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Field fitness, phalanx-guerrilla morphological variation, and symmetry of colonial growth in the encrusting hydroid genus Hydractinia

Published online by Cambridge University Press:  18 December 2008

David L. Ferrell
David L. Ferrell*
Affiliation:
Department of Biological Science, Florida State University, Tallahassee, FL 32306-1100, USA
*
Correspondence should be addressed to: David L. Ferrell, Department of Biological Science, Florida State University, Tallahassee, FL 32306-1100, USA email: ferrell@bio.fsu.edu
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Abstract

‘Phalanx’ and ‘guerrilla’ phenotypes have been characterized as distinct, adaptive growth strategies exhibited by marine encrusting taxa, as well as a variety of other colonial taxa, that differ in patterns of colonial growth and areal expansion. Phalanx morphs exhibit compact growth, expanding outward concentrically and generating radially symmetric colony shapes, whereas guerrillas exhibit diffuse growth and typically elongate, asymmetric colony shapes. Several species in the colonial hydroid genus Hydractinia display inter-genotypic morphological variation in early developmental growth, although it is unclear if and how this growth form variation is tied to colony symmetry. Here I show that the phalanx versus guerrilla distinction does not adequately characterize genetic variation in Hydractinia growth form. Genotypes characterized by extreme mat and stoloniferous growth exhibited high levels of symmetry while genotypes generating growth forms intermediate between these two extremes were more asymmetric. Asymmetric growth is tied to reduced field fitness as a result of slower growth, reduced investment in future reproduction, and increased susceptibility to abiotic environmental stress. Asymmetric, guerrilla-like growth may be the morphological symptom of maladaptive growth early in colony development. This notion contrasts greatly with the traditional view of guerrilla growth as an adaptive strategy. Several hypotheses are proposed to address why asymmetric, guerrilla-like growth may be maladaptive in this and similar systems.

Keywords

competitive abilitydevelopmental instabilityfield experimentgenotypehermit crablife historyshell
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 88 , Special Issue 8: Hydrozoans , December 2008 , pp. 1577 - 1587
Copyright
Copyright © Marine Biological Association of the United Kingdom 2008

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References

REFERENCES

Ballard, W.W. (1942) The mechanism of synchronous spawning in Hydractinia and Pennaria. Biological Bulletin. Marine Biological Laboratory, Woods Hole 82, 329–339.Google Scholar
Blackstone, N.W., Bivins, M.J., Cherry, K.S., Fletcher, R.E. and Geddes, G.C. (2005) Redox signaling in colonial hydroids: many pathways for peroxide. Journal of Experimental Biology 208, 383–390.Google Scholar
Blackstone, N.W. and Buss, L.W. (1991) Shape variation in hydractiniid hydroids. Biological Bulletin. Marine Biological Laboratory, Woods Hole 180, 394–405.Google Scholar
Blackstone, N.W. and Buss, L.W. (1992) Treatment with 2,3-dinitrophenol mimics ontogenetic and phylogenetic changes in a hydractiniid hydroid. Proceedings of the National Academy of Sciences of the United States of America 89, 4057–4061.Google Scholar
Blackstone, N.W. and Buss, L.W. (1993) Experimental heterochrony in hydractiniid hydroids: why mechanisms matter. Journal of Evolutionary Biology 6, 307–327.CrossRefGoogle Scholar
Blackstone, N.W., Cherry, K.S. and Glockling, S.L. (2004a) Structure and signaling in polyps of a colonial hydroid. Invertebrate Biology 123, 43–53.CrossRefGoogle Scholar
Blackstone, N.W., Cherry, K.S. and Van Winkle, D.H. (2004b) The role of polyp-stolon junctions in the redox signaling of colonial hydroids. Hydrobiologia 530/531, 291–298.Google Scholar
Bouillon, J., Gravili, C., Pagès, F., Gili, J.P. and Boero, F. (2006) An introduction to Hydrozoa. Paris: Publications Scientifiques du Muséum.Google Scholar
Brown, B.E., Dunne, R.P., Scoffin, T.P. and Le Tissier, M.D.A. (1994) Solar damage in intertidal corals. Marine Ecology Progress Series 105, 219–230.Google Scholar
Bunting, M. (1894) The origin of sex cells in Hydractinia and Podocoryne and the development of Hydractinia. Journal of Morphology 9, 203–246.Google Scholar
Buss, L.W. (1979) Habitat selection, directional growth and spatial refuges: why colonial animals have more hiding places. In Larwood, G. and Rosen, B. (eds) Biology and systematics of colonial organisms. London: Academic Press, pp. 459–497.Google Scholar
Buss, L.W. and Blackstone, N.W. (1991) An exploration of Waddington's epigenetic landscape. Philosophical Transactions of the Royal Society B 332, 49–58.Google Scholar
Buss, L.W. and Grosberg, R.K. (1990) Morphogenetic basis for phenotypic differences in hydroid competitive behavior. Nature 343, 63–66.Google Scholar
Buss, L.W., McFadden, C.S. and Keene, D.R. (1984) Biology of Hydractiniid hydroids. 2. Histocompatibility effector system/competitive mechanism mediated by nematocyst discharge. Biological Bulletin. Marine Biological Laboratory, Woods Hole 167, 139–158.Google Scholar
Buss, L.W. and Yund, P.O. (1988) A comparison of recent and historical populations of the colonial hydroid Hydractinia. Ecology 69, 646–654.CrossRefGoogle Scholar
Buss, L.W. and Yund, P.O. (1989) A sibling species of Hydractinia in the north-eastern United States. Journal of the Marine Biological Association of the United Kingdom 69, 857–874.Google Scholar
Cunningham, C.W., Buss, L.W. and Anderson, C. (1991) Molecular and geologic evidence of shared history between hermit crabs and the symbiotic genus Hydractinia. Evolution 45, 1301–1316.Google Scholar
Dudgeon, S.R. and Buss, L.W. (1996) Growing with the flow: on the maintenance and malleability of colony form in the hydroid Hydractinia. American Naturalist 147, 667–691.Google Scholar
Ferrell, D.L. (2004a) Fitness consequences of allorecognition-mediated agonistic interactions in the colonial hydroid Hydractinia GM. Biological Bulletin. Marine Biological Laboratory, Woods Hole 206, 173–187.Google Scholar
Ferrell, D.L. (2004b) Gastropod shell size and morphology influence conspecific interactions in an encrusting hydroid. Marine Ecology Progress Series 275, 153–162.CrossRefGoogle Scholar
Ferrell, D.L. (2005) Competitive equivalence maintains persistent inter-clonal boundaries. Oecologia 142, 184–190.Google Scholar
Folino, N.C. and Yund, P.O. (1998) The distribution of hydroid sibling species on hermit crabs in estuaries in the Gulf of Maine. Estuaries 21, 829–836.CrossRefGoogle Scholar
Frank, U., Leitz, T. and Müller, W.A. (2001) The hydroid Hydractinia: a versatile, informative cnidarian representative. BioEssays 23, 963–971.Google Scholar
Hart, M.W. and Grosberg, R.K. (1999) Kin interactions in a colonial hydrozoan (Hydractinia symbiolongicarpus): population structure on a mobile landscape. Evolution 53, 793–805.Google Scholar
Hoffmann, A.A., Woods, R.E., Collins, E., Wallin, K., White, A. and McKenzie, J.A. (2005) Wing shape versus asymmetry as an indicator of changing environmental conditions in insects. Australian Journal of Entomology 44, 233–243.Google Scholar
Ivker, F.S. (1972) A hierarchy of histo-compatibility in Hydractinia echinata. Biological Bulletin. Marine Biological Laboratory, Woods Hole 143, 162–174.Google Scholar
Jackson, J.B.C. (1977) Competition on marine hard substrata: the adaptive significance of solitary and colonial strategies. American Naturalist 111, 743–768.CrossRefGoogle Scholar
Jackson, J.B.C. (1979a) Morphological strategies of sessile animals. In Larwood, G. and Rosen, B. (eds) Biology and systematics of colonial organisms. London: Academic Press, pp. 499–556.Google Scholar
Jackson, J.B.C. (1979b) Overgrowth competition between encrusting cheilostome ectoprocts in a Jamaican cryptic reef environment. Journal of Animal Ecology 48, 805–823.Google Scholar
Karlson, R.H. (1980) Alternative competitive strategies in a periodically disturbed habitat. Bulletin of Marine Science 30, 894–900.Google Scholar
Levitan, D.L. and Grosberg, R.K. (1993) The analysis of paternity and maternity in the marine hydrozoan Hydractinia symbiolongicarpus using randomly amplified polymorphic DNA (RAPD) markers. Molecular Ecology 2, 315–326.CrossRefGoogle ScholarPubMed
McFadden, C.S., McFarland, M.J. and Buss, L.W. (1984) Biology of hydractiniid hydroids. 1. Colony ontogeny in Hydractinia echinata (Flemming). Biological Bulletin. Marine Biological Laboratory, Woods Hole 166, 54–67.Google Scholar
Møller, A.P. (1997) Developmental stability and fitness: a review. American Naturalist 149, 916–932.Google Scholar
Polak, M. (2003) Developmental instability. New York: Oxford University Press.Google Scholar
Sebens, K.P. (1986) Spatial relationship among encrusting marine organisms in the New England subtidal zone. Ecological Monographs 56, 73–96.Google Scholar
Sokal, R.R. and Rohlf, F.J. (1995) Biometry, 3rd edn.New York: W.H. Freeman.Google Scholar
Sutherland, J.P. and Karlson, R.H. (1977) Development and stability of fouling community at Beaufort, North Carolina. Ecological Monographs 47, 425–446.CrossRefGoogle Scholar
Sutherland, W.J. and Stillman, R.A. (1988) The foraging tactics of plants. Oikos 52, 239–244.Google Scholar
Van Winkle, D.H. and Blackstone, N.W. (2002) Variation in growth and competitive ability between sexually and clonally produced hydroids. Biological Bulletin. Marine Biological Laboratory, Woods Hole 202, 156–165.CrossRefGoogle ScholarPubMed
Van Winkle, D.H., Longnecker, K. and Blackstone, N.W. (2000) The effects of hermit crabs on hydractiniid hydroids. Marine Ecology 21, 55–67.CrossRefGoogle Scholar
Wood-Jones, F. (1907) On the growth forms and supposed species in corals. Proceedings of the Zoological Society of London 1907, 518–556.Google Scholar
Yund, P.O. (1987) Intraspecific competition and the maintenance of morphological variation in the colonial hydroid Hydractinia symbioacadianus. PhD thesis, Yale University, New Haven, CT, USA.Google Scholar
Yund, P.O. (1991) Natural selection on hydroid colony morphology by intraspecific competition. Evolution 45, 1564–1573.Google Scholar
Yund, P.O., Cunningham, C.W. and Buss, L.W. (1987) Recruitment and postrecruitment interactions in a colonial hydroid. Ecology 68, 971–982.CrossRefGoogle Scholar
Yund, P.O. and Parker, H.M. (1989) Population structure of the colonial hydroid Hydractinia sp. nov. C in the Gulf of Maine. Journal of Experimental Marine Biology and Ecology 125, 63–82.Google Scholar