Temperature and developmental plasticity of muscle phenotype in herring larvae

I A Johnston, N J Cole, V L A Vieira, I R Davidson

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Abstract

Myogenesis, the expression of myofibrillar protein isoforms and the development of muscle innervation were investigated in Clyde herring (Clupea harengus L.) in two successive spawning seasons at temperatures ranging from 5 degrees C to 15 degrees C. Myotube formation occurred in a rostral to caudal progression at similar somite stages at all temperatures. Superficial mononuclear muscle pioneer fibres were present at the horizontal septum. Myofibrillogenesis was retarded with respect to somite stage at low temperatures; for example, by the 50-somite stage, myofibrils were observed in the muscle pioneers of the first 31 somites at 12 degrees C, but only the first 20 somites at 5 degrees C. In the electron microscope, the earliest stages of myofibril assembly were observed in the muscle pioneer cells and in a proportion of the multinucleated myotubes within the same somite. By the end of somitogenesis, the density of myofibrils in the rostral myotomes was much higher at 15 degrees C than at 5 degrees C. Embryonic isoforms of myosin light chain 2 (LC2), troponin I and troponin T were identified in the presumptive white muscle using two-dimensional gel electrophoresis. Expression of the embryonic isoforms was gradually switched off during the larval stages. The size range over which embryonic isoforms were present was inversely related to rearing temperature. For example, the adult pattern of myosin LC2 expression was established at 11 mm total length (TL) at 15 degrees C, but not until 15 mm TL at 5 degrees C. Acetylcholinesterase staining was apparent at the myosepta in 31-somite stage embryos at 15 degrees C, but not until approximately the 40-somite stage at 5 degrees C. The red muscle fibres of larvae were initially innervated only at their myoseptal ends. The temperature at which the red muscle fibres became multiply innervated was inversely related to body size, occurring at 12-14 mm at 12 degrees C, but not until 16-19 mm at 5 degrees C. We conclude that the temperature during early development determines the relative timing and degree of expression of the myogenic programme, resulting in significant phenotypic variation in the swimming muscles of the larval stages. Our results highlight a potential mechanism whereby early thermal experience could influence survival and hence the strength of particular year classes of fish.
Original languageEnglish
Pages (from-to)849-868
Number of pages20
JournalJ EXP BIOL
Volume200
Issue number5
Publication statusPublished - 1997

Keywords

  • SKELETAL-MUSCLE
  • LATERAL MUSCLE
  • CLUPEA-HARENGUS L
  • IDENTIFIED MOTONEURONS
  • MYOSIN LIGHT-CHAINS
  • SWIMMING MUSCLES
  • MYOFIBRILLAR PROTEINS
  • FIBER TYPES
  • TROPONIN-T ISOFORMS
  • SALVELINUS-ALPINUS L
  • Biology

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    Johnston, I. A., Cole, N. J., Vieira, V. L. A., & Davidson, I. R. (1997). Temperature and developmental plasticity of muscle phenotype in herring larvae. J EXP BIOL, 200(5), 849-868.