Skip to main content
Springer Nature Link
Log in

Reduction, rearrangement, fusion, and hypertrophy: evolution of the muscular system in polymorphic zooids of cheilostome Bryozoa

  • Original Article
  • Published:
Organisms Diversity & Evolution Aims and scope Submit manuscript

Abstract

Morpho-functional polymorphism of modules, also known as “division of labor”, is a widespread phenomenon independently evolving multiple times in the colonies of many aquatic invertebrates and invertebrate chordates. Polymorphic zooids are especially diverse among Cheilostomata, the evolutionarily most successful clade in the phylum Bryozoa. The most diverse among cheilostome polymorphs are avicularia and vibracularia, acting as defensive, repelling, cleaning and locomotory “colonial organs”. While their skeletal characters were intensively studied, the soft tissues have largely been neglected. This hampers evolutionary interpretations. In this study, we compared the muscular system in five contrasting types of these polymorphs from 10 species of eight related as well as distant families. In contrast with the prevailing view, we found that the structural and functional changes affecting the muscular system during evolutionary transition from autozooid to polymorph were considerably more diverse and complex than mere “vestigialization”. These changes included muscle loss, hypertrophy, rearrangement (regrouping and relocation), fusion, and acquisition of asymmetry and muscle striation. Asynchronous contraction of originally synchronously working muscles was presumably evolved in advanced vibracularia. Some of these modifications were recorded in all avicularian types, whereas others were characteristic only for particular taxa or polymorphic categories. Our study showed that not only skeletal, but also soft parts of the polymorphs were evolutionarily very flexible and modified to various degrees and in various directions.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11
Fig. 12
Fig. 13
Fig. 14
Fig. 15
Fig. 16
Fig. 17
Fig. 18
Fig. 19

Similar content being viewed by others

Availability of data and materials

The datasets used and/or analyzed in this study are available from the corresponding author upon request.

References

  • Banta, W. C. (1973). Evolution of avicularia in cheilostome Bryozoa. In R. S. Boardman, A. Cheetham, & W. Oliver (Eds.), Animal colonies: Development and function through time (pp. 295–303). Dowden, Hutchinson & Ross. Inc.

  • Beklemishev, W. N. (1969). Principles of comparative anatomy of invertebrates. University of Chicago Press.

    Google Scholar 

  • Boardman, R. S., & Cheetham, A. H. (1969). Skeletal growth, intracolony variation, and evolution in Bryozoa: A review. Journal of Paleontology, 43(2), 205‒233. https://www.jstor.org/stable/1302305

  • Boardman, R. S., & Cheetham, A. H. (1973). Degrees of colony dominance in stenolaemate and gymnolaemate Bryozoa. In R. S. Boardman, A. H. Cheetham, & W. A. Oliver (Eds.), Animal colonies: Development and function through time (pp. 121‒220). Dowden, Hutchinson & Ross. Inc.

  • Borg, F. (1926). Studies on recent cyclostomatous Bryozoa. Zoologiska Bidrag Från Uppsala, 10(1), 181–507.

    Google Scholar 

  • Busk, G. (1849). Observations on the Shepherd’s Purse Coralline of Ellis, (Notamia bursaria, Fleming). Transactions of the Microscopical Society of London, 2(1), 110–121. https://doi.org/10.1111/j.1365-2818.1849.tb05113.x

    Article  Google Scholar 

  • Busk, G. (1854). Remarks on the structure and function of the avicularian and vibracular organs of the Polyzoa; and on their value as diagnostic characters in the classification of those creatures. Transactions of the Microscopical Society of London, New Series, 2, 26–33.

    Google Scholar 

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

  • Cáceres-Chamizo, J. P., Sanner, J., Tilbrook, K. J., & Ostrovsky, A. N. (2017). Revision of the Recent species of Exechonella Canu and Bassler in Duvergier, 1924 and Actisecos Canu & Bassler, 1927 (Bryozoa, Cheilostomata): Systematics, biogeography and evolutionary trends in skeletal morphology. Zootaxa, 4305, 1–79. https://doi.org/10.11646/zootaxa.4305.1.1

  • Carter, M. C. (2008). The functional morphology of avicularia in cheilostome bryozoans. PhD Thesis. Victoria University of Wellington.

  • Carter, M. C., Gordon, D. P., & Gardner, J. P. A. (2010a). Polymorphism and vestigiality: Comparative anatomy and morphology of bryozoan avicularia. Zoomorphology, 129(3), 195–211. https://doi.org/10.1007/s00435-010-0113-9

    Article  Google Scholar 

  • Carter, M. C., Gordon, D. P., & Gardner, J. P. A. (2010b). Polymorphism and variation in modular animals: Morphometric and density analyses of bryozoan avicularia. Marine Ecology Progress Series, 399, 117–130. https://doi.org/10.3354/meps08348

    Article  Google Scholar 

  • Carter, M. C., Lidgard, S., Gordon, D. P., & Gardner, J. P. A. (2011). Functional innovation through vestigialisation in a modular marine invertebrate. Biological Journal of the Linnean Society, 104(1), 63–74. https://doi.org/10.1111/j.1095-8312.2011.01706.x

    Article  Google Scholar 

  • Catwright, P., & Nawrocki, A. M. (2010). Character evolution in Hydrozoa (phylum Cnidaria). Integrative and Comparative Biology, 50(3), 456–472. https://doi.org/10.1093/icb/icq089

    Article  CAS  Google Scholar 

  • Cheetham, A. H., Sanner, J., Taylor, P. D., & Ostrovsky, A. N. (2006). Morphological differentiation of avicularia and the proliferation of species in mid-Cretaceous Wilbertopora Cheetham, 1954 (Bryozoa: Cheilostomata). Journal of Paleontology, 80(1), 49–71. https://doi.org/10.1666/0022-3360(2006)080[0049:MDOAAT]2.0.CO;2

  • Cook, P. L. (1968). Polyzoa from west Africa: The Malacostega. Part I. Bulletin of the British Museum (Natural History), Zoology, 16(3), 113–160.

  • Cook, P. L., & Chimonides, P. J. (1978). Observations on living colonies of Selenaria (Bryozoa, Cheilostomata). I. Cahiers De Biologie Marine, 19, 147–158.

    Google Scholar 

  • Cook, P. L., & Chimonides, P. J. (1983). A short history of the lunulite Bryozoa. Bulletin of Marine Science, 33(3), 566–581.

    Google Scholar 

  • Daly, M., Brugler, M. R., Cartwright, P., Collins, A. G., Dawson, M. N., Fautin, D. G., France, S. C., McFadden, C. S., Opresco, D. M., Rodriguez, E., Romano, S. L., & Stake, J. L. (2007). The phylum Cnidaria: A review of phylogenetic patterns and diversity 300 years after Linnaeus. Zootaxa. In Z.-Q. Zhang, & W. A. Shear (Eds.), Linnaeus tercentenary: Progress in invertebrate taxonomy. Zootaxa, 1668, 127–182. https://doi.org/10.5281/zenodo.180149

  • Darwin, C. (1839). Narrative of the surveying voyages of His Majesty’s ships Adventure and Beagle, between the years 1826 and 1836, describing their examination of the southern shores of South America, and the Beagle’s circumnavigation of the globe. Volume 3, Journal and remarks, 1832–1836. Henry Colburn.

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

  • Delage, Y., & Hérouard, E. (1897). Bryozoaires. – Bryozoaria. In S. Frères (Ed.), Traité de zoologie concrète, Les Vermidiens – Vermidea, 5, 47–155, Libraire C. Reinwald.

  • Dick, M. H., Grischenko, A. V., Gordon, D. P., & Ostrovsky, A. N. (2021). The "Cribrilina annulata" problem and new species of Juxtacribrilina (Bryozoa: Cheilostomata: Cribrilinidae) from the North Pacific. Zootaxa, 5016(3), 333–364. https://doi.org/10.11646/zootaxa.5016.3.2

  • Ellis, J. (1755). An essay towards a natural history of the corallines and other marine productions of the like kind, commonly found on the coasts of Great Britain and Ireland. A. Millar.

  • Fleming, J. (1814). Contributions to the British fauna. Memoirs of the Wernerian Natural History Society, 2, 238–251.

    Google Scholar 

  • Gordon, D. P. (1984). The marine fauna of New Zealand: Bryozoa: Gymnolaemata from the Kermadec Ridge. New Zealand Oceanographic Institute Memoir, 91, 1–198.

    Google Scholar 

  • Gordon, D. P., & Costello, M. J. (2016). Bryozoa – not a minor phylum. New Zealand Science Review, 73(3–4), 63–66. https://scientists.org.nz/resources/Documents/NZSR/NZSR73(3-4).pdf

  • Harvell, C. D. (1994). The evolution of polymorphism in colonial invertebrates and social insects. The Quarterly Review of Biology, 69(2), 155–185. https://doi.org/10.1086/418538

    Article  Google Scholar 

  • Herrera-Cubilla, A., Dick, M. H., Sanner, J., Jackson, J. B. C. (2008). Neogene Cupuladriidae of tropical America. II: Taxonomy of recent Discoporella from opposite sides of the Isthmus of Panama. Journal of Paleontology, 82(2), 279–298. https://doi.org/10.1666/06-034.1

  • Herwig, E. (1915). Die Avicularien von Bugula flabellata. Archiv Für Naturgeschichte. Abteilung A, 81(7), 156–159.

    Google Scholar 

  • Hiebert, L. S., Simpson, C., & Tiozzo, S. (2021). Coloniality, clonality, and modularity in animals: The elephant in the room. Journal of Experimental Zoology Part B: Molecular and Developmental Evolution, 336(3), 198–211. https://doi.org/10.1002/jez.b.22944

    Article  Google Scholar 

  • Hincks, T. (1878). Note on the movements of the vibracula in Caberea Boryi, and on the supposed common nervous system in the Polyzoa. Journal of Cell Science, 2(69), 7–9. https://doi.org/10.1242/jcs.s2-18.69.7

    Article  Google Scholar 

  • Hincks, T. (1880a). A history of the British marine Polyzoa. J. Van Voorst.

  • Hincks, T. (1880b). Contributions towards a general history of the marine Polyzoa. Part II. Foreign Membraniporina. Annals & Magazine of Natural History, 6(5), 81–92.

  • Hincks, T. (1882). III. On certain remarkable modifications of the avicularium in a species of Polyzoon; and on the relation of the vibraculum to the avicularium. Journal of Natural History, 9(49), 20–25. https://doi.org/10.1080/00222938209458984

  • Hyman, L. H. (1959). The invertebrates: Smaller coelomate groups, Chaetognatha, Hemichordata, Pogonophora, Phoronida, Ectoprocta, Brachipoda, Sipunculida, the coelomate Bilateria. Volume V. McGraw-Hill.

  • Jullien, J. (1888). Bryozoaires. Mission scientifique Cap Horn, 1882–1883, 6 (Zoologie Part 3), 1–92. Gauthier Villars et Fils, Imprimeurs-Libraires.

  • Kluge, G. A. (1914). Die Bryozoen der Deutschen Südpolar-Expeditionen 1901–1903. 1. Die Familien Aetidae, Cellularidae, Bicellaridae, Farciminaridae, Flustridae, Membraniporidae und Cribrilinidae. Deutschen Sudpolar Expedition, 15. Zoologie, 7, 601–678.

  • Krohn, A. (1843). Ueber die vogelkopfähnlichen und ihnen verwandten Organe bei den Bryozoën. Neue Notizen Aus Dem Gebiete Der Natur- Und Heilkunde, 25(533), 70–72.

    Google Scholar 

  • Lidgard, S., Carter, M. C., Dick, M. H., Gordon, D. P., & Ostrovsky, A. N. (2012). Division of labor and recurrent evolution of polymorphisms in a group of colonial animals. Evolutionary Ecology, 26(2), 233–257. https://doi.org/10.1007/s10682-011-9513-7

  • Linnaeus, C. (1758). Systema Naturae per regna tria naturae, secundum classes, ordines, genera, species, cum characteribus, differentiis, synonymis, locis. 10th revised edition, Vol. 1. Laurentius Salvius.

  • Lutaud, G. (1965). Sur la présence de microorganismes spécifiques dans les glandes vestibulaires de Palmicellaria skenei (Ellis et Solander), Bryozoaire Chilostome. Cahiers de Biologie Marine, 6(2), 181–190.

    Google Scholar 

  • Lutaud, G. (1977). L’innervation de l’aviculaire pédonculé des Bicellariidae (Bryozoaires Chilostomes). Cahiers de Biologie Marine, 18(4), 435–448.

    Google Scholar 

  • Lutaud, G. (1983). Autozooid morphogenesis in anascan cheilostomates. In R. S. Boardman, A. H. Cheetham, D. B. Blake, J. Utgaard, O. L. Karklins, P. L. Cook, P. A. Sandberg, G. Lutaud, & T. S. Wood (Eds.), Bryozoa (revised). Treatise on invertebrate paleontology. Part G (pp. 208–237). The Geological Society of America & The University of Kansas.

  • Lutaud, G. (1984). La structure et l’innervation du diaphragme de la gaine tentaculaire chez deux Bryozoaires Malacostèges. Zoologica Scripta, 13(1), 59–67. https://doi.org/10.1111/j.1463-6409.1984.tb00023.x

    Article  Google Scholar 

  • Marcus, E. (1926). Bryozoa. In G. Grimpe & E. Wagler (Eds.), Die Tierwelt der Nord- und Ostsee (pp. 1–100). Academische Verlagsgesellschaft.

    Google Scholar 

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

  • Marcus, E., & Marcus, E. (1962). On some lunulitiform Bryozoa. Boletims da Faculdade de Filosofia, Ciências e Letras, Universidade de São Paulo, Zoologia, 24(24), 281–324. https://doi.org/10.11606/issn.2526-3382.bffclzoologia.1962.120591

  • Martha, S. O., Vieira L. M., Souto-Derungs J., Grischenko A. V., Gordon D. P., & Ostrovsky A. N. (2021). Gymnolaemata, Cheilostomata. In T. F. Schwaha (Ed.), Handbook of zoology. Phylum Bryozoa (pp. 101–121). De Gruyter. https://doi.org/10.1515/9783110586312-011

  • McKinney, F. K., & Jackson, J. B. (1991). Bryozoan evolution. University of Chicago Press.

    Google Scholar 

  • Mukai, H., Terakado, K., & Reed, C. (1997). Bryozoa. In F. W. Harrison & R. M. Woollacott (Eds.), Microscopic anatomy of invertebrates (pp. 45–206). John Wiley & Sons. Inc.

    Google Scholar 

  • Munro, C., Zapata, F., Howison, M., Siebert, S., & Dunn, C. W. (2022). Evolution of gene expression across species and specialized zooids in Siphonophora. Molecular Biology and Evolution, 39(2), msac027. https://doi.org/10.1093/molbev/msac027

  • Nekliudova, U. A., Shunkina, K. V., Grishankov, A. V., Varfolomeeva, M. A., Granovitch, A. I., & Ostrovsky, A. N. (2019a). Colonies as dynamic systems: Reconstructing the life history of Cribrilina annulata (Bryozoa) on two algal substrates. Journal of the Marine Biological Association of the United Kingdom, 99(6), 1363–1377. https://doi.org/10.1017/S0025315419000286

    Article  CAS  Google Scholar 

  • Nekliudova, U. A., Schwaha, T. F., Kotenko, O. N., Gruber, D., Cyran, N., & Ostrovsky, A. N. (2019b). Sexual reproduction of the placental brooder Celleporella hyalina (Bryozoa, Cheilostomata) in the White Sea. Journal of Morphology, 280(2), 278–299. https://doi.org/10.1002/jmor.20943

    Article  PubMed  PubMed Central  Google Scholar 

  • Nekliudova, U. A., Schwaha, T. F., Kotenko, O. N., Gruber, D., Cyran, N., & Ostrovsky, A. N. (2021). Three in one: Evolution of viviparity, coenocytic placenta and polyembryony in cyclostome bryozoans. BMC Ecology Evolution, 21(1), 1–34. https://doi.org/10.1186/s12862-021-01775-z

    Article  Google Scholar 

  • Nitsche, H. (1871a). On some interesting points concerning the mode of reproduction of the Bryozoa. Quarterly Journal of Microscopical Science (N. S.), 11, 155–162. https://doi.org/10.1242/jcs.s2-11.42.155

  • Nitsche, H. (1871b). Beiträge zur Kenntnis der Bryozoen. III. Über die Anatomie und Entwicklungsgeschichte von Flustra membranacea. Zeitschrift für Wissenschaftliche Zoologie, 21(4), 416–470.

  • Nordmann de, M. A. (1840). Observations sur la fauna Pontique. In Voyage dans la Russie Méridionale et la Crimée, par la Hongrie, la Valachie et la Moldavie, exécuté en 1837 sous la direction de m. Anatole de Demidoff, 3, 1–756. Ernest Bourdin et Ce, Éditeurs.

  • Ostrovsky, A. N. (1998). Comparative studies of ovicell anatomy and reproductive patterns in Cribrilina annulata and Celleporella hyalina (Bryozoa: Cheilostomatida). Acta Zoologica, 79(4), 287–318. https://doi.org/10.1111/j.1463-6395.1998.tb01280.x

    Article  Google Scholar 

  • Ostrovsky, A. N. (2013a). Evolution of sexual reproduction in marine invertebrates: Example of gymnolaemate bryozoans. Springer. http://link.springer.com/book/10.1007%2F978-94-007-7146-8

  • Ostrovsky, A. N. (2013b). From incipient to substantial: Evolution of placentotrophy in a phylum of aquatic colonial invertebrates. Evolution, 67(5), 1368–1382. https://doi.org/10.1111/evo.12039https://doi.org/10.1111/j.1463-6395.1998.tb01280.x

  • Ostrovsky, A. N. (2021). Sexual reproduction in Bryozoa. In T. F. Schwaha (Ed.), Handbook of zoology. Phylum Bryozoa (pp. 101–121). De Gruyter. https://doi.org/10.1515/9783110586312-004

  • Ostrovsky, A. N., Schäfer, P., & Gordon, D. P. (2003). Ultrastructure and development of the ooecial walls in some calloporid bryozoans. Zoologischer Anzeiger, 242(3), 223–240. https://doi.org/10.1078/0044-5231-00100

    Article  Google Scholar 

  • Ostrovsky, A. N., Grischenko, A. V., Taylor, P. D., Bock, P. E., & Mawatari, S. F. (2006). Comparative anatomical study of internal brooding in three anascan bryozoans (Cheilostomata) and its taxonomic and evolutionary implications. Journal of Morphology, 267(6), 739–749. https://doi.org/10.1002/jmor.10438

    Article  PubMed  Google Scholar 

  • Ostrovsky, A. N., Dick, M. H., & Mawatari, S. F. (2007). The internal brooding apparatus in the bryozoan genus Cauloramphus (Cheilostomata: Calloporidae) and its inferred homology to ovicells. Zoological Science, 24(12), 1187–1196. https://doi.org/10.2108/zsj.24.1187

    Article  PubMed  Google Scholar 

  • Ostrovsky, A. N., Nielsen, C., Vavra, N., & Yagunova, E. (2009a). Diversity of the brooding structures in calloporod bryozoans (Gymnolaemata: Cheilostomata): Comparative anatomy and evolutionary trends. Zooomorphology, 128(1), 13–35. https://doi.org/10.1007/s00435-008-0070-8

    Article  Google Scholar 

  • Ostrovsky, A. N., O’Dea, A., & Rodriguez, F. (2009b). Comparative anatomy of internal incubational sacs in cupuladriid bryozoans and the evolution of brooding in free-living cheilostomes. Journal of Morphology, 270(12), 1413–1430. https://doi.org/10.1002/jmor.10767

    Article  PubMed  Google Scholar 

  • Ostrovsky, A. N., & Taylor, P. D. (2004). Systematics of Upper Cretaceous calloporid bryozoans with primitive spinose ovicells. Palaeontology, 47(3), 775–793. https://doi.org/10.1111/j.0031-0239.2004.00379.x

    Article  Google Scholar 

  • Ostrovsky, A. N., & Taylor, P. D. (2005). Brood chambers constructed from spines in fossil and Recent cheilostome bryozoans. Zoological Journal of the Linnean Society, 144(3), 317–361. https://doi.org/10.1111/j.1096-3642.2005.00179.x

    Article  Google Scholar 

  • Packard, A. S. (1863). A list of animals dredged near Caribou Island, southern Labrador, during July and August, 1860. Canadian Naturalist, 8, 401–429.

    Google Scholar 

  • Plachetzki, D. C., Sabrina Pankey, M., Johnson, B. R., Ronne, E. J., Kopp, A., & Grosberg, R. K. (2014). Gene co-expression modules underlying polymorphic and monomorphic zooids in the colonial hydrozoan. Hydractinia symbiolongicarpus. American Zoologist, 54(2), 276–283. https://doi.org/10.1093/icb/icu080

    Article  Google Scholar 

  • Prenant, M., & Bobin, G. (1966). Bryozoaires. Deuxième partie, Chilostomes Anasca. In Faune de France, 68, 1–647. Lechevalier.

  • Reid, J. (1845). Anatomical and physiological observations on some zoophytes. Journal of Natural History, 16(107), 385–400. https://doi.org/10.1080/037454809495965

    Article  Google Scholar 

  • Ryland, J. S. (1970). Bryozoans. Hutchinson University Library.

  • Ryland, J. S. (2005). Bryozoa: An introductory overview. In E. Woess (Ed.), Moostiere (Bryozoa). Denisia, 16, 9–20. Oberösterreichisches Landesmuseum.

  • Sanders, S. M., Shcheglovitova, M., & Cartwright, P. (2014). Differential gene expression between functionally specialized polyps of the colonial hydrozoan Hydractinia symbiolongicarpus (Phylum Cnidaria). BMC Genomics, 15(1), 1–15. https://doi.org/10.1186/1471-2164-15-406

    Article  Google Scholar 

  • Santagata, S. (2021). Genes with evidence of positive selection as potentially related to coloniality and the evolution of morphological features among the lophophorates and entoprocts. Journal of Experimental Zoology Part B: Molecular and Developmental Evolution, 336(3), 267–280. https://doi.org/10.1002/jez.b.22975

    Article  Google Scholar 

  • Sars, M. (1851). Beretning om i sommeren 1849 fortagen zoologisk reise i Lofoten og Finmarken. Nyt Magazin Naturvidenskaberne, 6(2), 121–211.

    Google Scholar 

  • Schack, C. R., Gordon, D. P., & Ryan, K. G. (2018). Classification of cheilostome polymorphs. In P. N. Wyse Jackson, & M. E. Spencer Jones (Eds.), Annals of bryozoology, 6, 85–134. International Bryozoology Association.

  • Schack, C. R., Gordon, D. P., & Ryan, K. G. (2019). Modularity is the mother of invention: A review of polymorphism in bryozoans. Biological Reviews, 94(3), 773–809. https://doi.org/10.1111/brv.12478

    Article  PubMed  Google Scholar 

  • Schopf, T. J. (1977). Patterns and themes of evolution among the Bryozoa. In Developments in Palaeontology and Stratigraphy, 5, 159–207. Elsevier. https://doi.org/10.1016/S0920-5446(08)70326-1

  • Schopf, T. J., Boardman, R. S., Cheetham, A. H., & Oliver, W. A. (1973). Ergonomics of polymorphism: Its relation to the colony as the unit of natural selection in species of the phylum Ectoprocta. In R. S. Boardman, A. H. Cheetham & W. A. Oliver (Eds.), Animal colonies: Development and function through time (pp. 247–294). Dowden, Hutchinson & Ross. Inc.

  • Schwaha, T. (2021). Phylum Bryozoa. In Handbook of zoology. DeGruyter. https://doi.org/10.1515/9783110586312

  • Schwaha, T. F., Handschuh, S., Ostrovsky, A. N., & Wanninger, A. (2018). Morphology of the bryozoan Cinctipora elegans (Cyclostomata, Cinctiporidae) with first data on its sexual reproduction and the cyclostome neuro-muscular system. BMC Evolutionary Biology, 18(1), 92. https://doi.org/10.1186/s12862-018-1206-1

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Schwaha, T. F., Ostrovsky, A. N., & Wanninger, A. (2020). Key novelties in the evolution of aquatic colonial phylum Bryozoa: Evidence from soft body morphology. Biological Reviews, 95(3), 696–729. https://doi.org/10.1111/brv.12583

    Article  PubMed  Google Scholar 

  • Schwaha, T. F., & Wanninger, A. (2015). The serotonin-lir nervous system of the Bryozoa (Lophotrochozoa): A general pattern in the Gymnolaemata and implications for lophophore evolution of the phylum. BMC Evolutionary Biology, 15(1), 223. https://doi.org/10.1186/s12862-015-0508-9

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Schwaha, T. F., & Wanninger, A. (2018). Unity in diversity: A survey of muscular systems of ctenostome Gymnolaemata (Lophotrochozoa, Bryozoa). Frontiers in Zoology, 15(1), 24. https://doi.org/10.1186/s12983-018-0269-6

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Schwaha, T., Wood, T. S., & Wanninger, A. (2011). Myoanatomy and serotonergic nervous system of the ctenostome Hislopia malayensis: Evolutionary trends in bodyplan patterning of Ectoprocta. Frontiers in Zoology, 8(1), 1–16. https://doi.org/10.1186/1742-9994-8-11

    Article  Google Scholar 

  • Serova, K. M., Vishnyakov, A. E., Zaitseva, O. V., & Ostrovsky, A. N. (2016). Distribution of serotonin and FMRF-Amide in the nervous system of different zooidal types of cheilostome Bryozoa: A case study of Arctonula arctica. Doklady Biological Sciences, 471(1), 288–290. https://doi.org/10.1134/S0012496616060107

    Article  PubMed  CAS  Google Scholar 

  • Serova, K. M., Vishnyakov, A. E., Zaitseva, O. V., Kotenko, O. N., & Ostrovsky, A. N. (2017). Comparative analysis of the nervous system structure of polymorphic zooids in marine bryozoans. Doklady Biological Sciences, 475(1), 144–147. https://doi.org/10.1134/S0012496617040056

    Article  PubMed  CAS  Google Scholar 

  • Shunkina, K. V., Zaytseva, O. V., Starunov, V. V., & Ostrovsky, A. N. (2015). Comparative morphology of the nervous system in three phylactolaemate bryozoans. Frontiers in Zoology, 12(1), 28. https://doi.org/10.1186/s12983-015-0112-2

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Shunatova, N., & Tamberg, Y. (2019). Body cavities in bryozoans: Functional and phylogenetic implications. Journal of Morphology, 280(9), 1332–1358. https://doi.org/10.1002/jmor.21034

    Article  PubMed  Google Scholar 

  • Shunatova, N., & Borisenko, I. (2020). Proliferating activity in a bryozoan lophophore. PeerJ, 8, e9179. https://doi.org/10.7717/peerj.9179

    Article  PubMed  PubMed Central  Google Scholar 

  • Shunatova, N., Denisova, S., & Shchenkov, S. (2021). Ultrastructure of rhizoids in the marine bryozoan Dendrobeania fruticosa (Gymnolaemata: Cheilostomata). Journal of Morphology, 282(6), 847–862. https://doi.org/10.1002/jmor.21351

    Article  PubMed  CAS  Google Scholar 

  • Shunatova, N., Serova, K., Denisova, S., Shchenkov, S., & Ostrovsky, A. (2022). Small, but smart: Fine structure of an avicularium in Dendrobeania fruticosa (Bryozoa: Cheilostomata). Journal of Morphology, 283(2), 174–206. https://doi.org/10.1002/jmor.21436

    Article  PubMed  Google Scholar 

  • Siebert, S., Robinson, M. D., Tintori, S. C., Goetz, F., Helm, R. R., Smith, S. A., Shaner, N., Haddock, S. H. D., & Dunn, C. W. (2011). Differential gene expression in the siphonophore Nanomia bijuga (Cnidaria) assessed with multiple next-generation sequencing workflows. PLoS ONE, 6(7), e22953. https://doi.org/10.1371/journal.pone.0022953

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Silén, L. (1938). Zur Kenntnis des Polymorphismus der Bryozoen: Die Avicularien der Cheilostomata Anasca. Zoologiska Bidrag Från Uppsala, 17, 149–366.

    Google Scholar 

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

    Google Scholar 

  • Silén, L. (1950). On the mobility of entire zoids in Bryozoa. Acta Zoologica, 31(2–3), 349–386. https://doi.org/10.1111/j.1463-6395.1950.tb00515.x

    Article  Google Scholar 

  • Silén, L. (1977). Polymorphism. In R. M. Woollacott & R. L. Zimmer (Eds.), Biology of bryozoans (pp. 184–231). Academic Press.

    Google Scholar 

  • Silén, L. (1980). Colony-substratum relations in Scrupocellariidae (Bryozoa, Cheilostomata). Zoologica Scripta, 9, 211–217.

  • Simpson, C., Jackson, J. B., & Herrera-Cubilla, A. (2017). Evolutionary determinants of morphological polymorphism in colonial animals. American Naturalist, 190(1), 17–28. https://doi.org/10.1086/691789

    Article  PubMed  Google Scholar 

  • Smitt, F. A. (1865). Om Hafs-Bryozoernas utveckling och fettkroppar. Öfversigt Af Kongliga Vetenskaps-Akademiens Förhandlingar, 1, 5–50.

    Google Scholar 

  • Smitt, F. A. (1868). Kritisk forteckning ofver Skandinaviens Hafs-Bryozoer. Part 4. Öfversigt Af Kongliga Vetenskaps-Academiens Förhandlingar, 25, 3–320.

    Google Scholar 

  • Taylor, P. D. (2020). Bryozoan paleobiology. John Wiley & Sons.

    Book  Google Scholar 

  • Temereva, E. N., & Kosevich, I. A. (2016). The nervous system of the lophophore in the ctenostome Amathia gracilis provides insight into the morphology of ancestral ectoprocts and the monophyly of the lophophorates. BMC Evolutionary Biology, 16(1), 1–24. https://doi.org/10.1186/s12862-016-0744-7

    Article  CAS  Google Scholar 

  • Temereva, E. N., & Kosevich, I. A. (2018). The nervous system in the cyclostome bryozoan Crisia eburnea as revealed by transmission electron and confocal laser scanning microscopy. Frontiers in Zoology, 15(1), 1–15. https://doi.org/10.1186/s12983-018-0295-4

    Article  CAS  Google Scholar 

  • Treibergs, K. A., & Giribet, G. (2020). Differential gene expression between polymorphic zooids of the marine bryozoan Bugulina stolonifera. G3: Genes, Genomes, Genetics, 10(10), 3843–3857. https://doi.org/10.1534/g3.120.401348

  • Van Beneden, P. J. (1845). Recherches sur l’anatomie, la physiologie et le développement des Bryozoaires qui habitent la côte d’Ostende. Nouvelle Memoires de L’academie Royale des Sciences, des Lettres et des Beaux-Arts de Belgique, 18, 1–44.

    Google Scholar 

  • Van Beneden, P. J. (1848). Recherches sur les polypes bryozoaires de la Mer du Nord. Bulletins de L’academie Royale des Sciences, des Lettres et des Beaux-Arts de Belgique, 15, 67–82.

    Google Scholar 

  • Venit, E. P. (2007). Evolutionary trends in the individuation and polymorphism of colonial marine invertebrates. PhD Thesis. Duke University.

  • Vigelius, W. J. (1884). Morphologische Untersuchungen über Flustra membranaceotruncata Smith. Biologisches Zentralblatt, 3(23), 705–721.

    Google Scholar 

  • Waters, A. (1904). Bryozoa. Résultats du Voyage du SY Belgica en 1897–1898–1899. Expédition Antarctique Belge, Zoologie, 4, 1–114.

    Google Scholar 

  • Winston, J. E. (1984). Why bryozoans have avicularia – A review of the evidence. American Museum of Natural History, 2789, 1–26. http://digitallibrary.amnh.org/dspace/handle/2246/5383

  • Winston, J. E. (1986). Victims of avicularia. Marine Ecology, 7(3), 193–199. https://doi.org/10.1111/j.1439-0485.1986.tb00157.x

    Article  Google Scholar 

  • Winston, J. E. (1991). Avicularian behavior – a progress report. In F. P. Bigey & J.-L. d’Hondt (Eds.), Bryozoaires actuels et fossiles: Bryozoa living and fossil. Bulletin de la Société des Sciences Naturelles de l’Ouest de la France, Mémoire Hors Série, 1, 531–540.

  • Winston, J. E. (2010). Life in the colonies: Learning the alien ways of colonial organisms. Integrative & Comparative Biology, 50(6), 919–933. https://doi.org/10.1093/icb/icq146

    Article  Google Scholar 

  • Winston J. E., & Migotto A. E. (2021). Behavior. In T. F. Schwaha (Ed.), Handbook of zoology. Phylum Bryozoa (pp. 143–187). De Gruyter.

  • Worsaae, K., Frykman, T., & Nielsen, C. (2020). The neuromuscular system of the cyclostome bryozoan Crisia eburnea (Linnaeus, 1758). Acta Zoologica, 101(2), 133–146. https://doi.org/10.1111/azo.12280

    Article  Google Scholar 

  • Zhang, Z., Zhang, Z., Ma, J., Taylor, P. D., Strotz, L. C., Jacquet, S. M., Skovsted, C. B., Chen, F., Han, J., & Brock. G. A. (2021). Fossil evidence unveils an early Cambrian origin for Bryozoa. Nature, 599(7884), 251–255. https://doi.org/10.1038/s41586-021-04033-w

Download references

Acknowledgements

This study was partly performed using the laboratories and equipment of the Educational and Research Station “Belomorskaia”, Saint Petersburg State University, Russia, and of the Sven Lovén Centre for Marine Sciences, Kristineberg, University of Gothenburg, Sweden. Light and confocal laser scanning microscopical work was done at the Department of Invertebrate Zoology and Resource Centers “Development of Molecular and Cell Technologies” and “Microscopy and Microanalysis”, all Saint Petersburg State University. We thank Mr S.V. Bagrov, Department of Invertebrate Zoology, Saint Petersburg University, for his help in collecting the material, and Ms N.P. Karagodina, Department of Invertebrate Zoology, Saint Petersburg University, for additional photo images. Drs U.A. Nekliudova, Department of Invertebrate Zoology, Saint Petersburg University, and K.V. Shunkina, Department of Evolutionary Morphology, Zoological Institute, Russian Academy of Sciences, kindly taught the first author histological methods at the early stages of her career. Dr M. Stachowitsch, University of Vienna, Austria, revised an early draft of the manuscript and improved its English. One reviewer kindly helped to improve the manuscript.

Funding

SKM received financial support from the Russian Science for Basic Research (grant 20–34-90081). OAN received financial support from the Smithsonian Marine Science Network Award, USA (grant FY11), which supported the research trip to Panama.

Author information

Authors and Affiliations

  1. Laboratory of Evolutionary Morphology, Zoological Institute, Russian Academy of Sciences, Universitetskaja nab. 1, 199034, Saint Petersburg, Russia

    K.M. Serova & O.V. Zaitseva

  2. Department of Invertebrate Zoology, Faculty of Biology, Saint Petersburg State University, Universitetskaja nab. 7/9, 199034, Saint Petersburg, Russia

    K.M. Serova, E.V. Belikova, O.N. Kotenko, A.E. Vishnyakov, E.A. Bogdanov, N.N. Shunatova & A.N. Ostrovsky

  3. Department of Palaeontology, Faculty of Earth Sciences, Geography and Astronomy, Geozentrum, University of Vienna, Althanstraße 14, 1090, Vienna, Austria

    A.N. Ostrovsky

Authors
  1. K.M. Serova
    View author publications

    You can also search for this author inPubMed Google Scholar

  2. E.V. Belikova
    View author publications

    You can also search for this author inPubMed Google Scholar

  3. O.N. Kotenko
    View author publications

    You can also search for this author inPubMed Google Scholar

  4. A.E. Vishnyakov
    View author publications

    You can also search for this author inPubMed Google Scholar

  5. E.A. Bogdanov
    View author publications

    You can also search for this author inPubMed Google Scholar

  6. O.V. Zaitseva
    View author publications

    You can also search for this author inPubMed Google Scholar

  7. N.N. Shunatova
    View author publications

    You can also search for this author inPubMed Google Scholar

  8. A.N. Ostrovsky
    View author publications

    You can also search for this author inPubMed Google Scholar

Contributions

OAN designed and coordinated research. SKM, KON, BEV, VAE, and OAN collected material. SKM, BEV, KON, VAE, ZOV, and SNN conducted practical work and contributed to data interpretation. BEA did art work and contributed to data interpretation. SKM and OAN analyzed the data and wrote the manuscript. All authors have read and approved the manuscript.

Corresponding author

Correspondence to A.N. Ostrovsky.

Ethics declarations

Ethics approval and consent to participate

Not applicable.

Competing interests

The authors declare no competing interests.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Serova, K., Belikova, E., Kotenko, O. et al. Reduction, rearrangement, fusion, and hypertrophy: evolution of the muscular system in polymorphic zooids of cheilostome Bryozoa. Org Divers Evol 22, 925–964 (2022). https://doi.org/10.1007/s13127-022-00562-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13127-022-00562-y

Keywords