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The structure of sarcomeres imposes limits to the capacity of striated muscle to change length and produce force, with z-disc and myosin filament interactions constraining shortening. Conversely, supercontracting muscles, hitherto only known among vertebrates in the tongue retractor muscle (m. hyoglossus) of chameleons, have perforated z-discs that allow myosin filaments to extend through them into adjacent sarcomeres, permitting continued shortening and force development. Additional hyolingual muscles in chameleons undergo extreme length changes during feeding as well and may benefit from supercontractile properties. We compared length–tension relationship data and transmission electron microscopy images from four chameleon muscles to test for the presence of additional supercontracting muscle. We document the second known example of a supercontracting muscle among vertebrates (the m. sternohyoideus superficialis) and show that the m. sternohyoideus profundus exhibits functional convergence with supercontracting muscles by increasing the range of muscle lengths over which it can exert force through the exploitation of sarcomere length non-uniformity across its muscle fibres. Additionally, we show that chameleon supercontracting muscles may share common contractile and structural properties due to a common origin from occipital somites. These results provide important insights into the developmental and evolutionary patterns associated with supercontracting muscle and extreme muscle elongation.
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One size does not fit all: diversity of length–force properties of obliquely striated muscles
ABSTRACT Obliquely striated muscles occur in 17+ phyla, likely evolving repeatedly, yet the implications of oblique striation for muscle function are unknown. Contrary to the belief that oblique striation allows high force output over extraordinary length ranges (i.e. superelongation), recent work suggests diversity in operating length ranges and length–force relationships. We hypothesize oblique striation evolved to increase length–force relationship flexibility. We predict that superelongation is not a general characteristic of obliquely striated muscles and instead that length–force relationships vary with operating length range. To test these predictions, we measured length–force relationships of five obliquely striated muscles from inshore longfin squid, Doryteuthis pealeii: tentacle, funnel retractor and head retractor longitudinal fibers, and arm and fin transverse fibers. Consistent with superelongation, the tentacle length–force relationship had a long descending limb, whereas all others exhibited limited descending limbs. The ascending limb at 0.6P0 was significantly broader (P<0.001) for the tentacle length–force relationship (0.43±0.04L0; where L0 is the preparation length that produced peak isometric stress, P0) than for the arm (0.29±0.03L0), head retractor (0.24±0.06L0), fin (0.20±0.04L0) and funnel retractor (0.27±0.03L0). The fin's narrow ascending limb differed significantly from those of the arm (P=0.004) and funnel retractor (P=0.012). We further characterized the tentacle preparation's maximum isometric stress (315±78 kPa), maximum unloaded shortening velocity (2.97±0.55L0 s−1) and ultrastructural traits (compared with the arm), which may explain its broader length–force relationship. Comparison of obliquely striated muscles across taxa revealed length–force relationship diversity, with only two species exhibiting superelongation.
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- PAR ID:
- 10431466
- Publisher / Repository:
- The Company of Biologists Ltd
- Date Published:
- Journal Name:
- Journal of Experimental Biology
- Volume:
- 226
- Issue:
- Suppl_1
- ISSN:
- 0022-0949
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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