The enigma of reversed asymmetry in lithodid crabs: Absence of evidence for heritability or induction of morphological handedness in Lopholithodes foraminatus

Evolution and Development

Volumn 12, Issue 1, 2010, Pages 74-83

  Duguid, William D P ^a  

^a UNIVERSITY OF VICTORIA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CRAB; ENVIRONMENTAL FACTOR; EVOLUTIONARY BIOLOGY; HANDEDNESS; HERITABILITY; MORPHOLOGY; MUTATION; PHENOTYPE;

ABDOMEN; ANIMAL; ANIMAL ANATOMY; ANOMURA; ARTICLE; EVOLUTION; FEMALE; GENETICS; GROWTH, DEVELOPMENT AND AGING; LARVA; MANDIBLE; MORPHOGENESIS; PHENOTYPE; SCANNING ELECTRON MICROSCOPY; TEMPERATURE;

ABDOMEN; ANIMAL STRUCTURES; ANIMALS; ANOMURA; BODY PATTERNING; EVOLUTION; FEMALE; LARVA; MANDIBLE; MICROSCOPY, ELECTRON, SCANNING; PHENOTYPE; TEMPERATURE;

CALAPPIDAE; CHACEON AFFINIS; DECAPODA (CRUSTACEA); LIMULUS; LITHODIDAE; LOPHOLITHODES FORAMINATUS;

EID: 74849108899     PISSN: 1520541X     EISSN: 1525142X     Source Type: Journal    
DOI: 10.1111/j.1525-142X.2009.00392.x     Document Type: Article

References (69)

1. Abby-Kalio, N. J. Warner, G. F. 1989. Heterochely and handedness in the shore crab Carcinus maenas (L.) (Crustacea: Brachyura). Zool. J. Linn. Soc. 96 : 19 26.
2. Afzelius, B. A. 1976. A human syndrome caused by immotile cilia. Science 193 : 317 319.
3. Aritaki, M., Ohta, K., Hotta, Y., Tagawa, M. Tanaka, M. 2004. Temperature effects on larval development and occurrence of metamorphosis-related morphological abnormalities in hatchery-reared spotted halibut Verasper variegatus juveniles. Nippon Suisan Gakkaishi 70 : 8 15.
4. Asami, T., Cowie, R. H. Ohbayashi, K. 1998. Evolution of mirror images by sexually asymmetric mating behavior in hermaphroditic snails. Am. Nat. 152 : 225 236.
5. Asami, T., Gittenberger, E. Falkner, G. 2008. Whole-body enantiomorphy and maternal inheritance of chiral reversal in the pond snail Lymnaea stagnalis. J. Heredity 99 : 552 557.
6. Bergmann, D. C., Crew, J. R., Kramer, J. M. Wood, W. B. 1998. Cutical chirality and body handedness in Caenorhabditis elegans. Dev. Genet. 23 : 164 174.
7. Brown, N. A. Wolpert, L. 1990. The development of handedness in left/right asymmetry. Development 109 : 1 9.
8. Campodonico, G. I. 1978. Un caso de inversión en la asimetría abdominal de las hembras de Paralomis granulosa (Jacquinot) (Decapoda, Anomura, Lithodidae). An. Inst. Patagonia 9 : 231 232.
9. Crain, J. A. McLaughlin, P. A. 2000. Larval and early juvenile development in the Lithodidae (Decapoda: Anomura: Paguroidea) reared under laboratory conditions. 1. subfamily Lithodinae: Lopholithodes mandtii Brandt, 1848. Invertebr. Reprod. Dev. 37 : 43 59.
10. Crampton, H. E. 1894. Reversal of cleavage in a sinistral gastropod. Ann. NY Acad. Sci. 7 : 167 171.
11. Cunningham, C. W., Blackstone, N. W. Buss, L. W. 1992. Evolution of king crabs from hermit crab ancestors. Nature 335 : 539 542.
12. Duguid, W. D. P. Page, L. R. 2009. Larval and early post-larval morphology, growth, and behaviour of laboratory reared Lopholithodes foraminatus (brown box crab). J. Mar. Biol. Assoc. UK, doi :.
13. Factor, J. R. 1978. Morphology of the mouthparts of larval lobsters, Homarus americanus (Decapoda: Nephropidae), with special emphasis on their setae. Biol. Bull. 154 : 383 408.
14. Farmer, A. S. 1974. The functional morphology of the mouthparts and pereiopods of Nephrops norvegicus (L.) (Decapoda: Nephropidae). J. Nat. His. 8 : 121 142.
15. Fisheries and Oceans Canada. 2008. Inside passage: Northern Strait of Georgia: winter and spring. Range Profiles Data Page. Fisheries and Oceans Canada. Available at (accessed January 22, 2009).
16. Fornbacke, M., Gombrii, M. Lundberg, A. 2002. Sidedness frequencies in the flounder Platichthys flesus (Pleuronectiformes) along a biogeographical cline. Sarsia 87 : 392 395.
17. Freeman, G. Lundelius, J. W. 1982. The developmental genetics of dextrality and sinistrality in the gastropod Lymnaea peregra. Wilhelm Roux's Arch. Dev. Biol. 191 : 69 83.
18. Goddard, J. 1997. Size at maturity in box crabs, Lopholithodes foraminatus, from Oregon. Report prepared for the Oregon Department of Fish and Wildlife, 7pp.
19. Gould, S. J. Young, N. D. 1985. The consequences of being different: sinistral coiling in Cerion. Evolution 39 : 1364 1379.
20. Gould, S. J. 1992. We are all monkeys' uncles. Nat. Hist. 6 : 14 21.
21. Govind, C. K. Pearce, J. 1986. Differential reflex activity determines claw and closer muscle asymmetry in developing lobsters. Science 233 : 354 356.
22. Govind, C. K. Pearce, J. 1989a. Critical period for determining claw and closer muscle asymmetry in developing lobsters. J. Exp. Zool. 249 : 31 35.
23. Govind, C. K. Pearce, J. 1989b. Delayed determination of claw laterality in lobsters following loss of target. Development 107 : 547 551.
24. Jones, D. S. George, R. W. 1982. Handedness in fiddler crabs as an aid in taxonomic groupings of the genus Uca (Decapoda Ocypodidae). Crustaceana 43 : 100 102.
25. Konishi, K. 2007. Morphological notes on the mouthparts of decapod crustacean larvae, with emphasis on palinurid phyllosomas. Bull. Fish. Res. Agency 20 : 73 75.
26. Ladle, R. J. Todd, P. A. 2006. A developmental model for predicting the handedness frequencies in crabs. Acta Oecol. 30 : 283 287.
27. Layton, W. M. 1976. Random determination of a developmental process - reversal of normal visceral asymmetry in mouse. J Heredity 67 : 336 338.
28. Levin, M. Palmer, A. R. 2007. Left-right patterning from the inside out: widespread evidence for intracellular control. BioEssays 29 : 271 287.
29. MacGinitie, G. E. MacGinitie, N. 1949. Natural History of Marine Animals. McGraw-Hill, New York, p. 300.
30. Mariappan, P., Balasundaram, C. Schmitz, B. 2000. Decapod crustacean chelipeds: an overview. J. Biosci. 25 : 301 313.
31. McGaw, I. J. Duff, S. D. 2008. Cardiovascular system of anomuran crabs, genus Lopholithodes. J. Morphol. 269 : 1295 1307.
32. McLaughin, P. A., Anger, K., Kaffenberger, A. Lovrich, G. A. 2003. Larval and early juvenile development in Paralomis granulosa (Jacquinot) (Decapoda: Anomura: Paguroidea: Lithodidae), with emphasis on abdominal changes in megalopal and crab stages. J. Nat. Hist. 37 : 1433 1452.
33. McLaughlin, P. A. Lemaitre, R. 1997. Carcinization in the Anomura - fact or fiction? I. Evidence from adult morphology. Contrib. Zool. 67 : 79 123.
34. McLaughlin, P. A. Lemaitre, R. 2001. A new family for a new genus and new species of hermit crab of the superfamily Paguroidea (Decapoda: Anomura) and its phylogenetic implications. J. Crust. Biol. 21 : 1062 1076.
35. McLaughlin, P. A., Lemaitre, R. Sorhannus, U. 2007. Hermit crab phylogeny: a reappraisal and its "fall-out". J. Crust. Biol. 27 : 97 115.
36. McLaughlin, P. A., Lemaitre, R. Tudge, C. C. 2004. Carcinization in the Anomura - fact or fiction? II. Evidence from larval, megalopal and early juvenile morphology. Contrib. Zool. 73 : 165 205.
37. McLaughlin, P. A. Paul, A. J. 2002. Abdominal and pleopod changes in Lithodes aequispinus Benedict, 1895 (Crustacea: Decapoda: Anomura: Lithodidae) from megalopa to juvenile. Proc. Biol. Soc. Wash. 115 : 138 147.
38. Meshcheryakov, V. N. Beloussov, L. V. 1975. Asymmetrical rotations of blastomeres in early cleavage of Gastropoda. Deve. Genes Evol. 177 : 193 203.
39. Motoh, H. 2002. A case of reversed asymmetry in the red king crab, Paralithodes camtschaticus. Cancer 11 : 11 13.
40. Motoh, H. 2003. A further case of reversed asymmetry in the red king crab, Paralithodes camtschaticus. Cancer 12 : 23 25.
41. Motoh, H. Toyota, K. 2006. A case of reversed asymmetry in a lithodid crab, Paralomis hystrix. Cancer 15 : 25 27.
42. Newman, H. H. 1925. An experimental analysis of asymmetry in the starfish, Patria miniata. Biol. Bull. 49 : 111 138.
43. Ng, P. K. L. Tan, L. W. H. 1985. Right-handedness' in heterochelous calappoid and xanthoid crabs - suggestions for a functional advantage. Crustaceana 49 : 98 100.
44. Okumura, T., Utsuno, H., Kuroda, J., Gittenberger, E., Asami, T. Matsuno, K. 2008. The development and evolution of left-right asymmetry in invertebrates: lessons from Drosophila and snails. Dev. Dyn. 237 : 3497 3515.
45. Palmer, A. R. 1996. From symmetry to asymmetry: phylogenetic patterns of asymmetry variation in animals and their evolutionary significance. Proc. Nat. Acad. Sci. USA 93 : 14279 14286.
46. Palmer, A. R. 2004. Symmetry breaking and the evolution of development. Science 306 : 828 833.
47. Palmer, A. R. 2005. Antisymmetry. In B. Hallgrimsson B. K. Hall (eds.). Variation. Academic, New York, pp. 359 397.
48. Parker, G. H. 1903. The optic chiasma in teleosts and its bearing on the asymmetry of the Heterostomata (flatfishes). Bull. Mus. Compar. Zool Harv. Univ. 40 : 221 242.
49. Policansky, D. 1982. Flatfishes and the inheritance of asymmetries. Behav. Brain Sci. 5 : 262 265.
50. Powell, G. C. Hurd, C. L. 1972. Observations of initial king crab egg attachment. Trans. Am. Fish. Soc. 101 : 557 559.
51. Read, A. T. Govind, C. K. 1997. Claw transformation and regeneration in adult snapping shrimp: test of the inhibition hypothesis for maintaining bilateral asymmetry. Biol. Bull. 193 : 401 409.
52. Richter, S. Scholtz, G. 1994. Morphological evidence for a hermit crab ancestry of lithodids (Crustacea, Decapoda, Anomala, Paguroidea). Zool. Anz. 223 : 187 219.
53. Robertson, R. 1993. Snail handedness. Nat. Geogr. Res. Explor. 9 : 104 119.
54. Sandberg, L. McLaughlin, P. A. 1998. Crustacea, Decapoda, Paguridae. In Marine Invertebrates of Scandinavia. Universitesforlaget, Oslo, 10 : 1 113.
55. Schreiber, A. M. 2006. Asymmetric craniofacial remodelling and lateralized behaviour in larval flatfish. J. Exp. Biol. 209 : 610 621.
56. Shigemiya, Y. 2003. Does the handedness of the pebble crab Eriphia smithii influence its attack success on two dextral snail species? J. Zool. Lond. 260 : 259 265.
57. Spéder, P., Ádám, G. Noselli, S. 2006. Type ID unconventional myosin controls left-right asymmetry in Drosophila. Nature 440 : 803 807.
58. Spéder, P., Petzoldt, A., Magali, S. Noselli, S. 2007. Strategies to establish left/right asymmetry in vertebrates and invertebrates. Curr. OpGenet. Dev. 17 : 351 358.
59. Stevens, B. G. Munk, J. E. 1991. Lateral asymmetry in the thoracic segmentation of a king crab, Paralithodes camtschaticus (Tilesius, 1815) (Decapoda, Anomura), from Kodiak, Alaska. Crustaceana 61 : 317 320.
60. Sucharit, C., Asami, T. Panha, S. 2007. Evolution of whole-body enantiomorphy in the tree snail genus Amphidromus. J. Evol. Biol. 20 : 661 672.
61. Sumner, F. B. Huestis, R. R. 1921. Bilateral asymmetry and its relation to certain problems of genetics. Genetics 6 : 445 485.
62. Trott, T. J. 1987. The prevalence of left-handedness in the painted ghost crab Ocypode gaudichaudii H. Milne Edwards and Lucas (Decapoda, Brachyura, Ocypodidae). Crustaceana 52 : 213 215.
63. Van Valen, L. 1962. A study of fluctuating asymmetry. Evolution 16 : 125 142.
64. Vermeij, G. T. 1977. Patterns in crab claw size: the geography of crushing. Syst. Zool. 26 : 138 151.
65. Wood, W. B., Bergmann, D. Florance, A. 1996. Maternal effect of low temperature on handedness determination in C. elegans embryos. Devel. Genet. 19 : 222 230.
66. Yamaguchi, T. 1977. Studies on the handedness of the fiddler crab, Uca lactea. Biol. Bull. 152 : 424 436.
67. Yokoyama, T., Copeland, N. G., Jenkins, N. A., Montgomery, C. A., Elder, F. B. Overbeek, P. A. 1993. Reversal of left-right asymmetry: a situs inversus mutation. Science 260 : 679 682.
68. Zaklan, S. D. 2000. A case of reversed asymmetry in Lithodes maja (Linnaeus, 1758) (Decapoda, Anomura, Lithodidae). Crustaceana 73 : 1019 1022.
69. Zaklan, S. D. 2002. Review of the family Lithodidae (Crustacea: Anomura: Paguroidea): distribution, biology, and fisheries. In A. J. Paul, E. G. Dawe, R. Elner, G. S. Jamieson, G. H. Kruse, R. S. Otto, B. Sainte-Marie, T. C. Shirley D. Woodby (eds.). Crabs in Cold Water Regions: Biology, Management, and Economics. University of Alaska Sea Grant College Program, Fairbanks, pp. 751 845.