonic and epaxial muscles simultaneously in the red bellied piranhas (Pygocentrus nattereri) to seek for possible common characteristics.

Results: Call, pulse and period durations increased significantly with the fish size, but the call dominant frequencies decreased, and the number of pulses and the call amplitude formed a bell curve. In epaxial muscles, the fibre diameters of younger fish are first positioned in the graphical slope corresponding to sonic muscles, before diverging. The fibre diameter of older fish trunk muscles was bigger, and the area of the myofibrils was larger than in sonic muscles. Moreover, in two of the biggest fish, the sonic muscles were invaded by fat cells and the sonic muscle ultrastructure was similar to the epaxial one. These two fish were also unable to produce any sound, meaning they lost their ability to contract quickly.

Conclusions: The volume occupied by myofibrils determines the force of contraction, the volume of sarcoplasmic reticulum sets the contraction frequency, and the volume of mitochondria sets the level of sustained performance. The functional outcomes in muscles are all attributable to shifts in the proportions of those structures. A single delay in the development restricts the quantity of myofibrils, maintains a high proportion of space in the sarcoplasm and develops sarcoplasmic reticulum. High-speed sonic muscles could thus be skeletal muscles with delayed development. This hypothesis has the advantage that it could easily explain why high-speed sonic muscles have evolved so many times in different lineages.

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Fiber diameter (Mean ± SD) of sonic and epaxial muscles in Pygocentrus nattereri of different standard length. The black line represents the linear regression for sonic muscle and the dotted line represents the linear regression for the epaxial muscle. Note that epaxial muscle diameter of younger fish (3 and 25 mm) are on the same slope as sonic muscles.
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Figure 4: Fiber diameter (Mean ± SD) of sonic and epaxial muscles in Pygocentrus nattereri of different standard length. The black line represents the linear regression for sonic muscle and the dotted line represents the linear regression for the epaxial muscle. Note that epaxial muscle diameter of younger fish (3 and 25 mm) are on the same slope as sonic muscles.

Mentions: In fish size classes, when the comparison was possible (all except size classes 1 and 2), the fiber diameter of epaxial muscle was always higher than the fiber diameter of sonic muscle (F2,22 = 27.62, p < 0.001; Figure 4). In fish from size class 3 to 5, the fiber diameter of sonic and epaxial muscle significantly increased with the fish standard length (F2,11 = 58.09, p < 0.001; F3,12 = 146.73, p < 0.001 respectively; Figure 4). The positioning of data from the trunk muscle of younger fish (size classes 1 and 2) was interesting because they were positioned on the slope of the sonic muscles and not of the epaxial muscles. There seemed to be an acceleration in the growth of the epaxial muscles, but the sonic muscles, which are derived from hypaxial muscles, were still developing at the same rate.


Development of the ultrastructure of sonic muscles: a kind of neoteny?

Millot S, Parmentier E - BMC Evol. Biol. (2014)

Fiber diameter (Mean ± SD) of sonic and epaxial muscles in Pygocentrus nattereri of different standard length. The black line represents the linear regression for sonic muscle and the dotted line represents the linear regression for the epaxial muscle. Note that epaxial muscle diameter of younger fish (3 and 25 mm) are on the same slope as sonic muscles.
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC3924398&req=5

Figure 4: Fiber diameter (Mean ± SD) of sonic and epaxial muscles in Pygocentrus nattereri of different standard length. The black line represents the linear regression for sonic muscle and the dotted line represents the linear regression for the epaxial muscle. Note that epaxial muscle diameter of younger fish (3 and 25 mm) are on the same slope as sonic muscles.
Mentions: In fish size classes, when the comparison was possible (all except size classes 1 and 2), the fiber diameter of epaxial muscle was always higher than the fiber diameter of sonic muscle (F2,22 = 27.62, p < 0.001; Figure 4). In fish from size class 3 to 5, the fiber diameter of sonic and epaxial muscle significantly increased with the fish standard length (F2,11 = 58.09, p < 0.001; F3,12 = 146.73, p < 0.001 respectively; Figure 4). The positioning of data from the trunk muscle of younger fish (size classes 1 and 2) was interesting because they were positioned on the slope of the sonic muscles and not of the epaxial muscles. There seemed to be an acceleration in the growth of the epaxial muscles, but the sonic muscles, which are derived from hypaxial muscles, were still developing at the same rate.

Bottom Line: Interestingly, some characters of sonic muscles can also be found in the trunk muscles of newly hatched larvae that are able to maintain tail beat frequencies up to 100 Hz.Call, pulse and period durations increased significantly with the fish size, but the call dominant frequencies decreased, and the number of pulses and the call amplitude formed a bell curve.This hypothesis has the advantage that it could easily explain why high-speed sonic muscles have evolved so many times in different lineages.

View Article: PubMed Central - HTML - PubMed

Affiliation: Laboratoire de Morphologie Fonctionnelle et Evolutive, Institut de Chimie, B6C, 4000 Liège, Belgium. E.Parmentier@ulg.ac.be.

ABSTRACT

Background: Drumming muscles of some sound-producing fish are 'champions' of contraction speed, their rate setting the fundamental frequency. In the piranha, contraction of these muscles at 150 Hz drives a sound at the same frequency. Drumming muscles of different not closely related species show evolutionary convergences. Interestingly, some characters of sonic muscles can also be found in the trunk muscles of newly hatched larvae that are able to maintain tail beat frequencies up to 100 Hz. The aim of this work was to study the development of sound production and sonic and epaxial muscles simultaneously in the red bellied piranhas (Pygocentrus nattereri) to seek for possible common characteristics.

Results: Call, pulse and period durations increased significantly with the fish size, but the call dominant frequencies decreased, and the number of pulses and the call amplitude formed a bell curve. In epaxial muscles, the fibre diameters of younger fish are first positioned in the graphical slope corresponding to sonic muscles, before diverging. The fibre diameter of older fish trunk muscles was bigger, and the area of the myofibrils was larger than in sonic muscles. Moreover, in two of the biggest fish, the sonic muscles were invaded by fat cells and the sonic muscle ultrastructure was similar to the epaxial one. These two fish were also unable to produce any sound, meaning they lost their ability to contract quickly.

Conclusions: The volume occupied by myofibrils determines the force of contraction, the volume of sarcoplasmic reticulum sets the contraction frequency, and the volume of mitochondria sets the level of sustained performance. The functional outcomes in muscles are all attributable to shifts in the proportions of those structures. A single delay in the development restricts the quantity of myofibrils, maintains a high proportion of space in the sarcoplasm and develops sarcoplasmic reticulum. High-speed sonic muscles could thus be skeletal muscles with delayed development. This hypothesis has the advantage that it could easily explain why high-speed sonic muscles have evolved so many times in different lineages.

Show MeSH
Related in: MedlinePlus