Evolution and dynamics of branching colonial form in marine modular cnidarians: gorgonian octocorals
Cite this article as: Sánchez, J.A. Hydrobiologia (2004) 530: 283. doi:10.1007/s10750-004-2684-2 Abstract
Multi-branched arborescent networks are common patterns for many sessile marine modular organisms but no clear understanding of their development is yet available. This paper reviews new findings in the theoretical and comparative biology of branching modular organisms (e.g. Octocorallia Cnidaria) and new hypotheses on the evolution of form are discussed. A particular characteristic of branching Caribbean gorgonian octocorals is a morphologic integration at two levels of colonial organization based on whether the traits are at the module or colony level. This revealed an emergent level of integration and modularity produced by the branching process itself and not entirely by the module replication. In essence, not just a few changes at the module level could generate changes in colony architecture, suggesting uncoupled developmental patterning for the polyp and branch level traits. Therefore, the evolution of colony form in octocorals seems to be related to the changes affecting the process of branching. Branching in these organisms is sub-apical, coming from mother branches, and the highly self-organized form is the product of a dynamic process maintaining a constant ratio between mother and daughter branches. Colony growth preserves shape but is a logistic growth-like event due to branch interference and/or allometry. The qualitative branching patterns in octocorals (e.g. sea feathers, fans, sausages, and candelabra) occurred multiple times when compared with recent molecular phylogenies, suggesting independence of common ancestry to achieve these forms. A number of species with different colony forms, particularly alternate species (e.g. sea candelabrum), shared the same value for an important branching parameter (the ratio of mother to total branches). According to the way gorgonians branch and achieve form, it is hypothesized that the diversity of alternate species sharing the same narrow variance in that critical parameter for growth might be the product of canalization (or a developmental constraint), where uniform change in growth rates and maximum colony size might explain colony differences among species. If the parameter preserving shape in the colonies is fixed but colonies differ in their growth rates and maximum sizes, heterochrony could be responsible for the evolution among some gorgonian corals with alternate branching.
Keywords colonial organisms heterochrony Cnidaria References Ackerly, D. D., Donoghue, M. J. 1998 Leaf size, sapling allometry, and Corner’s rules: phylogeny and correlated evolution in Maples (Acer) American Naturalist 752 767 791 Google Scholar Aerne, B. L., Groger, H., Schuchert, P., Spring, J., Schmid, V. 1996 The polyp and its medusa: a molecular approach Scientia Marina 60 7 16 Google Scholar Bayer, F. M. 1953 Zoogeography and evolution in the octocorallian family Gorgoniidae Bulletin of Marine Science of the Gulf and Caribbean 3 100 119 Google Scholar Bayer, F. M. 1973 Colonial organization in Octocorals Boardman, R. S. Cheetham, A. H. Oliver, W. A. eds. Animal Colonies, Development and Function through Time. Dowden Hutchinson & Ross Stroudsburg 69 93 Google Scholar Bayer, F. M., Muzik, K. M. 1976 A new solitary octocoral, Taiaroa tauhou gen. et sp. nov. (Coelenterata: Protoalcyonaria) from New Zealand Journal of the Royal Society of New Zealand 6 499 515 Google Scholar Bayer, F. M., Grasshoff, M., Verseveldt, J. 1983An Illustrated Trilingual Glossary of Morphological and Anatomical Terms Applied to Octocorallia E. J. Brill Leiden, The Netherlands Google Scholar Berntson, E. A., Bayer, F. M., McArthur, A. G., France, S. C. 2001 Phylogenetic relationships within the Octocorallia (Cnidaria: Anthozoa) based on nuclear 18S rRNA sequences Marine Biology 138 235 246 CrossRef Google Scholar Blackstone, N. W. 1999 Redox control in development and evolution: evidence from colonial hydroids Journal of Experimental Biology 202 3541 3553 PubMed Google Scholar Blackstone, N. W. 2000 Redox control and the evolution of multicellularity BioEssays 22 947 953 CrossRef PubMed Google Scholar Blackstone, N. W., Buss, L. 1993 Experimental heterochrony in hydractinid hydroids: why mechanisms matter Journal of Evolutionary Biology 6 307 327 CrossRef Google Scholar Buss, L. W. 2001 Growth by intussusception in Hydractiniid hydroids Jackson, J. B. C. Lidgard, S. McKinney, F. K. eds. Evolutionary Patterns: Growth, Form, and Tempo in the Fossil Record University of Chicago Press Chicago 3 26 Google Scholar Cartwright, P., Buss, L. W. 1999 Colony integration and the expression of the Hox gene, Cnox-2, in Hydractinia symbiologicarpus (Cnidaria: Hydrozoa) Journal of Experimental Zoology 285 57 62 CrossRef PubMed Google Scholar Cartwright, P., Bowsher, J., Buss, L. W. 1999 Expression of a Hox gene, Cnox-2, and the division of labor in a colonial hydroid Proceedings of the National Academy of Sciences of the USA 96 2183 2186 CrossRef PubMed Google Scholar Coma, R., Ribes, M., Zabala, M., Gili, J. -M. 1998 Growth in a modular colonial marine invertebrate Estuarine and Coastal Shelf Science 47 459 470 Google Scholar Debat, V., David, P. 2001 Mapping phenotypes: canalization, plasticity and developmental stability Trends in Ecology and Evolution 16 555 561 CrossRef Google Scholar Finnerty, J. R., Martindale, M. Q. 1997 Homeoboxes in sea anemones (Cnidaria: Anthozoa): a PCR-based survey of Nematostella vectensis and Metridium senile Biological Bulletin 193 62 76 PubMed Google Scholar France, S. C., Rosel, P. E., Agenbroad, J. E., Mullineaux, L. S., Kocher, T. D. 1996 DNA sequence variation of mitochondrial large-subunit rRNA provides support for a two-subclass organization of the Anthozoa (Cnidaria) Molecular Marine Biology and Biotechnology 5 15 28 PubMed Google Scholar Gould, S. J. 1977Ontogeny and Phylogeny Belknap Press Cambridge Google Scholar Hughes, R. N. 1983 Evolutionary ecology of colonial reef-organisms, with particular reference to corals Biological Journal of the Linnaean Society 20 39 58 Google Scholar Jackson, J. B. C. 1977 Competition on marine hard substrata: the adaptive significance of solitary and colonial strategies American Naturalist 111 743 767 CrossRef Google Scholar Kaandorp, J. A., Kübler, J. 2001The Algorithmic Beauty of Seaweeds, Sponges and Corals Springer-Verlag Amsterdam Google Scholar Kapela, W., Lasker, H. R. 1999 Size-dependent reproduction in the Caribbean gorgonian Pseudoplexaura porosa Marine Biology 135 107 114 CrossRef Google Scholar Kaufmann, K. W. 1981 Fitting and using growth curves Oecologia 49 293 299 CrossRef Google Scholar Kossevitch, I. A., Herrmann, K., Berking, S. 2001 Shaping of colony elements in Laomedea flexuosa Hinks (Hydrozoa, Thecaphora) includes a temporal and spatial control of skeleton hardening Biological Bulletin 201 417 423 PubMed Google Scholar Kuhn, K., Streit, B., Schierwater, B. 1999 Isolation of Hox genes from the Scyphozoan Cassiopeia xamachana: implications for the early evolution of Hox genes Journal of Experimental Zoology 285 63 75 CrossRef PubMed Google Scholar Lasker, H. R., Sánchez, J. A. 2002 Allometry and Astogeny of modular organisms Hughes, R. N. eds. Reproductive Biology of Invertebrates, Vol. XI. Progress in Asexual Reproduction John Wiley New York 207 253 Google Scholar
Lasker, H. R., M. L. Boller, J. Castanaro & J. A Sánchez, 2004. Modularity and determinate growth in a gorgonian coral. Biological Bulletin.
Lewontin, R. C. 1966 On the measurement of relative variability Systematic Zoology 15 141 142 Google Scholar McKinney, F. K., Raup, D. M. 1982 A turn in the right direction: simulation of erect spiral growth in the bryozoans Arquimedes and Bugula Paleobiology 8 101 112 Google Scholar McKinney, M. L. 1988 Classifying heterochrony allometry, size, and time McKinney, M. L. eds. Heterochrony in Evolution. A Multidisciplinary Approach Plenum Press New York 17 34 Google Scholar McNamara, K.J. 1995Evolutionary Change and Heterochrony John Wiley & Sons New York Google Scholar Müller, W. A., Hauch, A., Plickert, G. 1987 Morphogenetic factors in hydroids. I. Stolon tip activation and inhibition Journal of Experimental Zoology 243 111 124 Google Scholar Pandolfi, J. M. 1988 Heterochrony in colonial marine animals McKinney, M. L. eds. Heterochrony in Evolution. A Multidisciplinary Approach Plenum Press New York 135 158 Google Scholar Pigliucci, M., Marlow, E. T. 2001 Differentiation for flowering time and phenotypic integration in Arabidopsis thaliana in response to season length and vernalization Oecologia 127 501 508 CrossRef Google Scholar Popadic, A., Abzhanov, A., Ruch, D., Kaufman, T. C. 1998 Understanding the genetic basis of morphological evolution: the role of homeotic genes in the diversification of the arthropod bauplan International Journal of Developmental Biology 42 453 461 PubMed Google Scholar Purugganan, M. D. 1999 The molecular evolution of development BioEssays 29 700 711 Google Scholar Resnik, D. 1995 Developmental constraints and patterns: some pertinent distinctions Journal of Theoretical Biology 173 231 240 CrossRef Google Scholar Rice, S. H. 1997 The analysis of ontogenetic trajectories: when a change in size or shape is not heterochrony Proceedings of the National Academy of Sciences of the USA 94 907 912 PubMed Google Scholar Rinkevich, B. 2002 The branching coral Stylophora pistillata: contribution of genetics in shaping colony landscape Israel Journal of Zoology 48 71 82 Google Scholar Sánchez, J. A. 2002Dynamics and evolution of colony form among branching modular organisms Ph.D. Thesis University at Buffalo (The State University of New York) Buffalo (USA) Google Scholar Sánchez, J. A., Lasker, H. R. 2004 Do multi-branched colonial organisms exceed normal growth after partial mortality Proceedings of the Royal Society of London series B-Biological Sciences (supplement) 271 S117 120 Google Scholar Sánchez, J. A., Lasker, H. R. 2003 Patterns of morphologic integration in branching colonies of marine modular organisms: supra-module organization in gorgonian corals Proceedings of the Royal Society of London series B-Biological Sciences 270 2039 2044 Google Scholar Sánchez, J. A., Lasker, H. R., Taylor, D. J. 2003a Phylogenetic analyses among octocorals (Cnidaria) according to mitochondrial and nuclear DNA sequences (lsu-rRNA 16S, and ssu-rRNA 18S) support two convergent clades of branching gorgonians Molecular Phylogenetics Evolution 29 31 42 Google Scholar Sánchez, J. A., Mcfadden, C. S., France, S. C., Lasker, R. 2003b Molecular phylogenetic analyses of shallow-water Caribbean octocorals Marine Biology 142 975 987 Google Scholar Sánchez, J. A., Zeng, W., Coluci, V. R., Simpson, C., Lasker, R. 2003c How similar are branching networks in natureA view from the ocean: caribbean gorgonian corals Journal of Theoretical Biology 222 135 138 Google Scholar Sánchez, J. A., Lasker, H. R., Nepomuceno, E. G., Sánchez, J. D., Woldenberg, M. J. 2004 Branching and self-organization in marine modular colonial organisms: a model American Naturalist 163 E24 39 PubMed Google Scholar Stebbing, A. R. D. 1981 The kinetics of growth control in a colonial hydroid Journal of the Marine Biological Association of the United Kingdom 61 35 63 CrossRef Google Scholar Waitt, D. E., Levin, D. A. 1993 Phenotypic integration and plastic correlations in Phlox drummondii (Polomoniaceae) American Journal of Botany 80 1224 1233 Google Scholar Copyright information
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