Skip to main content
Log in

Influence of contrasting larval developmental types upon the population-genetic structure of cheilostome bryozoans

  • Research Article
  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

For many sedentary or sessile benthic marine invertebrates the planktonic duration of the larval stage is believed to be a key determinant of the magnitude of genetic differences between populations. An obvious dichotomy in dispersal potential exists within cheilostome bryozoans that develop from either (1) a cyphonautes larva that spends several weeks in the plankton or (2) a brooded coronate larva that settles soon after release from the adult colony. This study characterises the pattern of variation at allozyme loci among British populations of four species of bryozoan—two species with cyphonautes and two with coronate larvae. There is some variation in the estimates of genetic differentiation among similarly separated populations that may be a consequence of non-equilibrium genetic conditions arising from sporadic migration, possibly through dispersal by rafting on macroalgae by mature colonies. Despite this, however, both the level of genetic differentiation between populations and the pattern of migrant exchange correlate with the larval developmental mode. Bryozoan species that brood coronate larvae show higher levels of genetic heterogeneity between populations and significant isolation by distance genetic structure while, by contrast, distance has little or no effect upon the amount of genetic differentiation among populations of bryozoans with cyphonautes larvae. For cheilostome bryozoans, therefore, it appears that genetic differentiation between populations is directly associated with the type of larval development. These data are discussed also with respect to levels of gene diversity and the geological pattern of cheilostome bryozoan species diversity.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Allcock AL, Brierly AS, Thorpe JP, Rodhouse PG (1997) Restricted gene flow and evolutionary divergence between geographically separated populations of the Antarctic octopus Pareledone turqueti. Mar Biol 129:97–102

    Article  Google Scholar 

  • Anil AC, Venkat K, Sawant SS, Dileepkumar M, Dhargalkar VK, Ramaiah N, Harkantra SN, Ansari ZA (2002) Marine bioinvasion: concern for ecology and shipping. Curr Sci 83:214–218

    Google Scholar 

  • Barnes DKA, Milner P (2005) Drifting plastic and its consequences for sessile organism dispersal in the Atlantic Ocean. Mar Biol 146:815–825

    Article  Google Scholar 

  • Bohonak AJ (1999) Dispersal, gene flow, and population structure. Q Rev Biol 74:21–45

    Article  PubMed  CAS  Google Scholar 

  • Burton RS (1983) Protein polymorphisms and genetic differentiation of marine invertebrate populations. Mar Biol Lett 4:193–206

    Google Scholar 

  • Burnett WJ, Benzie JAH, Beardmore JA, Ryland JS (1994) High genetic variability and patchiness in a common Great Barrier Reef zoanthid (Palythoa caesia). Mar Biol 121:153–160

    Article  Google Scholar 

  • Carlton JT, Geller JB (1993) Ecological roulette: the global transport of nonindigenous marine organisms. Science 261:78–82

    Article  Google Scholar 

  • Carlton JT, Hodder J (1995) Biogeography and dispersal of coastal marine organisms: experimental studies on a replica of a 16th-century sailing vessel. Mar Biol 121:721–730

    Article  Google Scholar 

  • Chapman AS, Scheibling RE, Chapman ARO (2002) Species introductions and changes in marine vegetation of Atlantic Canada. In: Claudi R, Nantel P, Muckle-Jeffs E (eds) Alien invasive species in Canada’s waters, wetlands and forests. Natural Resources Canada, Ottawa, pp 133–148

    Google Scholar 

  • Colson I, Hughes RN (2004) Rapid recovery o genetic diversity of dogwhelk (Nucella lapillus L.) populations after local extinction and recolonization contradicts predictions from life-history characteristics. Mol Ecol 13:2223–2233

    Article  PubMed  CAS  Google Scholar 

  • Craddock C, Lutz RA, Vrijenhoek RC (1997) Patterns of dispersal and larval development of archaeogastropod limpets at hydrothermal vents in the eastern Pacific. J Exp Mar Biol Ecol 210:37–51

    Article  Google Scholar 

  • Crisp DJ (1978) Genetic consequences of different reproductive strategies in marine invertebrates. In: Battaglia B, Beardmore JA (eds) Marine organisms: genetics, ecology and evolution. Plenum Press, New York, pp 257–273

    Google Scholar 

  • Edmands S, Potts DC (1997) Population genetic structure in brooding sea anemones (Epiactis spp.) with contrasting reproductive modes. Mar Biol 127:485–498

    Article  Google Scholar 

  • Falconer DS, Mackay TFC (1996) An introduction to quantitative genetics. Longman Group Ltd., Harlow

    Google Scholar 

  • Frankham R, Ballou JD, Briscoe DA (2002) Introduction to conservation genetics. Cambridge University Press, Cambridge

    Google Scholar 

  • Gilpin M (1991) The genetic effective size of a metapopulation. Biol J Linn Soc 42:165–175

    Article  Google Scholar 

  • Goldson AJ, Hughes RN, Gliddon CJ (2001) Population genetic consequences of larval dispersal mode and hydrography: a case study with bryozoans. Mar Biol 138:1037–1042

    Article  Google Scholar 

  • Goudet J (1994) FSTAT, a program for IBM PC compatibles to calculate Weir and Cockerham’s (1984) estimators of F-statistics. (version 1.2). Bangor University, privately distributed

  • Grant WS, Lang M (1991) Mode of larval development and genetic population structure in Nodolittorina africana knysnaensis (Prosobranchia: Littorinidae). Mar Biol 109:479–483

    Article  Google Scholar 

  • Grant WS, ds Silva-Tatley FM (1997) Lack of genetically-subdivided population structure in Bullia digitalis, a southern African marine gastropod with lecithotrophic development. Mar Biol 129:123–137

    Article  Google Scholar 

  • Hanski I (1999) Metapopulation ecology. Oxford University Press, New York

    Google Scholar 

  • Hayward PJ, Ryland JS (1979) British ascophoran bryozoans. In: Kermack DM, Barnes RSK (eds) Synopses of the British Fauna, new series. Plenum Press, London

    Google Scholar 

  • Hedgecock D (1986) Is gene flow from pelagic larval dispersal important in the adaptation and evolution and evolution of marine invertebrates? Bull Mar Sci 39:550–564

    Google Scholar 

  • Hellberg ME (1994) Relationships between inferred levels of gene-flow and geographic distance in a philopatric coral, Ballanophyllia elegans. Evolution 48:1829–1854

    Article  Google Scholar 

  • Hellberg ME (1995) Stepping-stone gene flow in the solitary coral Ballanophyllia elegans: equilibrium and nonequilibrium at different spatial scales. Mar Biol 123:573–581

    Article  Google Scholar 

  • Hellberg ME (1996) Dependence of gene flow on geographic distance in two solitary corals with different larval dispersal capabilities. Evolution 50:1167–1175

    Article  Google Scholar 

  • Hewitt GM (2000) The genetic legacy of the Quaternary ice ages. Nature 405:907–913

    Article  PubMed  CAS  Google Scholar 

  • Highsmith RC (1985) Floating and algal rafting as potential dispersal mechanisms in brooding invertebrates. Mar Ecol Prog Ser 25:169–175

    Article  Google Scholar 

  • Hilbish TJ (1996) Population genetics of marine species: the interaction of natural selection and historically differentiated populations. J Exp Mar Biol Ecol 200:67–83

    Article  Google Scholar 

  • Hoare K, Hughes RN, Goldson AJ (1999) Molecular genetic evidence for the prevalence of outcrossing in the hermaphroditic brooding bryozoan Celleporella hyalina. Mar Ecol Prog Ser 188:73–79

    Article  Google Scholar 

  • Hoskin MG (1997) Effects of contrasting modes of larval development on the genetic structures of populations of three species of prosobranch gastropods. Mar Biol 127:647–656

    Article  Google Scholar 

  • Hunt A (1993) Effects of contrasting patterns of larval dispersal on the genetic connectedness of local populations of two intertidal starfish, Patiriella calcar and P. exigua. Mar Ecol Prog Ser 92:179–186

    Article  Google Scholar 

  • Ingólfsson A (1995) Floating clumps of seaweed around Iceland: natural microcosms and a means of dispersal for shore fauna. Mar Biol 122:13–21

    Article  Google Scholar 

  • Jablonski D (1986) Larval ecology and macroevolution in marine invertebrates. Bull Mar Sci 39:565–587

    Google Scholar 

  • Jablonski D, Lutz RA (1983) Larval ecology of marine invertebrates: paleobiological implications. Biol Rev 58:21–89

    Article  Google Scholar 

  • Jablonski D, Roy K (2004) Geographical range and speciation in fossil and living molluscs. Proc R Soc Lond Biol Sci 270:401–406

    Article  Google Scholar 

  • Janson K (1987) Allozyme and shell variation in two marine snails (Littorina, Prosobranchia) with different dispersal abilities. Bio J Linn Soc 30:245–256

    Article  Google Scholar 

  • Johannesson K (1988) The paradox of Rockall: why is a brooding gastropod (Littorina saxatilis) more widespread than one having a planktonic larval dispersal stage (L. littorea)? Mar Biol 99:507–513

    Article  Google Scholar 

  • Johannesson K, Tatarenkov A (1997) Allozyme variation in a snail (Littorina saxatilis)—deconfounding the effects of microhabitat and gene flow. Evolution 51:402–409

    Article  CAS  Google Scholar 

  • Johnson MS, Black R (1996) Geographic cohesiveness versus associations with habitat: genetic subdivision of Bembicium vittatum Phillipi (Gastropoda: Littorinidae) in the Houtman Abrolhos Islands. Bio J Linn Soc 58:57–74

    Google Scholar 

  • Keough MJ, Chernoff H (1987) Dispersal and population variation in the bryozoan Bugula neritina. Ecology 68:199–210

    Article  Google Scholar 

  • Kimura M, Weiss GH (1964) The stepping stone model of population structure and the decrease of genetic correlation with distance. Genetics 49:561–576

    PubMed  CAS  Google Scholar 

  • Kyle CJ, Boulding EG (2000) Comparative population genetic structure of marine gastropods (Littorina spp.) with and without pelagic larval dispersal. Mar Biol 137:835–845

    Article  CAS  Google Scholar 

  • Lavery S, Moritz C, Fielder DR (1995) Changing patterns of population structure and gene flow at different spatial scales in Birgus latro (the coconut crab). Heredity 74:531–541

    Article  CAS  Google Scholar 

  • Malécot G (1948) Les mathématiques de l’hérédité. Masson, Paris

    Google Scholar 

  • Marko PB (2004) ‘What’s larvae got to do with it?’ Disparate patterns of post-glacial population structure in two benthic marine gastropods with identical dispersal potential. Mol Ecol 13:597–691

    Article  PubMed  CAS  Google Scholar 

  • McKinney FK, Jackson JBC (1991) Bryozoan evolution. University of Chicago Press, Chicago

    Google Scholar 

  • Murphy RW, Sites JW Jr, Buth DG, Haufler CH (1990) Proteins I: isozyme electrophoresis. In: Hillis DM, Moritz C (eds) Molecular systematics. Sinauer Associates Inc., Sunderland, pp 45–126

    Google Scholar 

  • Nishida M, Lucas JS (1988) Genetic differences between geographic populations of the Crown-of-thorns starfish throughout the Pacific region. Mar Biol 98:359–368

    Article  Google Scholar 

  • Palumbi SR (1994) Genetic divergence, reproductive isolation, and marine speciation. Ann Rev Ecol Syst 25:547–572

    Article  Google Scholar 

  • Porter JS, Ryland JS, Carvalho GR (2002) Micro- and macrogeographic genetic structure in bryozoans with different larval strategies. J Exp Mar Biol Ecol 272:119–130

    Article  CAS  Google Scholar 

  • Raymond M, Rousset F (1995) GENEPOP, Version 1.2. Population genetics software for exact tests and ecumenicisms. J Hered 86:249–249

    Google Scholar 

  • Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–225

    Article  Google Scholar 

  • Rousset F (1997) Genetic differentiation and estimation of gene flow from F-statistics under isolation by distance. Genetics 145:1219–1228

    PubMed  CAS  Google Scholar 

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

    Google Scholar 

  • Ryland JS, Hayward PJ (1977) British anascan bryozoans. In: Kermack DM, Barnes RSK (eds) Synopses of the British Fauna, new series. Plenum Press, London

    Google Scholar 

  • Scheltema RS (1978) On the relationship between dispersal of pelagic veliger larvae and the evolution of marine prosobranch gastropods. In: Battaglia B, Beardmore JA (eds) Marine organisms: genetics, ecology and evolution. Plenum Press, New York, pp 303–322

    Google Scholar 

  • Schopf TJM (1973) Population genetics of Ectroprocts: In: Larwood GP (ed) Living and fossil Bryozoa. Academic, London, pp 585–592

    Google Scholar 

  • Schopf TJM (1977) Population genetics of bryozoans. In: Woollacott RM, Zimmer RL (eds) Biology of bryozoans. Academic, New York, pp 459–486

    Google Scholar 

  • Schwaninger HR (1999) Population structure of the widely dispersing marine bryozoan Membranipora membranacea (Cheilostomata): implications for population history, biogeography and taxonomy. Mar Biol 135:411–423

    Article  Google Scholar 

  • Shaw PW, Arkhipkin AI, Al-Khairulla H (2004) Genetic structuring of Patagonian toothfish populations in the Southwest Atlantic Ocean: the effect of the Antarctic Polar Front and deep-water troughs as barriers to genetic exchange. Mol Ecol 13:3293–3303

    Article  PubMed  CAS  Google Scholar 

  • Shapiro DF (1992) Intercolony coordination of zooid behaviour and a new class of pore plates in a marine bryozoan. Bil Bull 182:221–230

    Google Scholar 

  • Slatkin M (1993) Isolation by distance in equilibrium and non-equilibrium populations. Evolution 47:264–279

    Article  Google Scholar 

  • Stevens LM, Gregory MR, Foster BA (1996) Fouling Bryozoa on pelagic and moored plastics from northern New Zealand. In: Gordon DP, Smith AM, Grant-Mackie JA (eds) Bryozoans in space and time. NIWA, Wellington, pp 321–340

    Google Scholar 

  • Tatarenkov A, Johannesson K (1994) Habitat related allozyme variation on a microgeographic scale in a marine snail Littorina mariae (Prosobranchia, Littorinacea). Biol J Linn Soc 53:105–125

    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 (1994) An early cheilostome bryozoan from the Upper Jurassic of Yemen. Neues Jahrbuch für Geologie und Paläontologie. Abhandlungen 191:331–344

    Google Scholar 

  • Watts PC, Thorpe JP, Taylor PD (1998) Natural and anthropogenic dispersal mechanisms in the marine environment: a study using cheilostome Bryozoa. Phil Trans R Soc Lond B Biol Sci 353:453–464

    Article  Google Scholar 

  • Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370

    Article  Google Scholar 

  • Wright S (1931) Evolution in Mendelian populations. Genetics 16:97–159

    PubMed  CAS  Google Scholar 

  • Wright S (1943) Isolation by distance. Genetics 16:97–159

    Google Scholar 

  • Wright S (1951) The genetical structure of populations. Ann Eug 15:323–354

    Google Scholar 

  • Yoshioka PM (1982) Role of planktonic and benthic factors in the population dynamics of the bryozoan Membranipora membranacea. Ecology 63:457–468

    Article  Google Scholar 

Download references

Acknowledgements

This work was funded by the NERC. Louise Allcock and Sarah Reay assisted with the some sampling throughout the UK and John Bishop provided samples from Plymouth.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Phillip C. Watts.

Additional information

Communicated by O. Kinne, Oldendorf/Luhe

Rights and permissions

Reprints and permissions

About this article

Cite this article

Watts, P.C., Thorpe, J.P. Influence of contrasting larval developmental types upon the population-genetic structure of cheilostome bryozoans. Mar Biol 149, 1093–1101 (2006). https://doi.org/10.1007/s00227-006-0288-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00227-006-0288-2

Keywords

Navigation