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Marine Biology

, Volume 157, Issue 2, pp 221–236 | Cite as

The metabolic demands of swimming behavior influence the evolution of skeletal muscle fiber design in the brachyuran crab family Portunidae

  • Kristin M. Hardy
  • Sean C. Lema
  • Stephen T. Kinsey
Original Paper

Abstract

We investigated the influence of intracellular diffusion on muscle fiber design in several swimming and non-swimming brachyuran crabs. Species with sustained swimming behavior had aerobic dark fibers subdivided into small metabolic functional units, creating short diffusion distances necessary to support the high rates of aerobic ATP turnover associated with endurance activity. This dark fiber design was observed in all swimming species including Ovalipes ocellatus, which has apparently evolved swimming behavior independently of other Portunidae. In addition, we observed fiber and subdivision size-dependent differences in organelle distribution. Mitochondria, which rely on oxygen to function, were uniformly distributed in small fibers/subdivisions, but were clustered at the fiber periphery in larger fibers. The inverse pattern was observed for nuclei, which are not oxygen dependent, but rely on the transport of slow diffusing macromolecules. Phylogenetically independent contrast analysis revealed that these relationships were largely independent of phylogeny. Our results demonstrate cellular responses to diffusion that were necessary for the evolution of swimming and that are likely to be broadly applicable.

Keywords

Swimming Crab Hypertrophic Growth Mitochondrial Density Brachyuran Crab Mitochondrial Distribution 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

The authors are grateful for the helpful comments of Drs. Richard Dillaman, Ann Pabst, Richard Satterlie and Robert Roer, as well as the technical assistance of Mark Gay and Dr. Marcel van Tuinen. This research was supported by a National Science Foundation grant to STK (IOS-0719123) and a National Institute of Arthritis and Musculoskeletal and Skin Diseases grant to STK (R15-AR052708).

Supplementary material

227_2009_1301_MOESM1_ESM.jpg (5.6 mb)
Electronic Supplementary Material (jpg 5.55 mb)

References

  1. Badrinath AS, White AG (2003) Contrasting patterns of mitochondrial redistribution in the early lineages of Caenorhabditis elegans and Acrobeloides sp. PS1146. Dev Biol 258:70–75CrossRefPubMedGoogle Scholar
  2. Bates PC, Millward DJ (1983) Myofibrillar protein turnover. Synthesis rates of myofibrillar and sarcoplasmic protein fractions in different muscles and the changes observed during postnatal development and in response to feeding. Biochem J 214:587–592PubMedGoogle Scholar
  3. Bitoun M, Maugenre S, Jeannet P-Y, Lacene E, Ferrer X, Laforet P, Martin J-J, Laporte J, Lochmuller H, Beggs AH, Fardeau M, Eymard B, Romero NB, Guicheney P (2005) Mutations in dynamin 2 cause dominant centronuclear myopathy. Nat Genet 37:1207–1209CrossRefPubMedGoogle Scholar
  4. Blomberg SP, Garland T (2002) Tempo and mode in evolution: phylogenetic inertia, adaptation and comparative methods. J Evol Biol 15:899–910CrossRefGoogle Scholar
  5. Boyle KL, Dillaman RM, Kinsey ST (2003) Mitochondrial distribution and glycogen dynamics suggest diffusion constraints in muscle fibers of the blue crab, Callinectes sapidus. J Exp Zool 297A:1–16CrossRefGoogle Scholar
  6. Bruusgaard JC, Liestøl K, Ekmark M, Kollstad K, Gunderson K (2003) Number and spatial distribution of nuclei in the muscle fibers of normal mice studied in vivo. J Physiol 551(2):467–478CrossRefPubMedGoogle Scholar
  7. Bruusgaard JC, Brack AS, Hughes SM, Gunderson K (2005) Muscle hypertrophy induces by the ski protein: cyto-architecture and ultrastructure. Acta Physiol Scand 185:141–149CrossRefPubMedGoogle Scholar
  8. Bruusgaard JC, Liestøl K, Gunderson K (2006) Distribution of myonuclei and microtubules in live muscle fibers of young, middle-aged, and old mice. J Appl Physiol 100:2024–2030CrossRefPubMedGoogle Scholar
  9. Carr SD, Tankersley RA, Hench JL, Forward RB Jr, Luettich RA Jr (2004) Movement patterns and trajectories of ovigerous blue crabs Callinectes sapidus during the spawning migration. Estuar Coast Shelf Sci 60:567–579CrossRefGoogle Scholar
  10. Cheek DB, Holt AB, Hill DE, Talbert JL (1971) Skeletal muscle cell mass and growth: the concept of the deoxyribonucleic acid unit. Pediatr Res 5:312–328CrossRefGoogle Scholar
  11. Chilibeck PD, Syrotuik DG, Bell GJ (2002) The effect of concurrent endurance and strength training on quantitative estimates of subsarcolemmal and intermyofibrillar mitochondria. Int J Sports Med 23(1):33–39CrossRefPubMedGoogle Scholar
  12. Cochran DM (1935) The skeletal musculature of the blue crab Callinectes sapidus Rathbun. Smithson Misc Collns 92:1–96Google Scholar
  13. Crow MT, Kushmerick MJ (1982) Chemical energetics of slow- and fast-twitch muscle of the mouse. J Gen Physiol 79:147–166CrossRefPubMedGoogle Scholar
  14. Curtin NA, Kushmerick MJ, Wiseman RW, Woledge RC (1997) Recovery after contraction of white muscle fibres from the dogfish Scyliorhinus canicula. J Exp Biol 200:1061–1071PubMedGoogle Scholar
  15. Felsenstein J (1985) Phylogenies and the comparative method. Am Nat 125:1–15CrossRefGoogle Scholar
  16. Fiedler RA (1930) Solving the question of crab migration. Fish Gazette 47:18–21Google Scholar
  17. Fratini S, Vannini M, Cannicci S, Schubart CD (2005) Tree-climbing mangrove crabs, a case of convergent evolution. Evol Ecol Res 7:219–233Google Scholar
  18. Frederick RL, Shaw JM (2007) Moving mitochondria: establishing distribution of an essential organelle. Traffic 8:1668–1675CrossRefPubMedGoogle Scholar
  19. Fusco D, Bertrand E, Singer RH (2004) Imaging of single mRNAs in the cytoplasm of living cells. Prog Mol Subcell Biol 35:135–150CrossRefPubMedGoogle Scholar
  20. Garland T Jr, Ives AR (2000) Using the past to predict the present: confidence intervals or regression equations in phylogenetic comparative methods. Am Nat 155:346–364CrossRefGoogle Scholar
  21. Garland T, Harvey PH, Ives AR (1992) Procedures for the analysis of comparative data using phylogenetically independent contrasts. Syst Biol 41:18–32Google Scholar
  22. Garland T Jr, Midford PE, Ives AR (1999) An introduction to phylogenetically based statistical methods, with a new method for confidence intervals on ancestral states. Am Zool 39:374–388Google Scholar
  23. Garlick PJ, Maltin CA, Baillie AG, Delday MI, Grubb DA (1989) Fiber-type composition of nine rat muscles. II. Relationship to protein turnover. Am J Physiol 257:E828–E832PubMedGoogle Scholar
  24. Giddings CJ, Gonyea WJ (1992) Morphological observations supporting muscle fiber hyperplasia following weight-lifting exercise in cats. Anat Rec 233:178–195CrossRefPubMedGoogle Scholar
  25. Goldberg AL (1967) Protein synthesis in tonic and phasic skeletal muscle. Nat Lond 216:1219–1220CrossRefGoogle Scholar
  26. Hardy KM, Locke BR, Da Silva MD, Kinsey ST (2006) A reaction–diffusion analysis of energetics in large muscle fibers secondarily evolved for aerobic locomotor function. J Exp Biol 209:3610–3620CrossRefPubMedGoogle Scholar
  27. Hardy KM, Dillaman RM, Locke BR, Kinsey ST (2009) A skeletal muscle model of extreme hypertrophic growth reveals the influence of diffusion on cellular design. Am J Physiol Regul Integr Comp Physiol 296:R1855–R1867PubMedGoogle Scholar
  28. Hartnoll RG (1971) The occurrence, methods and significance of swimming in the Brachyura. Anim Behav 19:34–50CrossRefGoogle Scholar
  29. Hoppeler H, Vogt M (2001) Muscle tissue adaptations to hypoxia. J Exp Biol 204:3133–3139PubMedGoogle Scholar
  30. Howald H, Hoppeler H, Claassen H, Mathieu O, Straub R (1985) Influences of endurance training on the ultrastructural composition of the different muscle fiber types in humans. Pflugers Arch 403(4):369–376CrossRefPubMedGoogle Scholar
  31. Howard CV, Reed MG (1998) Unbiased stereology, 3-dimensional measurements in microscopy. BIOS Scientific, OxfordGoogle Scholar
  32. Jaspers RT, Feenstra HM, van Beek-Harmsen BJ, Huijing PA, van der Laarse WJ (2006) Differential effects of muscle fibre length and insulin on muscle-specific mRNA content in isolated mature muscle fibres during long-term culture. Cell Tissue Res 326:795–808CrossRefPubMedGoogle Scholar
  33. Jimenez AG, Locke BR, Kinsey ST (2008) The influence of oxygen and high-energy phosphate diffusion on metabolic scaling in three species of tail-flipping crustaceans. J Exp Biol 211:3214–3225CrossRefPubMedGoogle Scholar
  34. Johnson LK, Dillaman RM, Gay DM, Blum JE, Kinsey ST (2004) Metabolic influences of fiber size in aerobic and anaerobic muscles of the blue crab, Callinectes sapidus. J Exp Biol 207:4045–4056CrossRefPubMedGoogle Scholar
  35. Judy MH, Dudley DL (1970) Movement of tagged blue crabs in North Carolina waters. Commer Fish Rev 32:29–35Google Scholar
  36. Kayar SR, Claassen H, Hoppeler H, Weibel ER (1986) Mitochondrial distribution in relation to changes in muscle metabolism in rat soleus. Respir Physiol 64(1):1–11CrossRefPubMedGoogle Scholar
  37. Kelly FJ, Lewis SE, Anderson P, Goldspink DF (1984) Pre- and postnatal growth and protein turnover in four muscles of the rat. Muscle Nerve 7:235–242CrossRefPubMedGoogle Scholar
  38. Kim SK, Yu SH, Jeong-Hwa S, Hübner H, Buchholz R (1998) Calculations on O2 transfer in capsules with animal cells for the determination of maximum capsule size without O2 limitation. Biotech Lett 20:549–552CrossRefGoogle Scholar
  39. Kinsey ST, Pathi P, Hardy KM, Jordan A, Locke BR (2005) Does intracellular metabolite diffusion limit post-contractile recovery in burst locomotor muscle? J Exp Biol 208:2641–2652CrossRefPubMedGoogle Scholar
  40. Kinsey ST, Hardy KM, Locke BR (2007) The long and winding road: influences of intracellular metabolite diffusion on cellular organization and metabolism in skeletal muscle. J Exp Biol 210:3505–3512CrossRefPubMedGoogle Scholar
  41. Koch L (1996) What size should a bacterium be? A question of scale. Annu Rev Microbiol 50:317–348CrossRefPubMedGoogle Scholar
  42. Kumar S, Dudley J, Nei M, Tamura K (2008) MEGA: a biologist-centric software for evolutionary analysis of DNA and protein sequences. Brief Bioinfom 9:299–306CrossRefGoogle Scholar
  43. Kushmerick MJ, Paul RJ (1976) Aerobic recovery metabolism following a single isometric tetanus in frog sartorius muscle at 0°C. J Physiol 254:693–709PubMedGoogle Scholar
  44. Kushmerick MJ, Meyer RA, Brown TR (1992) Regulation of oxygen consumption in fast- and slow-twitch muscle. Am J Physiol 263:C598–C606 (Cell Physiol 32)PubMedGoogle Scholar
  45. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948CrossRefPubMedGoogle Scholar
  46. Laurent GJ, Sparrow MP, Bates PC, Millward DJ (1978) Turnover of muscle proteins in the fowl (Gallus domesticus). Rates of protein synthesis in fast and slow skeletal, cardiac and smooth muscle of the adult fowl. Biochem J 176:393–401PubMedGoogle Scholar
  47. Mahon BC, Neigel JE (2008) Utility of arginine kinase for resolution of phylogenetic relationships among brachyuran genera and families. Mol Phylogenet Evol 48:718–727CrossRefPubMedGoogle Scholar
  48. Mainwood GW, Rakusan K (1982) A model for intracellular energy transport. Can J Physiol Pharmacol 60:98–102PubMedGoogle Scholar
  49. Mantelatto FL, Robles R, Felder DL (2007) Molecular phylogeny of the western Atlantic species of the genus Portunus (Crustacea, Brachyura, Portunidae). Zool J Linn Soc 150:211–220CrossRefGoogle Scholar
  50. Midford PE, Garland T Jr, Maddison WP (2005) PDAP package of Mesquite. Version 1.07Google Scholar
  51. Milner DJ, Weitzer G, Tran D, Bradley A, Capetanaki Y (1996) Disruption of muscle architecture and myocardial degeneration in mice lacking desmin. J Cell Biol 134:1255–1270CrossRefPubMedGoogle Scholar
  52. Nyack AC, Locke BR, Valencia A, Dillaman RM, Kinsey ST (2007) Scaling of postcontractile phosphocreatine recovery in fish white muscle: effect of intracellular diffusion. Am J Physiol Regul Integr Comp Physiol 292:R2077–R2088PubMedGoogle Scholar
  53. Palumbi S, Martin A, Romano S, McMillan WO, Stice L, Grabowski G (1991) The simple fool’s guide to PCR. Department of Zoology and Kewalo Marine Laboratory, University of Hawaii, HonoluluGoogle Scholar
  54. Presnell JK, Schreibman MP (1997) Animal tissue techniques, 5th edn. Johns Hopkins University Press, BaltimoreGoogle Scholar
  55. Ralston E, Lu Z, Biscocho N, Soumaka E, Mavrodis M, Prats C, Lomo T, Capetanaki Y, Plous T (2006) Blood vessels and desmin control the positioning of nuclei in skeletal muscle fibers. J Cell Physiol 209(3):874–882CrossRefPubMedGoogle Scholar
  56. Rathbun MJ (1930) The cancroid crabs of America of the families euryalidae, portunidae, atelecyclidae, cancridae, and xanthidae. Bull US Natl Mus 152:1–609Google Scholar
  57. Robles R, Schubart CD, Conde JE, Carmona-Suarez C, Alvarez F, Villalobos JL, Felder DL (2007) Molecular phylogeny of the American Callinectes Stimpson, 1860 (Brachyura: Portunidae), based on two partial mitochondrial genes. Mar Biol 150:1265–1274CrossRefGoogle Scholar
  58. Roy RR, Monke SR, Allen DL, Edgerton VR (1999) Modulation of myonuclear number in functionally overloaded and exercised rat plantaris fibers. J Appl Physiol 87:634–642PubMedGoogle Scholar
  59. Rube DA, van der Bliek AM (2004) Mitochondrial morphology is varied and dynamic. Mol Cell Biochem 256–257:331–339CrossRefPubMedGoogle Scholar
  60. Russell B, Dix DJ (1992) Mechanisms for intracellular distribution of mRNA: in situ hybridization studies in muscle. Am J Physiol 262:C1–C8 (Cell Physiol 31)PubMedGoogle Scholar
  61. Russell B, Motlagh D, Ashley WW (2000) Form follows function: how muscle shape is regulated by work. J Appl Physiol 88:1127–1132PubMedGoogle Scholar
  62. Schmalbruch H, Hellhammer U (1977) The number of nuclei in adult rat muscles with special reference to satellite cells. Anat Rec 189:169–176CrossRefPubMedGoogle Scholar
  63. Schubart CD, Neigel JE, Felder DL (2000) Use of the mitochondrial 16S rRNA gene for phylogenetic and population studies of Crustacea. Crustac Issues 12:817–830Google Scholar
  64. Smirnova L, Shurland D-L, Ryazantsev SN, van der Bliek AM (1998) A human dynamin-related protein controls the distribution of mitochondria. J Cell Biol 143:351–358CrossRefPubMedGoogle Scholar
  65. Spirito CP (1972) An analysis of swimming behaviour in the Portunid crab Callinectes sapidus. Mar Behav Physiol 1:261–276CrossRefGoogle Scholar
  66. Starr DA (2007) Communication between the cytoskeleton and the nuclear envelope to position the nucleus. Mol BioSyst 3:583–589CrossRefPubMedGoogle Scholar
  67. Starr DA, Han M (2002) The role of ANC-1 in tethering nuclei to the actin cytoskeleton. Science 298:406–409CrossRefPubMedGoogle Scholar
  68. Teissier G (1939) Biometrie de la cellule. Tabulae Biologicae 19:1–64Google Scholar
  69. Thompson DW (1917) On growth and form. Cambridge University Press, CambridgeGoogle Scholar
  70. Tse FW, Govind CK, Atwood HL (1983) Diverse fiber composition of swimming muscles in the blue crab, Callinectes sapidus. Can J Zool 61:52–59CrossRefGoogle Scholar
  71. Tyler S, Sidell BD (1984) Changes in mitochondrial distribution and diffusion distances in muscle of goldfish upon acclimation to cold temperatures. J Exp Biol 232:1–9Google Scholar
  72. van Blerkom JV (1991) Microtubule mediation of cytoplasmic and nuclear maturation during the ear. Proc Natl Acad Sci 88:5031–5035CrossRefPubMedGoogle Scholar
  73. Williams A (1974) The swimming crabs of the genus Callinectes (Decapoda: Portunidae). Fish Bull 72:685–798Google Scholar
  74. Wright CS (1984) Structural comparison of the two distinct sugar binding sites in wheat germ agglutinin isolectin II. J Mol Biol 178:91–104CrossRefPubMedGoogle Scholar
  75. Zimmer-Faust RK, Fielder DR, Heck KL, Coen LD, Morgan SG (1994) Effects of tethering on predatory escape by juvenile blue crabs. Mar Ecol Prog Ser 111:299–303CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  • Kristin M. Hardy
    • 1
  • Sean C. Lema
    • 1
  • Stephen T. Kinsey
    • 1
  1. 1.Department of Biology and Marine BiologyUniversity of North Carolina WilmingtonWilmingtonUSA

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