Evolution, Development and Ecology of Capitella sp. I: A Waxing Model for Polychaete Studies

Annelids in Modern Biology

Volumn , Issue , 2009, Pages 88-115

  Hill, Susan D ^a,b   Savage, Robert M ^b,c  

^a MICHIGAN STATE UNIVERSITY   (United States)

^b MBL   (United States)

^c WILLIAMS COLLEGE   (United States)

Author keywords

Annelid genomics draft genome sequence; Evolution, development and ecology of capitella sp. i a waxing model; Gene expression during specification and germ layer differentiation

Indexed keywords

EID: 76949083465     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1002/9780470455203.ch6     Document Type: Chapter

References (118)

1. Agee, S.J., Lyons, D.C., Weisblat, D.A. 2006. Maternal expression of a NANOS homolog is required for early development of the leech Helobdella robusta. Dev. Biol. 298, 1-11.
2. Arenas-Mena, C. 2006. Embryonic expression of HeFoxA1 and HeFoxA2 in an indirectly developing polychaete. Dev. Genes Evol. 216, 727-736.
3. Arenas-Mena, C., Suk-Ying Wong, K., Arandi-Forosani, N. 2007. Ciliary band gene expression patterns in the embryo and trochophore larva of an indirectly developing polychaete. Gene Expr. Patterns 7, 544-549.
4. Arendt, D., Technau, U., Wittbrodt, J. 2001. Evolution of the bilaterian foregut. Nature 409, 81-85.
5. Barrallo-Gimeno, A., Nieto, M.A. 2005. The Snail genes as inducers of cell movement and survival: implications in development and cancer. Development 132, 3151-3161.
6. Bely, A.E., Weisblat, D.A. 2006. Lessons from leeches: a call for DNA barcoding in the lab. Evol. Dev. 8, 491-501.
7. Bely, A.E., Wray, G.A. 2001. Evolution of regeneration and fission in annelids: insights from engrailed-and orthodenticle-class gene expression. Development 128, 2781-2791.
8. Bergter, A., Paululat, A. 2007. Pattern of body wall muscle differentiation during embryonic development of Enchytraeus coronatus (Annelida: Oligochaeta; Enchytraeidae). J. Morph. 268, 537-549.
9. Bergter, A., Hunnekuhl, V.S., Schniederjans, M., Paululat, A. 2007. Evolutionary aspects of pattern formation during clitellate muscle development. Evol. Dev. 9, 602-617.
10. Bergter, A., Brubacher, J.L., Paululat, A. 2008. Muscle formation during embryogenesis of the polychaete Ophryotrocha diadema (Dorvalidae)-new insights into annelid muscle patterns. Front. Zool. 5.
11. Biggers, W.J., Laufer, H. 1992. Chemical induction of settlement and metamorphosis of Capitella capitata Sp. I (Polychaeta) larvae by juvenile hormone-active compounds. Invertebr. Reprod. Dev. 22, 39-46.
12. Biggers, W.J., Laufer, H. 1999. Settlement and metamorphosis of Capitella larvae induced by juvenile hormone -active compounds is mediated by protein kinase C and ion channels. Biol. Bull. 196, 187-198.
13. Blake, J.A., Grassle, J.P., Eckelbarger, K.J. In press. A new species designation for the experimental capitellid, Capitella sp. I, with a review of the literature for confirmed records. In: Maciolek, N.J., J.A. Blake (Eds). Proceedings of the Ninth International Polychaete Conference. Zoosymposia 2. Auckland, New Zealand: Magnolia Press.
14. Boyle, M.J., Seaver, E.C. 2008a. Developmental expression of Fox A and GATA genes during gut formation in the polychaete annelid, Capitella sp. I. Evol. Dev. 10, 89-105.
15. Boyle, M.J., Seaver, E.C. 2008b. Evidence of a dorsal pharynx in the marine polychaete, Capitella sp. I (Polychaeta: Capitellidae). Zootaxa (in press).
16. Brooke, N.M., Garcia-Fernandez, J., Holland, P.W.H. 1998. The ParaHox gene cluster is an evolutionary sister of the Hox gene cluster. Nature 392, 920-922.
17. Butman, C.A., Grassle, J.P., Webb, C.M. 1988. Substrate choices made by marine larvae settling in still water and in a flume flow. Nature 333, 771-773.
18. Butts, T., Holland, P.W.H., Ferrier, D.E.K. 2008. The urbilaterian Super-Hox cluster. Trends Genet. 24, 259-262.
19. Carroll, S.B., Grenier, J.K., Weatherbee, S.D. 2005. From DNA to Diversity Molecular Genetics and the Evolution of Animal Design, 2nd edn. Malden, MA: Blackwell Publishing.
20. Chipman, A.D. 2008. Annelids step forward. Evol. Dev. 10, 141-142.
21. Chipman, A.D., Arthur, W., Akam, M. 2004. A double segment periodicity underlies segment generation in centipede development. Curr. Biol. 14, 1250-1255.
22. Choe, C.P., Miller, S.C., Brown, S.J. 2006. A pair-rule gene circuit defines sequentially in the short-germ insectTribolium castaneum. Proc. Natl. Acad. Sci. U.S.A. 103, 6560-6564.
23. Cohen, R.A., Pechenik, J.A. 1999. Relationship between sediment organic content, metamorphosis, and postlarval performance in the deposit-feeding polychaete Capitella sp. I. J. Exp. Mar. Biol. Ecol. 240, 1-18.
24. Damen, W.G. 2007. Evolutionary conservation and divergence of segmentation process in arthropods. Dev. Dyn. 236, 1379-1391.
25. Damen, W.G., Janssen, R., Prpic, N.M. 2005. Pair rule gene orthologs in spider segmentation. Evol. Dev. 7, 618-628.
26. von Dassow, G., Meir, E., Munro, E., Odell, G. 2000. The segment polarity network is a robust developmental module. Nature 406, 188-192.
27. Davis, G.K., D' Alessio, J.A., Patel, N.H. 2005. Pax3/7 genes reveal conservation and divergence in the arthropod segmentation hierarchy. Dev. Biol. 285, 169-184.
28. Dequeant, M.L., Pourquie, O. 2008. Segmental patterning of the vertebrate embryonic axis. Nat. Rev. Genet. 9, 370-382.
29. Dill, K.K., Seaver, E.C. 2008. Vasa and nanos are co -expressed in somatic and germ line tissue from early embryonic cleavage stages through adulthood in the polychaete Capitella sp. I. Dev. Genes Evol. 218, 453-463.
30. Dill, K.K., Thamm, K., Seaver, E.C. 2007. Characterization of twist and snail gene expression during mesoderm and nervous system development in the polychaete annelid Capitella sp. I. Dev. Genes Evol. 217, 435-447.
31. Du, H., Han, J., Lin, K., Qu, X., Wang, W. 2007. Characterization of 11 microsatellite loci derived from genomic sequences of polychaete Capitella capitata complex. Mol. Ecol. Notes 7, 1144-1146.
32. Dunn, C.W., Hejnol, A., Matus, D.Q., Pang, K., Browne, W.E., Smith, S.A., Seaver, E., Rouse, G.W., Obst, M., Edgecombe, G.D., Sørensen, M.V., Haddock, S.H.D., Schmidt-Rhaesa, A., Okusu, A., Kristensen, R.M., Wheeler, W.C., Martindale, M.Q., Giribet, G. 2008. Broad phylogenetic sampling improves resolution of the animal tree of life. Nature 452, 745-749.
33. Eckelbarger, K.J., Grassle, J.P. 1983. Ultrastructural differences in the eggs and ovarian follicle cells of Capitella (Polychaeta) sibling species. Biol. Bull. 165, 379-393.
34. Eckelbarger, K.J., Grassle, J.P. 1987a. Interspecific variation in genital spine, sperm and larval morphology in six sibling species of Capitella. Bull. Biol. Soc. Wash. 7, 62-76.
35. Eckelbarger, K.J., Grassle, J.P. 1987b. Spermatogenesis, sperm storage and comparative sperm morphology in nine species of Capitella, Capitomastus and Capitellides (Polychaeta: Capitellidae). Mar. Biol. 95, 415-429.
36. Eisig, H. 1899. Zur Entwicklungsgeschichte der Capitelliden. Mitt. Zool. Station Neapel 13, 1-292.
37. Ferrier, D.E.K., Holland, P.W.H. 2001. Sipunculan ParaHox genes. Evol. Dev. 3, 263-270.
38. Finnerty, J.R., Paulson, D., Burton, P., Pang, K., Martindale, M.Q. 2003. Early evolution of a homeobox gene: the parahox gene Gsx in the Cnidaria and Bilateria. Evol. Dev. 5, 331-345.
39. Forbes, V.E., Andreassen, M.S.H., Christensen, L. 2001. Metabolism of the polycyclic aromatic hydrocarbon fluoranthene by the polychaete Capitella capitata species I. Environ. Toxicol. Chem. 20, 738-747.
40. Fröbius, A.C., Seaver, E.C. 2006a. Capitella sp.I homeobrain-like, the first lophotrochozoan member of a novel paired-like homeobox gene family. Gene Expr. Patterns 6, 985-991.
41. Fröbius, A.C., Seaver, E.C. 2006b. ParaHox gene expression in the polychaete annelid Capitella sp. I. Dev. Genes Evol. 216, 81-88.
42. Fröbius, A.C., Matus, D.Q., Seaver, E.C. In press. Genomic organization and expression demonstrate spatial and temporal Hox gene colinearity in the lophotrochozoan Capitella sp. I. PloS ONE.
43. Fugiwara, Y., Kawato, M., Yamamoto, T., Yamanaka, T., Sato-Okoshi, W., Noda, C., Tsuchida, S., Komai, T., Cubelio, S.S., Sasaki, T., Jacobsen, K., Kubokawa, K., Fujikura, K., Maruyama, T., Furushima, Y., Okoshi, K., Miyake, H., Miyazki, M., Nogi, Y., Yatabe, A., Okutani, T. 2007. Three-year investigations into sperm whale-fall ecosystems in Japan. Mar. Ecol. 38, 1-14.
44. Furlong, R.F., Younger, R., Kasahara, M., Reinhardt, R., Thorndyke, M., Holland, P.W.H. 2007. A degenerate Parahox gene cluster in a degenerate vertebrate. Mol. Biol. Evol. 24, 2681-2686.
45. Gabriel, W.N., Goldstein, B. 2007. Segmental expression of Pax3.7 and engrailed homologs in tardigrade development. Dev. Genes Evol. 217, 421-33.
46. Garcia-Fernández, J. 2005. The genesis and evolution of homeobox gene clusters. Nat. Rev. Genet. 6, 881-92.
47. Gillis, W.J., Bowerman, B., Schneider, S.Q. 2007. Ectoderm-and endoderm-specific GATA transcription factors in the marine annelid Platynereis dumerilii. Evol. Dev. 9, 39-50.
48. Gillis, W.Q., Bowerman, B.A., Schneider, S.Q. 2008. The evolution of protostome GATA factors: Molecular phylogenetics, synteny, and intron / exon structure reveal orthologous relationships. BMC Evol. Biol. 8, 112.
49. Goldstein, B., Leviten, M.W., Weisblat, D.A. 2001. Dorsal and snail homologs in leech development. Dev. Genes Evol. 211, 329-337.
50. Grassle, J.F., Grassle, J.P. 1974. Opportunistic life histories and genetic systems in marine benthic polychaetes. Jour. Mar. Res. 32, 253-284.
51. Grassle, J.F., Grassle, J.P. 1978. Life histories and genetic variation in marine invertebrates. In The Genetics, Ecology, and Evolution of Marine Organisms, edited by J.A. Beardmore and B. Battaglia. New York: Plenum Press, pp. 347-364.
52. Grassle, J.P., Grassle, J.F. 1976. Sibling species in the marine pollution indicator Capitella (Polychaeta). Science 192, 567-569.
53. Grassle, J.P., Gelfman, C.E., Mills, S.W. 1987. Karyotypes of Capitella sibling species, and of several speciesin the related genera Capitellides and Capitomastus (C. Polychaeta). Bull. Biol. Soc. Wash. 7, 77-88.
54. Halanych, K.M. 2004. A new view of animal phylogeny. Ann. Rev. Ecol. Syst. 35, 229-256.
55. Handel, K., Basal, A., Fan, X., Roth, S. 2005. Tribolium castaneum twist: gastrulation and mesoderm formation in a short germ-band beetle. Dev. Genes Evol. 215, 13-31.
56. Harfe, B.D., Vaz Gomes, A., Kenyon, C., Liu, J., Krause, M., Fire, A. 1998. Analysis of Caenorhabditis elegans Twist homologue identifies conserved and divergent patterning. Genes Dev. 12, 2623-2635.
57. He, Z.B., Cao, Y.Q., Wang, Z.K., Chen, B., Peng, G.X., Xia, Y.X. 2006. Role of hunchback in segment patterning of Locusta migratoria manilensis revealed by parental RNAi. Dev. Growth Differ. 48, 439-45.
58. Hebert, P.D.N., Cywinska, A., Ball, S.L., deWaard, J.R. 2003. Biological identifications through DNA barcodes. Proc. R. Soc. Lond. B 270, 313-321.
59. Henry, J.Q., Hejnol, A., Perry, K.J., Martindale, M.Q. 2007. Homology of ciliary bands in spiralian trochophores. Integr. Comp. Biol. 47, 865-871.
60. Hill, S.D., Boyer, B.C. 2001. Phalloidin labeling of developing muscle in embryos of the polychaete Capitella sp. I. Biol. Bull. 201, 257-258.
61. Hill, S.D., Boyer, B.C. 2003. HNK-1/N-CAM immunoreactivity correlates with ciliary patterns during development of the polychaete Capitella sp. I. Biol. Bull. 205, 182-184.
62. Hill, S.D., Boyer, B.C. 2005. The role of heterochrony in the evolution of the life cycle of the opportunistic polychaete Capitella sp. I. Developmental Basis of Evolutionary Change Symposium, Chicago, October 2005 (Abstract).
63. Hill, S.D., Grassle, J.P., Mills, S.W. 1982. Regeneration and maturation in two sympatric Capitella (Polychaeta) sibling species. Biol. Bull. 163, 366.
64. Hill, S.D., Grassle, J.P., Ferkowicz, M.J. 1987. Effect of segment loss on reproductive output in Capitella species I. Biol. Bull. 173, 430.
65. Hill, S.D., Ferkowicz, M.J., Grassle, J.P. 1988. Effect of tail regeneration on early fecundity in Capitella sp. I and II. Biol. Bull. 175, 311.
66. Holbrook, M.J.L., Grassle, J.P. 1984. The effect of low density on the development of simultaneous hermaphroditism in male Capitella sp. I (Polychaeta). Biol. Bull. 166, 103-109.
67. Hopwood, N.D., Pluck, A., Gurdon, J.B. 1989. A Xenopus mRNA related to Drosophila twist is expressed in response to induction in the mesoderm and the neural crest. Cell 59, 893-903.
68. Irvine, S.Q., Martindale, M.Q. 2001. Comparative analysis of Hox gene expression in the polychaete Chaetopterus: implications for the evolution of body plan regionalization. Am. Zool. 41, 640-651.
69. Jenner, R.A. 2006. Unburdening evo-dev: ancestral attractions, model organisms, and basal baloney. Dev. Genes Evol. 216, 385-394.
70. Kang, D., Huang, F., Li, D., Shankland, M., Gaffield, W., Weisblat, D.A. 2003. A hedgehog homolog regulates gut formation in leech ( Helobdella ). Development 130, 1645-1657.
71. Kerner, P., Zelada Gonzales, F., Le Gouar, M., Ledent, V., Arendt, D., Vervoort, M. 2006. The expression of a hunchback ortholog in the polychaete annelid Platynereis dumerilii suggests an ancestral role in mesoderm development and neurogenesis. Dev. Genes Evol. 216, 821-828.
72. Kinoshita, K., Tamaki, S., Yoshioka, M., Srithonguthai, S., Kunihiro, T., Hama, D., Ohwada, K., Tsutsumi, H. 2008. Bioremediation of organically enriched sediment deposited below fish farms with artificially mass-cultured colonies of a deposit-feeding polychaete Capitella sp. I. Fish. Sci. 74, 77-87.
73. Kulakova, M., Bakalenko, N., Novikova, E., Cook, C.E., Eliseeva, E., Steinmetz, P.R.H., Kostyuchenko, R.P., Dondua, A., Arendt, D., Akam, M., Andreeva, T. 2007. Hox gene expression in larval development of the polychaetes Nereis virens and Playnereis dumerilii (Annelida, Lophotrochozoa). Dev. Genes Evol. 217, 39-54.
74. Kulakova, M.A., Cook, C.E., Andreeva, T.F. 2008. ParaHox gene expression in larval and postlarval development of the polychaete Nereis virens (Annelida, Lophotrochozoa). BMC Dev. Biol. 8, Article 61.
75. Leptin, M. 1991. Twist and snail as positive and negative regulators during Drosophila mesoderm development. Genes Dev. 5, 1568-1576.
76. Lespinet, O., Nederbragt, A.J., Cassan, M., Dictus, W.J., van Loon, A.E., Adoutte, A. 2002. Characterization of two snail genes in the gastropod mollusk Patella vulgata. Implications for understanding the ancestral function of snail related genes in Bilateria. Dev. Genes Evol. 212, 186-195.
77. Li, B., Bisgaard, H.C., Forbes, V.E. 2004. Identification and expression of two novel cytochome P450 genes, belonging to CYP4 and a new CYP331 family, in the polychaete Capitella capitata sp. I. Biochem. Biophys. Res. Com. 325, 510-517.
78. Lui, P.Z., Kaufman, T.C. 2005. Even-skipped is not a pair -rule gene but has segmental and gap-like functions in Oncopeltus fasciatus, an intermediate germband insect. Development 1323, 2081-2092.
79. Martindale, M.Q., Pang, K., Finnerty, J.R. 2004. Investigating the origins of triploblasty: " mesodermal " gene expression in a diploblastic animal, the sea anemone Nematostella vectensis (phylum, Cnidaria; class, Anthozoa). Development 131, 2463-2474.
80. Neilson, C., Nørrevang, A. 1985. The Trochaea theory: an example life cycle phylogeny. In The Origins and Relationships of Lower Invertebrates, edited by S. Conway Morris, D. George, R. Gibson, H.M. Platt. Oxford: Clarendon Press, pp. 28-41.
81. Patel, N.H. 2003. The ancestry of segmentation. Dev. Cell. 5, 2-4.
82. Peterson, K.J., Cameron, R.A., Davidson, E.H. 1997. Set-aside cells in maximal indirect development: Evolutionary and developmental significance. Bioessays 19, 623-631.
83. Petraitis, P.S. 1985. Digametic sex determination in the marine polychaete, Capitella capitata (species type I). Heredity 55, 151-156.
84. Petraitis, P.S. 1988. Occurrence and reproductive success of feminized males in the polychaete Capitella capitata (species type I). Mar. Biol. 97, 403-412.
85. Petraitis, P.S. 1991. The effects of sex ratio and density on the expression of gender in the polychaete Capitella capitata. Evol. Ecol. 5, 393-404.
86. Pinnell, J., Lindeman, P.S., Colavito, S., Lowe, C., Savage, R.M. 2006. The divergent roles of the segmentation gene hunchback. Integr. Comp. Biol. 46, 519-532.
87. Prud' Homme, B., de Rosa, R., Arendt, D., Julien, J.-F., Pajaziti, R., Dorresteijn, A.W.C., Adoutte, A., Wittbrodt, J., Balavoine, G. 2003. Arthropod-like expression patterns of engrailed and wingless in the annelid Platynereis dumerilii suggest a role in segment formation. Curr. Biol. 13, 1876-1881.
88. Rebscher, N., Zelada-Gonzáles, F., Banisch, T.U., Raible, F., Arendt, D. 2007. Vasa unveils a common origin of germ cells and of somatic stem cells from the posterior growth zone in the polychaete Platynereis dumerilii. Dev. Biol. 306, 599-611.
89. Reiger, R.M., Purschke, G. 2005. The coelom and origin of the annelid body plan. Hydrobiologia 535/536, 127-138.
90. Rhode, B. 1993. Laval and adult eyes in Capitella spec. I (Annelida, Polychaeta). J. Morph. 217, 327-335.
91. de Rosa, R., Prud' Homme, B., Balavoine, G. 2005. caudal and even-skipped in the annelid Platyneries dumerilii and the ancestry of posterior growth. Evol. Dev. 7, 574-587.
92. Rouse, G.W. 1999. Trochophore concepts: ciliary bands and the evolution of larvae in spiralian metazoans. Biol. J. Linn. Soc. 66, 411-464.
93. Rouse, G.W. 2000a. Bias? What bias? Gain and loss of downstream larval-feeding in animals. Zool. Scr. 29, 213-236.
94. Rouse, G.W. 2000b. The epitome of hand waving? Larval feeding and the hypotheses of metazoan phylogeny. Evol. Dev. 2, 222-223.
95. Rousset, V., Pleijel, F., Rouse, G.W., Erséus, C., Siddall, M.E. 2007. A molecular phylogeny of annelids. Cladistics 23, 41-63.
96. Sanders, H.L., Grassle, J.F., Hampson, G.R., Morse, L. S., Garner-Price, S., Jones, C.C. 1980. Anatomy of an oil spill: Long term effects from the grounding of the barge Florida offWest Falmouth, Massachusetts. J. Mar. Res. 38: 265-380.
97. Savage, R.M., Shankland, M. 1996. Identification and characterization of a hunchback orthologue, Lzf2, and its expression during leech embryogenesis. Dev. Biol. 175, 205-217.
98. Schoppmeier, M., Damen, W.G. 2005. Suppressor of Hairless and Presenlin phenotypes imply involvement of canonical Notch-signaling in segmentation of the spider Cupiennius salie. Dev. Biol. 280, 211-224.
99. Seaver, E.C., Kaneshige, L.M. 2006. Expression of " segmentation " genes during larval and juvenile development in the polychaetes Capitella sp. I and H. elegans. Dev. Biol. 289, 179-194.
100. Seaver, E.C., Paulson, D.A., Irvine, S.Q., Martindale, M.Q. 2001. The spatial and temporal expression of Ch-en, the engrailed gene in the polychaete Chaetopterus, does not support a role in body axis segmentation. Dev. Biol. 236, 195-209.
101. Seaver, E.C., Thamm, K., Hill, S.D. 2005. Growth patterns during segmentation in the two polychaete annelids, Capitella sp. I and Hydroides elegans: comparisons at distinct life history stages. Evol. Dev. 7, 312-326.
102. Shain, D.H., Ramirez-Webe, F.A., Hsu, J., Weisblat, D.A. 1998. Gangliogenesis in leech: morphogenetic processes leading to segmentation in the central nervous system. Dev. Genes Evol. 208, 28-36.
103. Shi, S., Stanley, P. 2006. Evolutionary origins of Notch signaling in early development. Cell Cycle 5, 274-278.
104. Shimizu, T., Savage, R.M. 2002. Expression of hunchback protein in a subset of ectodermal teloblasts of the oligochaete annelid Tubifex. Dev. Genes Evol. 212, 520-525.
105. Sokol, N.S., Ambros, V. 2005. Mesodermally expressed Drosophila microRNA-1 is regulated by Twist and is required in muscles during larval growth. Genes Dev. 19, 2343-2354.
106. Song, M.H., Huang, F.Z., Gonsalves, F.C., Weisblat, D.A. 2004. Cell cycle-dependent expression of a hairy and Enhancer of split (hes) homolog during cleavage and segmentation in leech embryos. Dev. Biol. 269, 183-195.
107. Struck, T.H., Schult, N., Kusen, T., Hickman, E., Bleidorn, C., McHugh, D., Halanych, K.M. 2007. Annelid phylogeny and the status of Sipuncula and Echiura. BMC Evol. Biol. 7, Article 57.
108. Technau, U., Scholz, C.B. 2003. Origin and evolution of endoderm and mesoderm. Int. J. Dev. Biol. 47, 531-539.
109. Tessmar-Raible, K., Arendt, D. 2003. Emerging systems: between vertebrates and arthropods, the Lophotrochozoa. Curr. Opin. Genet. Dev. 13, 331-340.
110. Thamm, K., Seaver, E.C. 2008. Notch signaling during larval and juvenile development in the polychaete annelid Capitella sp. I. Dev. Biol. 320, 304-318.
111. Thisse, B., Stoetzel, C., Gorostiza-Thisse, C., Perrin-Schmitt, F. 1988. Sequence of the twist gene and nuclear localization of its protein in endomesodermal cells of early Drosophila embryos. EMBO J. 7, 2175-2183.
112. Tomassetti, P., Porrello, S. 2005. Polychaetes as indicators of marine fish farm organic enrichment. Aquac. Int. 13, 109-128.
113. Tsutsumi, H. 1990. Population persistence of Capitella sp. (Polychaeta, Capitellidae) on a mud flat subject to environmental disturbance by organic enrichment. Mar. Ecol. Prog. Ser. 63, 147-156.
114. Wedeen, C.J., Weisblat, D.A. 1991. Segmental expression of an engrailed-class gene during early development and neurogenesis in an annelid. Development 113, 805-814.
115. Werbrock, A.H., Meiklejohn, D.A., Sainz, A., Iwasa, J.H., Savage, R.M. 2001. A polychaete hunchback ortholog. Dev. Biol. 235, 476-488.
116. Wlodarska-Kowalczuk, M., Szymelfenig, M., Zajaczkowski, M. 2007. Dynamic sedentary environments of an Arctic glacier-fed river estuary (Adventfjorden, Svalbard). II: Meio-and macrobenthis fauna. Estuar. Coast. Shelf Sci. 74, 274-284.
117. Yasui, K., Zhang, S.C., Uemura, M., Aizawa, S., Ueki, T. 1998. Expression of a twist-related gene, Bbtwist, during the development of a lancelet species and its relation to cephalochordate anterior structures. Dev. Biol. 195, 49-50.
118. Yokoyama, H. 2002. Impact of fish and pearl farming on the benthic environments in Gokasho Bay: Evaluation from seasonal fluctuations of the macrobenthos. Fish. Sci. 68, 258-268.