Summary
Many freshwater organisms exhibit mixed life histories that include sexual and asexual phases of reproduction. Ecological and genetic studies have revealed insights about the consequences of mixed life histories for populations of planktonic cladocerans and rotifers and aquatic macrophytes. However, little is known of the consequences of mixed life histories for populations of benthic colonial freshwater invertebrates. A series of investigations of the ecology and genetics of local populations of the freshwater bryozoan, Cristatella mucedo, are reviewed in this context. Asexual reproduction achieved by colony growth, fission, and the production of numerous resistant statoblasts promotes the persistence and dispersal of clones and leads to extensive genetic similarity within and between populations in southern England. Genetic characterization of parent and larval colonies indicates that sexual reproduction results in inbreeding amongst genetically similar clonal stock within sites and so generates little genetic variation. Ecological sampling confirms that sexual reproduction is limited in duration and suggests that in some sites and/or years, a sexual phase is foregone entirely. Myxozoans parasitize these genetically similar host populations and apparently indiscriminately attack the highly-related bryozoan clones present within a site. As myxozoans adversely affect host fitness they may, in part, be responsible for the drastic reductions and occasional extinctions observed in C. mucedo populations. The presence of harmful parasites and the relative insignificance of sex suggest that host-parasite coevolution as predicted by the Red Queen does not apply in this system. Rather, evidence indicates that a metapopulation structure allows the persistence of genetically-similar sub-populations as long as rates of asexual replication and dispersal are sufficient to provide a means of escape from parasites and other adverse conditions. Thus metapopulation structure may provide at least a short-term alternative to the regular production of genetic novelty through sex. Perhaps due to features such as a sessile nature, asexual replication via vegetative growth, and indirect fertilization, the consequences of mixed life histories for bryozoans of southern England contrast with those in planktonic cladocerans and rotifers but show some similarities to those of aquatic macrophytes.
This is a preview of subscription content, log in via an institution.
Buying options
Tax calculation will be finalised at checkout
Purchases are for personal use only
Learn about institutional subscriptionsPreview
Unable to display preview. Download preview PDF.
References
Abrahamson, W.G. (1980) Demography and vegetative reproduction. In: O.T. Solbrig (ed.): Demography and Evolution in Plant Populations. Blackwell Scientific Publications, Oxford, pp 89–106.
Aspinwall, N. and Christian, T. (1992) Clonal structure, genotypic diversity, and seed production in populations of Filipendula rubra (Rosaceae) from the northcentral United States. Am. J.Bot. 79:294–299.
Backus, B.T. and Mukai, H. (1987) Chromosomal heteromorphism in a Japanese population of Pectinatella gelatinosa and karyotypic comparison with some other phylactolaemate bryozoans. Genetica 73:189–196.
Bell, G. (1982) The Masterpiece of Nature - The Evolution and Genetics of Sexuality. University of California Press, Berkeley, California.
Bierzychudek, P. (1987) Patterns in plant parthenogenesis. In: S.C. Stearns (ed.): The Evolution of Sex and Its Consequences. Birkhàuser Verlag, Basel, pp 197–217.
Brien, P. and Mordant, C. (1956) Relations entre les reproduction sexuée et asexuée a propose de phylactolaemates. Annls Soc. R. Zool. Belg. 86:169–189.
Brown, C.J.D. (1933) A limnological study of certain fresh-water Polyzoa with special reference to their statoblasts. Trans. Am. Microsc. Soc. 52:271–313.
Bushnell, J.H. (1973) The freshwater Ectoprocta: A zoogeographical discussion. In: G.P. Larwood (ed.): Living and Fossil Bryozoa. Academic Press, London, pp 503–521.
Buss, L.W. (1979) Habitat selection, directional growth and spatial refuges: Why colonial animals have more hiding places. In: G. Larwood and B.R. Rosen (eds): Biology and Systematics of Colonial Organisms. Academic Press, London, pp 459–497.
Canning, E.U., Okamura, B. and Curry, A. (1996) Development of a myxozoan parasite Tetra-capsula bryozoides n.g., n.sp. in Cristatella mucedo (Bryozoa, Phylactolaemata). Folia Parasitol. 43:249–261.
Carvalho, G.R. (1987) The clonal ecology of Daphnia magna (Crustacea: Cladocera) II. Thermal differentiation among seasonal clones. J. Anim. Ecol. 56:469–478.
Carvalho, G.R. (1994) Evolutionary genetics of aquatic clonal invertebrates: Concepts, problems and prospects. In: A. Beaumont (ed.): Genetics and Evolution of Aquatic Organisms. Chapman and Hall, London, pp 291–323.
Carvalho, G.R. and Crisp, D.J. (1987) The clonal ecology of Daphnia magna (Crustacea: Cladocera). I. Temporal changes in the clonal structure of a natural population. J.Anim. Ecol. 56:453–468.
Chapco, W., Ashton, N.W., Martel, R.K.B. and Antonishyn, N. (1992) A feasibility study of the use of randomly amplified polymorphic DNA in the population genetics and systematics of grasshoppers. Genome 35:569–574.
Cook, R.E. (1987) Vegetative growth and genetic mobility in some aquatic weeds. In: K.M. Urbanska (ed.): Differentiation Patterns in Higher Plants. Academic Press, London, pp 217–225.
DeMeester, L. (1991) An analysis of the phototactic behaviour of Daphnia magna clones and their sexual descendants. Hydrobiologia 225:217–227.
Denny, M.W. and Shibata, M.F. (1989) Consequences of surf-zone turbulence for settlement and external fertilization. Amer. Nat. 117:838–840.
Dias, P.C. (1996) Sources and sinks in population biology. Trends Ecol. Evol. 11:326–330.
Dybdahl, M.F. and Lively, C.M. (1995) Host-parasite interactions: Infection of common clones in natural populations of a freshwater snail (Potamopyrgus antipodarum). Proc. R. Soc. Lond. B 260:99–103.
Ebert, D. and Hamilton, W.D. (1996) Sex against virulence: The coevolution of parasitic diseases. Trends. Ecol. Evol. 11:79–82.
Eckert, C.G. and Barrett, S.C.H. (1993) Clonal reproduction and patterns of genotypic diversity in Decodon verticillatus (Lythraceae). Am. J. Bot. 80:1175–1182.
Ellstrand, N.C. and Roose, M.L. (1987) Patterns of genotypic diversity in clonal plant species. Am. J. Bot. 74:123–131.
Excoffier, L., Smouse, RE. and Quattro, J.M. (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: Application to human mitochondrial DNA restriction data. Genetics 131:479–491.
Ghiselin, M.T. (1974) The Economy of Nature and the Evolution of Sex. University of California Press, Berkeley, California.
Gotelli, N.J. (1995) A Primer of Ecology. Sinauer Associates, Inc., Sunderland, Massachusetts.
Grosberg, R.K., Levitan, D.R. and Cameron, B.B. (1996) Characterization of genetic structure and genealogies using RAPD-PCR markers: A random primer for the novice and nervous. In: J.D. Ferraris and S.R. Palumbi (eds): Molecular Zoology: Advances, Strategies and Protocols. Wiley-Liss, New York, pp 67–100.
Hamilton, W.D. (1980) Sex versus non-sex versus parasite. Oikos 35:282–290.
Hanski, I. (1996) Metapopulation ecology. In: O.E. Rhodes Jr., R.K. Chesser and M.H. Smith (eds): Population Dynamics in Ecological Space and Time. University of Chicago Press, Chicago, pp 13–43.
Harris, S.A., Maberly, S.C. and Abbott, R.J. (1992) Genetic variation within and between populations of Myriophyllum alterniflorum DC. Aquat. Bot. 44:1–21.
Harrison, S. and Hastings, A. (1996) Genetic and evolutionary consequences of metapopulation structure. Trends Ecol. Evol. 11:180–183.
Hebert, P.D.N. (1987) Genotypic characteristics of cyclic parthenogens and their obligately asexual derivatives. In: S.C. Stearns (ed.): The Evolution of Sex and Its Consequences. Birkhauser Verlag, Basel, pp 175–195.
Hebert, P.D.N., Ward, R.D. and Weider, L.J. (1988) Clonal-diversity patterns and breeding system variation in Daphnia pulex, an asexual-sexual complex. Evolution 42:147–159.
Hollingsworth, P.M., Gornall, R.J. and Preston, C.D. (1995) Genetic variability in British populations of Potamogeton coloratus (Potamogetonaceae).Plant Syst. Evol 197:71–85.
Howard, R.S. and Lively, C.M. (1994) Parasitism, mutation accumulation and the maintenance of sex. Nature 361:554–557.
Hughes, R.N. and Cancino, J.M. (1985) An ecological overview of cloning in Metazoa. In: J.B.C. Jackson, L.W. Buss and R.E. Cook (eds): Population Biology and Evolution of Clonal Organisms. Yale University Press, New Haven, Connecticut, pp 153–186.
Hurst, L.D. and Peck, J.R. (1996) Recent advances in understanding of the evolution and maintenance of sex. Trends Ecol Evol 11:46–52.
Hutchinson, J.E. (1975) A Treatise on Limnology, Vol 3 Limnological Botany. John Wiley and Sons, New York.
Jackson, J.B.C. (1985) Distribution and ecology of clonal and aclonal benthic invertebrates. In: J.B.C. Jackson, L.W. Buss and RE. Cook (eds): Population Bioloy and Evolution of Clonal Organisms. Yale University Press, New Haven, Connecticut, pp 297–355.
Jaenike, J. (1978) An hypothesis to account for the maintenance of sex within populations. Evol Theory 3:191–194.
Jonasson, P.M. (1963) The growth of Plumatella repens and P. fungosa (Bryozoa Ectoprocta) in relation to external factors in Danish eutrophic lakes. Oikos 14:121–137.
Jones, C.S., Okamura, B. and Noble, L.R. (1994) Parent and larval RAPD fingerprints reveal outcrossing in freshwater bryozoans. Mol Ecol 3:193–199.
Joo, G.-J., Ward, A.K. and Ward, G.M. (1992) Ecology of Pectinatella magnifica (Bryozoa) in an Alabama oxbow lake: Colony growth and association with algae. J. N. Am. Benthol. Soc. 11:324–333.
Judson, O.P. (1995) Preserving genes: A model of the maintenance of genetic variation in a metapopulation under frequency-dependent selection. Genet. Res. 65:175–191.
King, C.E. (1977) Genetics of reproduction, variation and adaptation in rotifers. Arch. Hydro-biol.Beih. 8:187–201.
King, C.E. and Zao, Y. (1987) Coexistence of rotifer (Brachionus plicatilis) clones in Soda Lake, Nevada. Hydrobiologia 147:57–64.
Lacourt, A.W. (1968) A monograph of the freshwater Bryozoa - Phylactolaemata. Zoologische Verhandelingen No. 93. Rijksmuseum von Nat. Hist., Leiden.
Ladle, R.J., Johnstone, R.A. and Judson, G.P. (1993) Coevolutionary dynamics of sex in a metapopulation: Escaping the Red Queen. Proc. R. Soc. Lond. B 253: 155–160.
Les, D.H. (1988) Breeding systems, population structure, and evolution in hydrophilous angio-sperms. Annls Miss. Bot. Gard. 75:819–835.
Levitan, D.R., Sewall, M.A. and Chia, F.-S. (1992) How distribution and abundance influence fertilization success in the sea urchin Strongylocentrotus franciscanus. Ecology 13:248–254.
Lively, C.M. (1992) Parthenogenesis in a freshwater snail: Reproductive assurance versus parasitic release. Evolution 46:907–913.
Lively, C.M. (1996) Through the Looking-Glass: Host-parasite coevolution and sex. Bioscience 46:107–114.
Lokker, C., Susko, D., Lovett Doust, L. and Lovett Doust, J. (1994) Population genetic structure of Vallisneria americana, a dioecious clonal macrophyte. Am. J. Bot. 81:1004–1012.
Lovett Doust, L. (1981) Population dynamics and local specialization in a clonal perennial (Ranunculus repens). I. The dynamics of ramets in contrasting habitats. J. Ecol. 69:743–755.
May, R.M. and Anderson, R.M. (1983) Epidemiology and genetics in the coevolution of parasites and hosts. Proc. R. Soc. Lond. B 219:281–313.
Mort, M.A. and Wolf, H.G. (1985) Enzyme variability in large-lake Daphnia populations. Heredity 55:27–36.
Mukai, H. (1982) Development of freshwater bryozoans. In: F.W. Harrison and R.R. Cowden (eds): Developmental Biology of Freshwater Invertebrates. Alan R. Liss, New York, pp 535–576.
Mukai, H., Karasawa, T. and Matsumoto, Y. (1979) Field and laboratory studies on the growth of Pectinatella gelatinosa Oka, a freshwater bryozoan. Sci. Rep. Fac. Educ. Gunma Univ. 28:27–57.
Okamura, B. (1994) Variation in local populations of the freshwater bryozoan Cristatella mucedo. In: P.J. Hayward, J.S. Ryland, and P.D. Taylor (eds): Biology and Paleobiology of Bryozoans. Olsen and Olsen, Fredensborg, Denmark, pp 145–149.
Okamura, B. (1996) Occurrence, prevalence and effects of the myxozoan Tetracapsula bryo-zoides Canning, Okamura et Curry parasitic in the freshwater bryozoan Cristatella mucedo Cuvier (Bryozoa, Phylactolaemata). Folia Parasitol. 43:262–266.
Okamura, B. and Hatton-Ellis, T. (1995) Population biology of bryozoans: Correlates of sessile, colonial life histories in freshwater habitats. Experientia 51:510–525.
Okamura, B., Jones, C.S. and Noble, L.R. (1993) Randomly amplified polymorphic DNA analysis of clonal population structure and geographic variation in a freshwater bryozoan. Proc. R. Soc. Lond. B 253:147–154.
Pennington, J.T. (1985) The ecology of fertilization of echinoid eggs: The consequences of sperm dilution, adult aggregation, and synchronous spawning. Biol. Bull. Woods Hole 183:417–430.
Piquot, Y., Saumitou-Laprade, P., Petit, D., Vernet, P. and Epplen, J.T. (1996) Genotypic diversity revealed by allozymes and oligonucleotide DNA fingerprinting in French populations of the aquatic macrophyte Sparganium erectum. Mol. Ecol. 5:251–258.
Pulliam, H.R. (1996) Sources and sinks: Empirical evidence and population consequences. In: O.E. Rhodes Jr., R.K. Chesser and M.H. Smith (eds): Population Dynamics in Ecological Space and Time. University of Chicago Press, Chicago, pp 45–69.
Rackham, O. (1986) The History of the Countryside. J.M. Dent and Sons, Ltd., London.
Rubin, J.A. (1987) Growth and refuge location in continuous, modular organisms: Experimental and computer simulation studies. Oecologia (Berlin) 72:46–51.
Schierwater, B., Ender, A., Schwenk, K., Spaak, P. and Streit, B. (1994) The evolutionary ecology of Daphnia. In: B. Schierwater, B. Streit, G.P. Wagner and R. DeSalle (eds): Molecular Ecology and Evolution: Approaches and Applications. Birkhauser Verlag, Basel, pp 495–508.
Schwenk, K. and Spaak, P. (1995) Evolutionary and ecological consequences of interspecific hybridization in cladocerans. Experientia 51:465–481.
Sculthorpe, C.D. (1967) The Biology of Aquatic Vascular Plants. Edward Arnold, London.
Siddall, M.E., Martin, D.S., Bridge, D., Desser, S.S. and Cone, D.K. (1995) The demise of a phylum of protists: Phylogeny of myxozoan and other parasitic Cnidaria. J. Parasitol. 81:961–987.
Silander, J.A. Jr. (1985) Microevolution in clonal plants. In: J.B.C. Jackson, L.W. Buss and R.E. Cook (eds): Population Biology and Evolution of Clonal Organisms. Yale University Press, New Haven, Connecticut, pp 107–152.
Smothers, J.F., Von Dohlen, C.D., Smith, L.H., Jr. and Spall, R.D. (1994) Molecular evidence that the myxozoan protists are metazoans. Science 265:1719–1721.
Stearns, S.C. (1987) Why sex evolved and the differences it makes.In.: S.C. Stearns (ed.): The Evolution of Sex and its Consequences. Birkhauser Verlag, Basel, pp 15–31.
Stewart, C.N. Jr. and Excoffier, L. (1996) Assessing population genetic structure and variability with RAPD data: Application to Vaccinium macrocarpon (American Cranberry). J. Evol. Biol. 9:153–171.
Titus, J.E. and Hoover, D.T. (1991) Toward predicting reproductive success in submersed freshwater angiosperms. Aquat. Bot. 41:111–136.
Tooby, J. (1982) Pathogens, polymorphism, and the evolution of sex. J. Theor. Biol. 97: 557–576.
Toriumi, M. (1974) Analysis of interspecific variation in Lophopodella carteri (Hyatt) from the taxonomical viewpoint. XXII. General considerations. Bull. Mar. Biol. Stn Asamushi 15:1–12.
Uotila, L. and Jokela, J. (1995) Variation in reproductive characteristics of colonies of the freshwater bryozoan Cristatella mucedo. Freshw. Biol. 34:513–522.
Vernon, J.G., Okamura, B., Jones, C.S. and Noble, L.R. (1996) Temporal patterns of clonality and parasitism in a population of freshwater bryozoans. Proc. R. Soc. Lond. B 263: 1313–1318.
Weider, L.J. (1989) Spatial heterogeneity and clonal structure in Arctic populations of apomic-tic Daphnia. Ecology 70:1405–1413.
Weider, L.J. (1993) Niche breadth and life history variation in a hybrid Daphnia complex. Ecology 74:935–943.
Welsh, J. and McClelland, M. (1990) Fingerprinting genomes using PCR with arbitrary primers. Nucl. Acids Res. 18:7213–7218.
Wesenberg-Lund, C. (1907) On the occurrence of Fredericella sultana Blumenbach and Paludi-cella ehrenbergi von Bened. in Greenland. Med. Gronl. 34:63–75.
Williams, J.G.K., Kubelik, A.R., Livak, K.J., Rafolski, J.A. and Tingey, S.V (1990) DNA polymorphisms amplified by arbitrary primers are useful as genetic markers. Nucl. Acids Res. 18:6531–6535.
Woss, E.R. (1994) Seasonal fluctuations of bryozoan populations in five water bodies with special emphasis on the life cycle of Plumatella fungosa (Pallas). In: P.J. Hayward, J.S. Ryland and P.D. Taylor (eds): Biology and Paleobiology of Bryozoans. Olsen and Olsen, Fredensborg, Denmark, pp 211–214.
Wolf, K. and Markiw, M.E. (1984) Biology contravenes taxonomy in the Myxozoa: New discoveries show alternation of invertebrate and vertebrate hosts. Science 225:1449–1452.
Wood, T.S. (1973) Colony development in species of Plumatella and Fredericella (Ectoprocta: Phylactolaemata). In: R.S. Boardman, A.H. Cheetham and W.A. Oliver, Jr. (eds): Development and Function of Animal Colonies through Time. Dowden, Hutchinson and Ross, Stroudsberg, Pennsylvania, pp 395–432.
Wood, T.S. (1989) Ectoproct bryozoans of Ohio. Bulletin of the Ohio Biological Survey New Series, Vol. 8, No. 2. The Ohio State University, Columbus, Ohio.
Wood, T.S. (1991) Bryozoans. In: J.H. Thorp and A.P. Covich (eds): Ecology and Classification of North American Freshwater Invertebrates. Academic Press, San Diego, pp 481–499.
Yokoyama, H., Ogawa, K. and Wakabayashi, H. (1993) Involvement of Branchiura sowerbyi (Oligochaeta: Annelida) in the transmission of Hoferellus carassii (Myxosporea: Myxozoa), the causative agent of kidney enlargement disease (KED) of goldfish Carassius auratus. Gyobyo Kenkyu 28:135–139.
Author information
Authors and Affiliations
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 1997 Springer Basel AG
About this chapter
Cite this chapter
Okamura, B. (1997). Genetic similarity, parasitism, and metapopulation structure in a freshwater bryozoan. In: Streit, B., Städler, T., Lively, C.M. (eds) Evolutionary Ecology of Freshwater Animals. EXS, vol 82. Birkhäuser, Basel. https://doi.org/10.1007/978-3-0348-8880-6_11
Download citation
DOI: https://doi.org/10.1007/978-3-0348-8880-6_11
Publisher Name: Birkhäuser, Basel
Print ISBN: 978-3-0348-9812-6
Online ISBN: 978-3-0348-8880-6
eBook Packages: Springer Book Archive