Evolutionary developmental biology has focused almost exclusively on multicellular organisms, but there are other relevant levels of biological organization that have remained largely neglected. Animal colonies are made up of multiple physiologically integrated and genetically identical units called zooids that are each homologous to solitary, free-living animals. Siphonophores, a group of pelagic hydrozoans (Cnidaria), have the most complex colony-level organization of all animals. Here the colony-level development of five siphonophore species, strategically sampled across the siphonophore phylogeny, is described from specimens collected using deep-sea submersibles and by self-contained underwater breathing apparatus diving. These species include three cystonects, Bathyphysa sibogae, Rhizophysa filiformis, and Rhizophysa eysenhardti, and two “physonects”, Agalma elegans and Nanomia bijuga. These data, together with previous findings, are analyzed in a phylogenetic framework to reconstruct key features of the history of colony-level organization and development in the Siphonophora. It is shown that gonodendra and gastrozooids of the examined cystonects arise as independent buds directly on the stem, whereas probud subdivision (the origin of feeding, reproductive, and other zooids from a single bud) is a synapomorphy of the Codonophora. The origin of probud subdivision is associated with the origin of cormidia as integrated units of colony organization, and may have allowed for greater morphological and ecological diversification in the Codonophora relative to the Cystonectae. It is also found that symmetry is labile in siphonophores, with multiple gains and/or losses of directional asymmetry in the group. This descriptive work will enable future mechanistic and molecular studies of colony-level development in the siphonophores.
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This work was supported by a mini-PEET grant from the Society for Systematic Biology, a National Science Foundation Graduate Research Fellowship, and a National Science Foundation (NSF) doctoral dissertation improvement grant (DEB-0408014). Thanks to S.H.D. Haddock, J. Godfrey, L. Madin, C. Sardet, and C. Carré for their assistance with collecting siphonophores. E. Edwards provided valuable comments on the text. Special thanks to P. Pugh for making his specimens available for this work, for providing feedback on the manuscript, for checking some of the observations presented here, and, in particular, for our many illuminating conversations.
Communicated by M. Q. Martindale
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Dunn, C.W., Wagner, G.P. The evolution of colony-level development in the Siphonophora (Cnidaria:Hydrozoa). Dev Genes Evol 216, 743–754 (2006). https://doi.org/10.1007/s00427-006-0101-8
- Major transition in evolution
- Asexual reproduction
- Animal colonies
- Division of labor
- Functional specialization