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Division of labor and recurrent evolution of polymorphisms in a group of colonial animals

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Abstract

Rendering developmental and ecological processes into macroevolutionary events and trends has proved to be a difficult undertaking, not least because processes and outcomes occur at different scales. Here we attempt to integrate comparative analyses that bear on this problem, drawing from a system that has seldom been used in this way: the co-occurrence of alternate phenotypes within genetic individuals, and repeated evolution of distinct categories of these phenotypes. In cheilostome bryozoans, zooid polymorphs (avicularia) and some skeletal structures (several frontal shield types and brood chambers) that evolved from polymorphs have arisen convergently at different times in evolutionary history, apparently reflecting evolvability inherent in modular organization of their colonial bodies. We suggest that division of labor evident in the morphology and functional capacity of polymorphs and other structural modules likely evolved, at least in part, in response to the persistent, diffuse selective influence of predation by small motile invertebrate epibionts.

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References

  • Barthélémy D, Caraglio Y (2007) Plant architecture: a dynamic, multilevel and comprehensive approach to plant form, structure and ontogeny. Ann Bot 99:375–407

    Article  PubMed  Google Scholar 

  • Beklemishev WN (1969) Principles of comparative anatomy of invertebrates, vol 1. Oliver and Boyd, Edinburgh

    Google Scholar 

  • Berning B (2008) Evidence for sublethal predation and regeneration among living and fossil ascophoran bryozoans. In: Hageman SJ, Key MMJ Jr, Winston JE (eds) Bryozoan studies 2007, Virginia Museum of Natural History Special Publication 15. Virginia Museum of Natural History, Martinsville, pp 1–5

    Google Scholar 

  • Best MA, Thorpe JP (1985) Autoradiographic study of feeding and the colonial transport of metabolites in the marine bryozoan Membranipora membranacea. Mar Biol 84:295–300

    Article  Google Scholar 

  • Best MA, Thorpe JP (2002) Use of radioactive labelled food to assess the role of the funicular system in the transport of metabolites in the cheilostome bryozoan Membranipora membranacea. In: Wyse Jackson PN, Buttler CJ, Spencer Jones ME (eds) Bryozoan studies 2001. Swets & Zeitlinger, Lisse, pp 29–35

    Google Scholar 

  • Best BA, Winston JE (1984) Skeletal strength of encrusting cheilostome bryozoans. Biol Bull 167:390–409

    Article  Google Scholar 

  • Boyce K (2010) The evolution of plant development in a paleontological context. Curr Opin Plant Biol 13:102–107

    Article  PubMed  Google Scholar 

  • Calvet L (1900) Contribution á l’histoire naturelle des Bryozoaires Ectoproctes marins. Travaux de l’Institut de Zoologie de l’Université de Montpellier, NS 8:1–488

    Google Scholar 

  • Carle KJ, Ruppert EE (1983) Comparative ultrastructure of the bryozoan funiculus—a blood-vessel homolog. Zeitschrift fur Zoologische Systematik und Evolutionsforschung 21:181–193

    Article  Google Scholar 

  • Carter MC, Gordon DP, Gardner JPA (2008) A preliminary analysis of avicularian morphology. In: Hageman SJ, Key MM, Winston JE (eds) Bryozoan Studies 2007, Virginia museum of natural history special publication 15. Virginia Museum of Natural History, Martinsville, pp 19–30

  • Carter MC, Gordon DP, Gardner JPA (2010a) Polymorphism and vestigiality: comparative anatomy and morphology of bryozoan avicularia. Zoomorphology 129:195–211

    Article  Google Scholar 

  • Carter MC, Gordon DP, Gardner JPA (2010b) Polymorphism and variation in modular animals: morphometric and density analyses of bryozoan avicularia. Mar Ecol Prog Ser 399:117–130

    Article  Google Scholar 

  • Carter MC, Lidgard S, Gordon DP, Gardner JPA (2011) Functional innovation through vestigialisation in a modular marine invertebrate. Biol J Linn Soc (in press)

  • Cheetham AH, Cook PL (1983) General features of the Class Gymnolaemata. In: Robison RA (ed) Treatise on invertebrate paleontology. University of Kansas and Geological Society of America, Lawrence, pp 138–207

    Google Scholar 

  • Cheetham AH, Jackson JBC, Hayek LAC (1993) Quantitative genetics of bryozoan phenotypic evolution. 1. Rate tests for random change versus selection in differentiation of living species. Evolution 47:1526–1538

    Article  Google Scholar 

  • Cheetham AH, Sanner J, Taylor PD, Ostrovsky AN (2006) Morphological differentiation of avicularia and the proliferation of species in mid-Cretaceous Wilbertopora Cheetham, 1954 (Bryozoa: Cheilostomata). J Paleontol 80:49–71

    Article  Google Scholar 

  • Clarke E (2011) Plant individuality and multilevel selection theory. In: Calcott B, Sterelny K (eds) Major transitions in evolution revisited. MIT Press, Cambridge, pp 227–250

    Google Scholar 

  • Cook PL (1968) Polyzoa from West Africa. The Malacostega. Part 1. Bull British Mus (Nat Hist) Zool 16:116–160

    Google Scholar 

  • Cook PL (1985) Bryozoa from Ghana; a preliminary survey. Koninklijk Museum Voor Midden Afrika Tervuren Belgie Annalen Zoologische Wetenschappen 238:1–315

    Google Scholar 

  • Cunningham CW, Omland KE, Oakley TH (1998) Reconstructing ancestral character states: a critical reappraisal. Trends Ecol Evol 13:361–366

    Article  PubMed  CAS  Google Scholar 

  • Darwin C (1872) On the origin of species by means of natural selection, or the preservation of favoured races in the struggle for life, 6th edn. John Murray, London

    Google Scholar 

  • Davidson B, Jacobs MW, Swalla BJ (2004) The individual as a module: solitary-to-colonial transitions in metazoan evolution and development. In: Schlosser G, Wagner GP (eds) Modularity in development and evolution. University of Chicago Press, Chicago, pp 443–465

    Google Scholar 

  • de Kroon H, Huber H, Stuefer JF, van Groenendael JM (2005) A modular concept of phenotypic plasticity in plants. New Phytol 166:73–82

    Article  PubMed  Google Scholar 

  • Dick MH, Lidgard S, Gordon DP, Mawatari SF (2009) The origin of ascophoran bryozoans was historically contingent but likely. Proc R Soc B 276:3141–3148

    Article  PubMed  Google Scholar 

  • Dick MH, Mawatari SF, Sanner J, Grishenko AV (2011) Cribrimorph and other Cauloramphus species (Bryozoa: Cheilostomata) from the northwestern Pacific. Zool Sci 28:134–147

    Article  PubMed  Google Scholar 

  • Dunn CW (2005) Complex colony-level organization of the deep-sea siphonophore Bargmannia elongata (Cnidaria, Hydrozoa) is directionally asymmetric and arises by the subdivision of pro-buds. Dev Dyn 234:835–845

    Article  PubMed  Google Scholar 

  • Elwick J (2007) Styles of reasoning in the British life sciences: shared assumptions, 1820–1858. Pickering & Chatto, London

    Google Scholar 

  • Fuchs J, Obst M, Sundberg P (2009) The first comprehensive molecular phylogeny of Bryozoa (Ectoprocta) based on combined analyses of nuclear and mitochondrial genes. Mol Phylogenet Evol 52:225–233

    Article  PubMed  CAS  Google Scholar 

  • Gavrilets S, Losos JB (2009) Adaptive radiation: contrasting theory with data. Science 323:732–737

    Article  PubMed  CAS  Google Scholar 

  • Geddes P, Mitchell PC (1911) Morphology. In: Chisholm H (ed) The Encyclopaedia Britannica eleventh edition, vol 18. Cambridge University Press, Cambridge, pp 863–869

  • Gilbert SF, Epel D (2008) Ecological developmental biology: integrating epigenetics, medicine, and evolution. Sinauer, Sunderland

    Google Scholar 

  • Glor RE (2010) Phylogenetic insights on adaptive radiation. Annu Rev Ecol Evol Syst 41:251–270

    Article  Google Scholar 

  • Gordon DP (2000) Towards a phylogeny of cheilostomes—morphological models of frontal wall/shield evolution. In: Herrera Cubilla A, Jackson JBC (eds) Proceedings of the 11th International Bryozoology Association conference. Smithsonian Tropical Research Institution, Balboa, pp 17–37

    Google Scholar 

  • Gordon DP, Voigt E (1996) The kenozooidal origin of the ascophorine hypostegal coelom and associated frontal shield. In: Gordon DP, Smith AM, Grant-Mackie JA (eds) Bryozoans in space and time. National Institute of Water and Atmospheric Research, Wellington, pp 89–107

    Google Scholar 

  • Gordon DP, Clark AG, Harper JF (1987) Bryozoa. In: Pandian TJ, Vernberg FJ (eds) Animal energetics. Academic Press, New York, pp 173–199

    Google Scholar 

  • Grosberg RK, Patterson MR (1989) Review: iterated ontogenies reiterated. Paleobiology 15:67–73

    Google Scholar 

  • Hageman SJ (2003) Complexity generated by iteration of hierarchical modules in Bryozoa. Integr Comp Biol 43:87–98

    Article  PubMed  Google Scholar 

  • Hageman SJ, Bayers MM, Todd CD (1999) Partitioning phenotypic variation: genotypic, environmental and residual components from bryozoan skeletal morphology. J Nat Hist 33:1713–1735

    Article  Google Scholar 

  • Hall BK (2003) Unlocking the black box between genotype and phenotype: cell condensations as morphogenetic (modular) units. Biol Philos 18:219–247

    Article  Google Scholar 

  • Harmer SF (1902) On the morphology of the Cheilostomata. Q J Microsc Sci 46:263–350

    Google Scholar 

  • Harmer SF (1926) The Polyzoa of the Siboga Expedition. II. Cheilostomata Anasca. Rep Siboga Exped 28b:181–501

    Google Scholar 

  • Harvell CD (1984) Predator-induced defense in a marine bryozoan. Science 224:1357–1359

    Article  PubMed  CAS  Google Scholar 

  • Harvell CD (1990) The evolution of inducible defense. Parasitology 100:S53–S61

    Article  PubMed  Google Scholar 

  • Harvell CD (1994) The evolution of polymorphism in colonial invertebrates and social insects. Q Rev Biol 69:155–185

    Article  Google Scholar 

  • Harvell CD (1998) Genetic variation and polymorphism in the inducible spines of a marine bryozoan. Evolution 52:80–86

    Article  Google Scholar 

  • Harvell CD, Grosberg RK (1988) The timing of sexual maturity in clonal animals. Ecology 69:1855–1864

    Article  Google Scholar 

  • Harvell CD, Helling R (1993) Experimental induction of localized reproduction in a marine bryozoan. Biol Bull 184:286–295

    Article  Google Scholar 

  • Hausdorf B, Helmkampf M, Nesnidal MP, Bruchhaus I (2010) Phylogenetic relationships within the lophophorate lineages (Ectoprocta, Brachiopoda and Phoronida). Mol Phylogenet Evol 55:1121–1127

    Article  PubMed  Google Scholar 

  • Herrera CM (2009) Multiplicity in unity: plant subindividual variation and interactions with animals. University of Chicago Press, Chicago

    Google Scholar 

  • Hyman LH (1959) The invertebrates: smaller coelomate groups Chaetognatha, Hemichordata, Pogonophora, Phoronida, Ectoprocta, Brachiopoda, Sipunculida. The coelomate Bilateria, vol V. McGraw-Hill Book Company, Inc, New York

    Google Scholar 

  • Iyengar EV, Harvell CD (2002) Specificity of cues inducing defensive spines in the bryozoan Membranipora membranacea. Mar Ecol Prog Ser 225:205–218

    Article  Google Scholar 

  • Jablonski D (2005) Evolutionary innovations in the fossil record: the intersection of ecology, development, and macroevolution. J Exp Zool Part B Mol Dev Evol 304B:504–519

    Article  Google Scholar 

  • Jablonski D (2007) Scale and hierarchy in macroevolution. Palaeontology 50:87–109

    Article  Google Scholar 

  • Jablonski D (2008) Biotic interactions and macroevolution: extensions and mismatches across scales and levels. Evolution 62:715–739

    Article  PubMed  Google Scholar 

  • Jablonski D, Sepkoski JJ (1996) Paleobiology, community ecology, and scales of ecological pattern. Ecology 77:1367–1378

    Article  PubMed  CAS  Google Scholar 

  • Jackson JBC (1988) Does ecology matter? Review of evolution: an ecological history of life by G. J. Vermeij. Paleobiology 14:307–312

    Google Scholar 

  • Jackson JBC, Erwin DH (2006) What can we learn about ecology and evolution from the fossil record? Trends Ecol Evol 21:322–328

    Article  PubMed  Google Scholar 

  • Jackson JBC, Buss LW, Cook RE (1986) Population biology and evolution of clonal organisms. Yale University Press, New Haven

    Google Scholar 

  • Johnston G (1847) A history of the British zoophytes, vol 2. Van Voorst, London

    Google Scholar 

  • Kalisz S, Kramer EM (2008) Variation and constraint in plant evolution and development. Heredity 100:171–177

    Article  PubMed  CAS  Google Scholar 

  • Karlson R (2002) Population processes in modular benthic invertebrates. In: Hughes RN (ed) Reproductive biology of invertebrates, vol XI. Wiley, Chichester, pp 255–281

    Google Scholar 

  • Kaufmann KW (1968) The biological role of Bugula-type avicularia (Bryozoa). In: Annoscia E (ed) Proceedings of the first international conference on Bryozoa. Società Italiana do Scienze Naturali e del Museo Civico di Storia Naturale di Milano, Milan, pp 173–182

    Google Scholar 

  • Kaufmann KW (1971) The form and functions of the avicularia of Bugula (Phylum Ectoprocta). Postilla 151:1–26

    Google Scholar 

  • Knight S, Gordon DP, Lavery SD (2011) A multi-locus analysis of phylogenetic relationships within cheilostome bryozoans supports multiple origins of ascophoran frontal shields. Mol Phylogenet Evol (in press)

  • Kuklinski P, Taylor PD (2006) A new genus and some cryptic species of Arctic and boreal calloporid cheilostome bryozoans. J Mar Biol Assoc UK 86:1035–1046

    Article  Google Scholar 

  • Larwood GP (1969) Frontal calcification and its function in some Cretaceous and recent cribrimorph and other cheilostome Bryozoa. Bull British Mus (Nat Hist) Zool 18:173–182

    Google Scholar 

  • Larwood GP (1985) Form and evolution of Cretaceous myagromorph Bryozoa. In: Nielsen C, Larwood GP (eds) Bryozoa: ordovician to recent. Olsen & Olsen, Fredensborg, pp 169–174

    Google Scholar 

  • Levinsen GMR (1902) Studies on Bryozoa. Videnskabelige Meddelelser fra Dansk Naturhistorisk Forening i Kjøbenhavn 54:1–32

    Google Scholar 

  • Lidgard S (1985) Zooid and colony growth in encrusting cheilostome bryozoans. Palaeontology 28:255–291

    Google Scholar 

  • Lidgard S (2008a) Predation on marine bryozoan colonies—taxa, traits and trophic groups. Mar Ecol Prog Ser 359:117–131

    Article  Google Scholar 

  • Lidgard S (2008b) How should we consider predation risk in marine bryozoans? In: Hageman SJ, Key MMJ, Winston JE (eds) Bryozoan studies 2007, Special Publication No. 15. Virginia Museum of Natural History, Martinsville, pp 123–131

    Google Scholar 

  • Lindsay SM (2010) Frequency of injury and the ecology of regeneration in marine benthic invertebrates. Integr Comp Biol 50(4):479–493

    Article  PubMed  Google Scholar 

  • Losos JB (2010) Adaptive radiation, ecological opportunity, and evolutionary determinism. Am Nat 175(6):623–639

    Article  PubMed  Google Scholar 

  • Losos JB (2011) Convergence, adaptation, and constraint. Evolution 65:1827–1840

    Article  PubMed  Google Scholar 

  • Lutaud G (1985) Preliminary experiments on interzooidal metabolic transfer in anascan bryozoans. In: Nielsen C, Larwood GP (eds) Bryozoa: Ordovician to Recent. Olsen & Olsen, Fredensborg, pp 183–191

    Google Scholar 

  • Mackie GO (1986) Aggregates to integrates: physiological aspects of modularity in colonial animals. Philos Trans R Soc B-Biol Sci 313:175–196

    Article  Google Scholar 

  • Marcus E (1939) Bryozoaros marinhos Brasileiros. III. Boletim da Faculdade de Filosofia, Ciências e Letras, Universidade de São Paulo, Zoologia 3:111–353

    Google Scholar 

  • McKinney FK, Jackson JBC (1989) Bryozoan evolution. Allen & Unwin, London

    Google Scholar 

  • McKinney FK, Taylor PD, Lidgard S (2003) Predation on bryozoans and its reflection in the fossil record. In: Kelley PH, Kowalewski M, Hansen T (eds) Predator–prey interactions in the fossil record. Klewer Academic/Plenum, New York, pp 239–261

    Chapter  Google Scholar 

  • Miles JS, Harvell CD, Griggs CM, Eisner S (1995) Resource translocation in a marine bryozoan—quantification and visualization of C-14 and S-35. Mar Biol 122(3):439–445

    Article  Google Scholar 

  • Miner BG, Sultan SE, Morgan SG, Padilla DK, Relyea RA (2005) Ecological consequences of phenotypic plasticity. Trends Ecol Evol 20:685–692

    Article  PubMed  Google Scholar 

  • Mukai H, Terakado K, Reed CG (1997) Bryozoa. In: Harrison FW, Woollacott RM (eds) Microscopic anatomy of invertebrates, vol 13: Lophophorates, Entoprocta and Cycliophora. Wiley-Liss, New York, pp 45–206

    Google Scholar 

  • Nordmann A (1840) Recherches microscopiques sur la Cellularia avicularia. In: Voyage dans la Russie méridionale et la Crimee, par la Hongrie, la Valachie et la Moldavie, exécuté en 1837 sous la direction de M Anatole de Demidoff, vol III. Ernest Bourdin, Paris, pp 679–707

    Google Scholar 

  • Nyhart LK, Lidgard S (2011) Individuals at the center of biology: Rudolf Leuckart’s Polymorphismus der Individuen and the ongoing narrative of parts and wholes. With an annotated translation. J Hist Biol 1–71. Online First doi:10.1007/s10739-011-9268-6

  • Okamura B, Freeland JR, Hatton-Ellis T (2002) Clones and metapopulations. In: Hughes RN (ed) Reproductive biology of invertebrates, vol XI. Wiley, Chichester, pp 283–312

    Google Scholar 

  • Osman RW, Whitlatch RB (2004) The control of the development of a marine benthic community by predation on recruits. J Exp Mar Biol Ecol 311:117–145

    Article  Google Scholar 

  • Ostrovsky AN (1998) Comparative studies of ovicell anatomy and reproductive patterns in Cribrilina annulata and Celleporella hyalina (Bryozoa: Cheilostomatida). Acta Zoologica 79:287–318

    Article  Google Scholar 

  • Ostrovsky AN (2008a) Brood chambers in cheilostome Bryozoa: diversity and revised terminology. In: Hageman SJ, Winston JE, Key MMJ (eds) Bryozoan studies 2007, Special Publication No. 15. Virginia Museum of Natural History, Martinsville, pp 193–205

    Google Scholar 

  • Ostrovsky AN (2008b) The parental care in cheilostome bryozoans: a historical review. In: Wyse Jackson PN, Spencer Jones ME (eds) Annals of bryozoology 2: aspects of the history of research on bryozoans. International Bryozoology Association, Dublin, pp 211–245

    Google Scholar 

  • Ostrovsky AN (2009) Evolution of the sexual reproduction in the bryozoan order Cheilostomata (Gymnolaemata). St Petersburg State University [in Russian with English summary]

  • Ostrovsky AN, Taylor PD (2004) Systematics of Upper Cretaceous calloporid bryozoans with primitive spinose ovicells. Palaeontology 47:775–793

    Article  Google Scholar 

  • Ostrovsky AN, Taylor PD (2005) Brood chambers constructed from spines in fossil and recent cheilostome bryozoans. Zool J Linn Soc 144:317–361

    Article  Google Scholar 

  • Ostrovsky AN, Grischenko AV, Taylor PD, Bock P, Mawatari SF (2006) Comparative anatomical study of internal brooding in three anascan bryozoans (Cheilostomata) and its taxonomical and evolutionary implications. J Morph 267:739–749

    Google Scholar 

  • Ostrovsky AN, Vávra N, Porter JS (2008) Sexual reproduction in gymnolaemate Bryozoa: history and perspectives of the research. In: Wyse Jackson PN, Spencer Jones ME (eds) Annals of bryozoology 2: aspects of the history of research on bryozoans. International Bryozoology Association, Dublin, pp 117–210

    Google Scholar 

  • Ostrovsky AN, Gordon DP, Lidgard S (2009a) Independent evolution of matrotrophy in the major classes of Bryozoa: transitions among reproductive patterns and their ecological background. Mar Ecol Prog Ser 378:113–124

    Article  Google Scholar 

  • Ostrovsky AN, O’Dea A, Rodrígues F (2009b) Comparative anatomy of internal incubational sacs in cupuladriid bryozoans and the evolution of brooding in free-living cheilostomes. J Morph 270:1413–1430

    Google Scholar 

  • Pfennig DW, Wund MA, Snell-Rood EC, Cruickshank T, Schlichting CD, Moczek AP (2010) Phenotypic plasticity’s impacts on diversification and speciation. Trends Ecol Evol 25:459–467

    Article  PubMed  Google Scholar 

  • Pratt MC (2004) Effect of zooid spacing on bryozoan feeding success: is competition or facilitation more important? Biol Bull 207:17–27

    Article  PubMed  Google Scholar 

  • Reed CG (1991) Bryozoa. In: Giese JS, Pearse JS, Pearse VB (eds) Reproduction of marine invertebrates. VI. Echinoderms and lophophorates. Boxwood Press, Pacific Grove, pp 85–245

    Google Scholar 

  • Rose MR, Lauder GV (1996) Post-spandrel adaptationism. In: Rose MR, Lauder GV (eds) Adaptation. Academic Press, London, pp 1–8

    Google Scholar 

  • Ruppert EE, Carle KJ (1983) Morphology of metazoan circulatory systems. Zoomorphology 103:193–208

    Article  Google Scholar 

  • Ryland JS (1970) Bryozoans. Hutchinson University Library, London

    Google Scholar 

  • Ryland JS (1977) Taxes and tropisms of bryozoans. In: Woollacott RM, Zimmer RL (eds) Biology of bryozoans. Academic Press, New York, pp 411–436

    Google Scholar 

  • Schlosser G, Wagner GP (2004) Modularity in development and evolution. University of Chicago Press, Chicago

    Google Scholar 

  • Schopf TJM (1973) Ergonomics of polymorphism: its relation to the colony as the unit of natural selection in species of the phylum Ectoprocta. In: Boardman RS, Cheetham AH, Oliver WAJ (eds) Animal colonies. Dowden, Hutchinson & Ross, Stroudsburg, pp 274–294

    Google Scholar 

  • Schwander T, Leimar O (2011) Genes as leaders and followers in evolution. Trends Ecol Evol 26:143–151

    Article  PubMed  Google Scholar 

  • Silén L (1942) Origin and development of the cheilo-ctenostomatous stem of Bryozoa. Zoologiska Bidrag Fran Uppsala 22:1–59

    Google Scholar 

  • Silén L (1977) Polymorphism. In: Woollacott RM, Zimmer RL (eds) Biology of bryozoans. Academic Press, New York, pp 184–231

    Google Scholar 

  • Ström R (1977) Brooding patterns of bryozoans. In: Woollacott RM, Zimmer RL (eds) Biology of bryozoans. Academic Press, New York, pp 23–56

    Google Scholar 

  • Tavener-Smith R, Williams A (1970) Structure of compensation sac in two ascophoran bryozoans. Proc R Soc Lond Ser B-Biol Sci 175:235–254

    Article  Google Scholar 

  • Taylor PD (1988) Major radiation of cheilostome bryozoans: triggered by the evolution of a new larval type? Hist Biol 1:45–64

    Article  Google Scholar 

  • Taylor PD, Larwood GP (1990) Major evolutionary radiations in the Bryozoa. In: Taylor PD, Larwood GP (eds) Major evolutionary radiations. Clarendon Press, Oxford, pp 209–233

    Google Scholar 

  • Taylor PD, McKinney FK (2002) Brooding in the Cretaceous bryozoan Stichomicropora and the origin of ovicells in cheilostomes. In: Wyse Jackson PN, Buttler CJ, Spencer Jones ME (eds) Bryozoan studies 2001. Proceedings of the 12th International Bryozoology Association symposium, Balkema, Lisse, pp 307–314

  • Taylor PD, Lazo DG, Aguirre-Urreta MB (2009) Lower Cretaceous bryozoans from Argentina: a ‘by-catch’ fauna from the Agrio Formation (Neuquén Basin). Cretac Res 30:193–203

    Article  Google Scholar 

  • Thorpe JP (1982) Bryozoa. In: Shelton GAB (ed) Electrical conduction and behaviour in ‘simple’ invertebrates. Clarendon Press, Oxford, pp 393–439

    Google Scholar 

  • Thorpe JP, Shelton GAB, Laverack MS (1975a) Colonial nervous control of lophophore retraction in cheilostome Bryozoa. Science 189:60–61

    Article  PubMed  CAS  Google Scholar 

  • Thorpe JP, Shelton GAB, Laverack MS (1975b) Electrophysiology and coordinated behavioral-responses in the colonial bryozoan Membranipora membranacea (L.). J Exp Biol 62:389–404

    Google Scholar 

  • Tsyganov-Bodounov A, Hayward PJ, Porter JS, Skibinski DOF (2009) Bayesian phylogenetics of Bryozoa. Mol Phylogenet Evol 52:904–910

    Article  PubMed  CAS  Google Scholar 

  • Tuomi J, Vuorisalo T (1989) Hierarchical selection in modular organisms. Trends Ecol Evol 4:209–213

    Article  PubMed  CAS  Google Scholar 

  • Vermeij GJ (1982) Unsuccessful predation and evolution. Am Nat 120(6):701–720

    Article  Google Scholar 

  • Vermeij GJ (1994) The evolutionary interaction among species—selection, escalation, and coevolution. Annu Rev Ecol Syst 25:219–236

    Article  Google Scholar 

  • Voigt E (1991) Mono- or polyphyletic evolution of cheilostomatous bryozoan divisions? Bulletin de la Société des Sciences Naturelles de l’Ouest de la France Memoire, H. S. 1:505–522

    Google Scholar 

  • Vuorisalo T, Tuomi J (1986) Unitary and modular organisms—criteria for ecological division. Oikos 47:382–385

    Article  Google Scholar 

  • Watson MA (1986) Integrated physiological units in plants. Trends Ecol Evol 1:119–123

    Article  PubMed  CAS  Google Scholar 

  • White J (1979) The plant as metapopulation. Annu Rev Ecol Syst 10:109–145

    Article  Google Scholar 

  • Winston JE (1984) Why bryozoans have avicularia—a review of the evidence. Am Mus Novitates 2789:1–26

    Google Scholar 

  • Winston JE (1986) Victims of avicularia. Mar Ecol 7:193–199

    Article  Google Scholar 

  • Winston JE (1991) Avicularian behaviour—a progress report. Bulletin de la Société des Sciences Naturelles de l’Ouest de la France Memoire, H. S. 1:531–540

    Google Scholar 

  • Winston JE (2010) Life in the colonies: learning the alien ways of colonial organisms. Integr Comp Biol 50:919–933

    Article  PubMed  Google Scholar 

  • Xing J, Qian PY (1999) Tower cells of the marine bryozoan Membranipora membranacea. J Morphol 239:121–130

    Article  Google Scholar 

  • Young RL, Badyaev AV (2006) Evolutionary persistence of phenotypic integration: influence of developmental and functional relationships on complex trait evolution. Evolution 60:1291–1299

    PubMed  Google Scholar 

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Acknowledgments

J.B.C. Jackson provided inspiration and cajoling that extend well beyond this paper. M. Hopkins, Field Museum, Chicago, and L.K. Nyhart, University of Wisconsin, Madison, provided useful comments on the manuscript. J.G. Harmelin, Centre d’Océanologie de Marseille, Université de la Méditerranée, graciously supplied the images in Fig. 4. MCC acknowledges support from a PhD Commonwealth Scholarship, Victoria University of Wellington, and the National Institute of Water & Atmospheric Research, Wellington. ANO thanks FWF, Austria (grant P22696-B17) and the RFBR, Russia (grants 10-04-00085-a, 10-04-10089-к) for financial support. We are grateful to all.

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Authors and Affiliations

  1. Department of Geology, Field Museum of Natural History, Chicago, IL, 60605, USA

    Scott Lidgard

  2. Centre for Marine Biodiversity and Biotechnology, School of Life Sciences, Heriot-Watt University, Edinburgh, EH14 4AS, Scotland, UK

    Michelle C. Carter

  3. Division of Natural History Sciences, Faculty of Science, Hokkaido University, N10 W8, Sapporo, 060-0810, Japan

    Matthew H. Dick

  4. National Institute of Water and Atmospheric Research, Private Bag 14901, Kilbirnie, Wellington, 6021, New Zealand

    Dennis P. Gordon

  5. Department of Invertebrate Zoology, Faculty of Biology and Soil Science, St. Petersburg State University, St. Petersburg, 199034, Russia

    Andrew N. Ostrovsky

  6. Department of Palaeontology, Faculty of Earth Sciences, Geography and Astronomy, Geozentrum, University of Vienna, 1090, Vienna, Austria

    Andrew N. Ostrovsky

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  2. Michelle C. Carter
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  3. Matthew H. Dick
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  4. Dennis P. Gordon
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  5. Andrew N. Ostrovsky
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Correspondence to Scott Lidgard.

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Lidgard, S., Carter, M.C., Dick, M.H. et al. Division of labor and recurrent evolution of polymorphisms in a group of colonial animals. Evol Ecol 26, 233–257 (2012). https://doi.org/10.1007/s10682-011-9513-7

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  • DOI: https://doi.org/10.1007/s10682-011-9513-7

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