Rapid evolution of muscle fibre number in post-glacial populations of Arctic charr Salvelinus alpinus

Ian Alistair Johnston, M Abercromby, VLA Vieira, RJ Sigursteindóttir, BK Kristjánsson, D Sibthorpe, S Skúlason

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67 Citations (Scopus)

Abstract

Thingvallavatn, the largest and one of the oldest lakes in Iceland, contains four morphs of Arctic charr Salvelinus alpinus. Dwarf benthic (DB), large benthic (LB), planktivorous (PL) and piscivorous (PI) morphs can be distinguished and differ markedly in head morphology, colouration and maximum fork length (FLmax,), reflecting their different resource specialisations within the lake. The four morphs in Thingvallavatn are thought to have been isolated for approximately 10 000 years, since shortly after the end of the last Ice Age.

We tested the null hypothesis that the pattern of muscle fibre recruitment was the same in all morphs, reflecting their recent diversification. The cross-sectional areas of fast and slow muscle fibres were measured at 0.7 FL in 46 DB morphs, 23 LB morphs, 24 PL morphs and 22 PI morphs, and the ages of the charr were estimated using sacculus otoliths. In fish larger than 10 g, the maximum fibre diameter scaled with body mass (M-b)(0.18) for both fibre types in all morphs. The number of myonuclei per cm fibre length increased with fibre diameter, but was similar between morphs. On average, at 60 pm diameter, there were 2264 nuclei cm(-1) in slow fibres and 1126 nuclei cm(-1) in fast fibres. The absence of fibres of diameter 4-10 mum was used to determine the FL at which muscle fibre recruitment stopped. Slow fibre number increased with body length in all morphs, scaling with b. In contrast, the recruitment of fast muscle fibres continued until a clearly identifiable FL, corresponding to 18-19 cm in the dwarf morph, 24-26 cm in the pelagic morph, 32-33 cm in the large benthic morph and 34-35 cm in the piscivorous morph. The maximum fast fibre number (FNmax) in the dwarf morph (6.97X 10(4)) was 56.5 % of-that found in the LB and PI morphs combined (1.23X10(5)) (P<0.001). Muscle fibre recruitment continued until a threshold body size and occurred at a range of ages, starting at 4+ years in the DB morph and 7+ years in the LB and PI morphs. Our null hypothesis was therefore rejected for fast muscle and it was concluded that the dwarf condition was associated with a reduction in fibre number.

We then investigated whether variations in development temperature associated with different spawning sites and periods were responsible for the observed differences in muscle cellularity between morphs. Embryos from the DB. LB and PL morphs were incubated at temperature regimes simulating cold subterranean spring-fed sites (2.2-3.2degreesC) and the general lakebed (4-7degreesC). Myogenic progenitor cells (MPCs) were identified using specific antibodies to Paired box protein 7 (Pax 7), Forkhead box protein K1-alpha (FoxK1-alpha), MyoD and Myf-5. The progeny showed no evidence of developmental plasticity in the numbers of either MPCs or muscle fibres. Juveniles and adult stages of the DB and LB morphs coexist and have a similar diet. We therefore conclude that the reduction in FNmax, in the dwarf morph probably has a genetic basis and that gene networks regulating myotube production are under high selection pressure. To explain these findings we propose that there is an optimal fibre size. and hence number, which varies with maximum body size and reflects a trade-off between diffusional constraints on fibre diameter and the energy costs of maintaining ionic gradients. The predictions of the optimal fibre size hypothesis and its consequences for the adaptive evolution of muscle architecture in fishes are briefly discussed.

Original languageEnglish
Pages (from-to)4343-4360
Number of pages18
JournalJournal of Experimental Biology
Volume207
Issue number25
DOIs
Publication statusPublished - Dec 2004

Keywords

  • muscle fibres
  • myogenesis
  • growth
  • myogenic progenitor cell
  • resource polymorphism
  • developmental plasticity
  • fish
  • Arctic charr
  • myogenic regulatory factor
  • paired box protein 7
  • forkhead box protein K1-alpha.
  • MYOGENIC SATELLITE CELLS
  • TROUT SALMO-GAIRDNERI
  • ATLANTIC-SALMON
  • SKELETAL-MUSCLE
  • RAINBOW-TROUT
  • SYMPATRIC MORPHS
  • WHITE MUSCLE
  • STEM-CELLS
  • CYPRINUS-CARPIO
  • SEAWATER STAGES

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