Skip to main content
SpringerLink
Log in

Microscale genetic differentiation in a sessile invertebrate with cloned larvae: investigating the role of polyembryony

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

Abstract

Microscale genetic differentiation of sessile organisms can arise from restricted dispersal of sexual propagules, leading to isolation by distance, or from localised cloning. Cyclostome bryozoans offer a possible combination of both: the localised transfer of spermatozoa between mates with limited dispersal of the resulting larvae, in association with the splitting of each sexually produced embryo into many clonal copies (polyembryony). We spatially sampled 157 colonies of Crisia denticulata from subtidal rock overhangs from one shore in Devon, England at a geographic scale of ca. 0.05 to 130 m plus a further 21 colonies from Pembrokeshire, Wales as an outgroup. Analysis of molecular variance (AMOVA) revealed that the majority (67%) of genetic variation was distributed among individuals within single rock overhangs, with only 16% of variation among different overhangs within each shore and 17% of variation between the ingroup and outgroup shores. Despite local genetic variation, pairwise genetic similarity analysed by spatial autocorrelation was greatest at the smallest inter-individual distance we tested (5 cm) and remained significant and positive across generally within-overhang comparisons (<4 m). Spatial autocorrelation and AMOVA analyses both indicated that patches of C. denticulata located on different rock overhangs tended to be genetically distinct, with the switch from positive to negative autocorrelation, which is often considered to be the distance within which individuals reproduce with their close relatives or the radius of a patch, occurring at the 4–8 m distance class. Rerunning analyses with twenty data sets that only included one individual of each multilocus genotype (n = 97) or the single data set that contained just the unique genotypes (n = 67) revealed that the presence of repeat genotypes had an impact on genetic structuring (PhiPT values were reduced when shared genotypes were removed from the dataset) but that it was not great and only statistically evident at distances between individuals of 1–2 m. Comparisons to a further 20 randomisations of the data set that were performed irrespective of genotype (n = 97) suggested that this conclusion is not an artefact of reduced sample size. A resampling procedure using kinship coefficients, implemented by the software package GENCLONE gave broadly similar results but the greater statistical power allowed small but significant impacts of repeat genotypes on genetic structure to be also detected at 0.125–0.5 and 4–16 m. Although we predict that a proportion of the repeat multilocus genotypes are shared by chance, such generally within-overhang distances may represent a common distance of cloned larval dispersal. These results suggests that closely situated potential mates include a significant proportion of the available genetic diversity within a population, making it unlikely that, as previously hypothesised, the potential disadvantage of producing clonal broods through polyembryony is offset by genetic uniformity within the mating neighbourhood. We also report an error in the published primer note of Craig et al. (Mol Ecol Notes 1:281–282, 2001): loci Cd5 and Cd6 appear to be the same microsatellite.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Alberto F, Gouveia L, Arnaud-Haond S Pérez-Lloréns JL, Duarte CM, Serrão EA (2005) Spatial genetic structure, neighbourhood size and clonal subrange in seagrass (Cymodocea nodosa) populations. Mol Ecol 14:2669–2681

    Article  CAS  PubMed  Google Scholar 

  • Arnaud-Haond S, Belkhir K (2007) Genclone: a computer program to analyse genotypic data, test for clonality and describe spatial clonal organization. Mol Ecol Notes 7(1):15–17

    Article  CAS  Google Scholar 

  • Arnaud-Haond S, Alberto F, Procaccini G, Serrao EA, Duarte CM (2005) Assessing genetic diversity in clonal organisms: low diversity or low resolution? Combining power and cost efficiency in selecting markers. J Heredity 96:1–8

    Article  Google Scholar 

  • Bell G (1982) The masterpiece of nature. Croom Helm, London

    Google Scholar 

  • Bishop JDD (1998) Fertilization in the sea: are the hazards of broadcast spawning avoided when free-spawned sperm fertilize retained eggs? Proc Roy Soc Lond Ser B 265:725–731

    Article  Google Scholar 

  • Boardman RS, McKinney FK, Taylor PD (1992) Morphology, anatomy, and systematics of the Cinctiporidae, new family (Bryozoa: Stenolaemata). Smithsonian Contrib Paleobiol 70:1–81

    Google Scholar 

  • Borg F (1926) Studies on recent cyclostomatous Bryozoa. Zoologiska Bidrag från Uppsala 10:181–507

    Google Scholar 

  • Burnett WJ, Benzie JAH, Beardmore JA, Ryland JS (1995) Patterns of genetic subdivision in populations of a clonal cnidarian, Zoanthus coppingeri, from the Great Barrier Reef. Marine Biol 122:665–673

    Article  Google Scholar 

  • Clarke KR, Gorley RN (2001) PRIMER v5: User Manual/Tutorial. PRIMER-E, Plymouth

  • Craig SF, D’Amato ME, Harley M, Bishop J, Hughes R, Carvalho GR (2001) Isolation and characterization of microsatellites in the bryozoan Crisia denticulata. Mol Ecol Notes 1:281–282

    Article  CAS  Google Scholar 

  • Craig SF, Slobodkin LB, Wray G (1995) The paradox of polyembryony. Trends Ecol Evol 10:371–372

    Article  CAS  PubMed  Google Scholar 

  • Craig SF, Slobodkin LB, Wray GA, Biermann CH (1997) The ‘paradox’ of polyembryony: a review of the cases and a hypothesis for its evolution. Evol Ecol 11:127–143

    Article  Google Scholar 

  • Eaves AA, Palmer AR (2003) Widespread cloning in echinoderm larvae. Nature 425:146–146

    Article  CAS  PubMed  Google Scholar 

  • Engel CR, Destombe C, Valero M (2004) Mating system and gene flow in the red seaweed Gracilaria gracilis: effect of haploid-diploid life history and intertidal rocky shore landscape on finescale genetic structure. Heredity 92:289–298

    Article  CAS  PubMed  Google Scholar 

  • Filonova LH, von Arnold S, Daniel G, Bozhkov PV (2002) Programmed cell death eliminates all but one embryo in a polyembryonic plant seed. Cell Death Differ 9:1057–1062

    Article  CAS  PubMed  Google Scholar 

  • Giron D, Dunn DW, Hardy ICW, Strand MR (2004) Aggression by polyembryonic wasp soldiers correlates with kinship but not resource competition. Nature 430:676–679

    Article  CAS  PubMed  Google Scholar 

  • Goddard MR, Charles H, Godfray J, Burt A (2005) Sex increases the efficacy of natural selection in experimental yeast populations. Nature 434:636–640

    Article  CAS  PubMed  Google Scholar 

  • Gregorius H-R (2005) Testing for clonal propagation. Heredity 94:173–179

    Article  PubMed  Google Scholar 

  • Hämmerli A, Reusch TBH (2003) Genetic neighbourhood of clone structures in eelgrass meadows quantified by spatial autocorrelation of microsatellite markers. Heredity 91:448–455

    Article  PubMed  Google Scholar 

  • Harmelin J-G (1974) Les bryozoaires cyclostomes de Méditerranée, écologie et systématique. PhD thesis. Université d’Aix-Marseille. 365pp

  • Harmer SF (1893) On the occurrence of embryonic fission in cyclostomatous Polyzoa. Q J Microsc Sci 34:199–241

    Google Scholar 

  • Hellberg ME (1995) Relationships between inferred levels of gene flow and geographic distance in a philopatric coral, Balanophyllia elegans. Evolution 49:398–398

    Article  Google Scholar 

  • Hughes RN (1989) A functional biology of clonal animals. Chapman and Hall, London

    Google Scholar 

  • Hughes RN, D’Amato ME, Bishop JDD, Carvalho GR, Craig SF, Hansson LJ, Harley MA, Pemberton AJ (2005) Paradoxical polyembryony? Embryonic cloning in an ancient order of marine bryozoans. Biol Lett 1:178–180

    Article  PubMed  PubMed Central  Google Scholar 

  • Hurst LD, Peck JR (1996) Recent advances in understanding of the evolution and maintenance of sex. Trends Ecol Evol 11:46–52

    Article  CAS  PubMed  Google Scholar 

  • Jackson JBC (1986) Modes of dispersal of clonal benthic invertebrates: consequences for species’ distributions and genetic structure of local populations. Bull Marine Sci 39:588–606

    Google Scholar 

  • Johnson SL, Yund PO (2004) Remarkable longevity of dilute sperm in a free-spawning colonial ascidian. Biol Bull 206:144–151

    Article  PubMed  Google Scholar 

  • Knowlton N, Jackson JBC (1993) Inbreeding and outbreeding in marine invertebrates. In: Thornhill NW (ed) The natural history of inbreeding and outbreeding. Theoretical and empirical perspectives. The University of Chicago Press, Chicago, pp 200–249

  • Krutovskii KV, Politov DV (1995) Allozyme evidence for polyzygotic polyembryony in Siberian stone pine (Pinussibirica dutour). Theor Appl Genet 90:811–818

    Article  CAS  PubMed  Google Scholar 

  • Lasker HR (2006) High fertilization success in a surface-brooding Caribbean gorgonian. Biol Bull 210:10–17

    Article  PubMed  Google Scholar 

  • Levin LA (1990) A review of methods for labelling and tracking marine invertebrate larvae. Ophelia 32:115–144

    Article  Google Scholar 

  • Loiselle BA, Sork VL, Nason J, Graham C (1995) Spatial genetic structure of a tropical understorey shrub, Psychotria officinalis (Rubiaceae). Am J Bot 82:1420–1425

    Article  Google Scholar 

  • Mantel N (1967) The detection of disease clustering and a generalized regression approach. Cancer Res 27:209–220

    CAS  PubMed  Google Scholar 

  • McFadden CS (1997) Contributions of sexual and asexual reproduction to population structure in the clonal soft coral, Alcyonium rudyi. Evolution 51:112–126

    Article  PubMed  Google Scholar 

  • McFadden CS, Aydin KY (1996) Spatial autocorrelation analysis of small-scale genetic structure in a clonal soft coral with limited larval dispersal. Marine Biol 126:215–224

    Article  Google Scholar 

  • McKinney FK (1981) Intercolony fusion suggests polyembryony in paleozoic fenestrate bryozoans. Paleobiology 7:247–251

    Article  Google Scholar 

  • Michalakis Y, Excoffier L (1996) A generic estimation of population subdivision using distances between alleles with special reference for microsatellite loci. Genetics 142:1061–1064

    CAS  PubMed  PubMed Central  Google Scholar 

  • Migliaccio M, De Martino F, Silvestre F, Procaccini G (2005) Meadow-scale genetic structure in Posidonia oceanica. Marine Ecol Prog Ser 304:55–65

    Article  CAS  Google Scholar 

  • Morgan SG (1995) Life and death in the plankton: larval mortality and adaptation. In: McEdward L (ed) Ecology of marine invertebrate larvae. CRC, Boca Raton, pp 279–321

    Google Scholar 

  • Montalvo AM, Conard SG, Conkle MT, Hodgskiss PD (1997) Population structure, genetic diversity, and clone formation in Quercus shrysolepsis (Fagaceae). Am J Bot 84:1553–1564

    Article  CAS  PubMed  Google Scholar 

  • Parks JC, Werth CR (1993) A study of spatial features of clones in a population of bracken fern, Pteridium aquilinum (Dennstaedtiaceae). Am J Bot 80:537–544

    Article  PubMed  Google Scholar 

  • Peakall R, Ruibal M, Lindenmayer DB (2003) Spatial autocorrelation analysis offers new insights into gene flow in the Australian bush rat, Rattus fuscipes. Evolution 57:1182–1195

    Article  PubMed  Google Scholar 

  • Peakall R, Smouse PE (2006) GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295

    Article  Google Scholar 

  • Peakall R, Smouse PE, Huff DR (1995) Evolutionary implications of allozyme and RAPD variation in diploid populations of dioecious buffalograss Buchloe dactyloides. Mol Ecol 4:135–147

    Article  CAS  Google Scholar 

  • Pemberton AJ, Hughes RN, Manriquez PH, Bishop JDD (2003) Efficient utilisation of very dilute aquatic sperm: sperm competition may be more likely than sperm limitation when eggs are retained. Proc Roy Soc Lond Biol Lett 270:S223–S226

    Article  Google Scholar 

  • Phillippi A, Hamann E, Yund PO (2004) Fertilization in an egg-brooding colonial ascidian does not vary with population density. Biol Bull 206:152–160

    Article  PubMed  Google Scholar 

  • Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Heredity 86:248–249

    Article  Google Scholar 

  • Reusch TBH, Hukriede W, Stam WT, Olsen JL (1999) Differentiating between clonal growth and limited gene flow using spatial autocorrelation of microsatellites. Heredity 83:120–126

    Article  PubMed  Google Scholar 

  • Ritland K (1996) Estimators for pairwise relatedness and individual inbreeding coefficients. Genet Res 67:175–185

    Article  Google Scholar 

  • Robertson A (1903) Embryology and embryonic fission in the genus Crisia. Univ Calif Publ Zool 1:115–156

    Google Scholar 

  • Rogers DL, Millar CI, Westfall RD (1999) Fine-scale genetic structure of whitebark pine (Pinus albicaulis): associations with watershed and growth form. Evolution 53:74–90

    PubMed  Google Scholar 

  • Rousset F, Raymond M (1995) Testing heterozygote excess and deficiency. Genetics 140:1413–1419

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ryland JS (1970) Bryozoans. Hutchinson and Co, London

    Google Scholar 

  • Ryland JS (1996) Polyembryony ‘paradox’: the case of cyclostomate bryozoa. Trends Ecol Evol 11:26

    Article  CAS  PubMed  Google Scholar 

  • Ryland JS (2000) Gonozooid placement and branching patterns in some species of Crisia (Cyclostomatida). In: Proceedings of the 11th International Bryozoology Association Conference, pp 343–354

  • Schmidt PS, Rand DM (1999) Intertidal microhabitat and selection at Mpi: interlocus contrasts in the northern acorn barnacle, Semibalanus balanoides. Evolution 53:135–146

    PubMed  Google Scholar 

  • Silen L (1972) Fertilization in the Bryozoa. Ophelia 10:27–34

    Article  Google Scholar 

  • Smouse PE, Peakall R (1999) Spatial autocorrelation analysis of individual multiallele and multilocus genetic structure. Heredity 82:561–573

    Article  PubMed  Google Scholar 

  • Temkin MH (1994) Gamete spawning and fertilization in the gymnolaemate bryozoan Membranipora membranacea. Biol Bull 187:143–155

    Article  CAS  PubMed  Google Scholar 

  • Vekemans X, Hardy OJ (2004) New insights from fine-scale spatial genetic structure analyses in plant populations. Mol Ecol 13:921–935

    Article  CAS  PubMed  Google Scholar 

  • Young AG, Hill JM, Murray BG, Peakall R (2002) Breeding system, genetic diversity and clonal structure in the sub-alpine forb Rutidosis leiolepis F. Muell. (Asteraceae). Biol Conserv 106:71–78

    Article  Google Scholar 

  • Yund PO (2000) How severe is sperm limitation in natural populations of marine free-spawners? Trends Ecol Evol 15:514–517

    Article  Google Scholar 

  • Yund PO, O’Neil PG (2000) Microgeographic genetic differentiation in a colonial ascidian (Botryllus schlosseri) population. Marine Biol 137:583–588

    Article  Google Scholar 

  • Waits LP, Luikart G, Taberlet P (2001) Estimating the probability of identity among genotypes in natural populations: cautions and guidelines. Mol Ecol 10:249–256

    Article  CAS  PubMed  Google Scholar 

  • Wright JT, Zuccarello GC, Steinberg PD (2000) Genetic structure of the subtidal red alga Delisea pulchra. Marine Biol 136:439–448

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The UK Natural Environment Research Council provided research grants (AJP, NER/M/S/2001/00112; RNH and SFC, GR9/03614) and recurrent grant-in-aid to the Marine Biological Association to fund this work. AJP was supported by the Leverhulme Trust. LJH received supplementary funding through Magn. Bergvalls Stiftelse. AJP was hosted by Ralph Smith, University of Waterloo during preparation of the manuscript. We thank John Ryland and anonymous reviewers for useful comments that improved the manuscript. All experiments comply with UK law.

Author information

Author notes

  1. Lars J. Hansson

    Present address: SMHI, Nya Varvet 31, 426 71, Västra Frölunda, Sweden

  2. Sean F. Craig

    Present address: Department of Biological Sciences, Humboldt State University, Arcata, CA, 95521, USA

Authors and Affiliations

  1. The Laboratory, Marine Biological Association of the U.K, Citadel Hill, Plymouth, PL1 2PB, UK

    Andrew J. Pemberton, Lars J. Hansson & John D. D. Bishop

  2. School of Biological Sciences, University of Wales, Bangor, Gwynedd, LL57 2UW, UK

    Sean F. Craig & Roger N. Hughes

  3. School of Biological Sciences, University of Plymouth, Drake Circus, Plymouth, PL4 8AA, UK

    John D. D. Bishop

  4. Zoological Museum of the University of Zurich, Winterthurerstrasse 190, 8057, Zurich, Switzerland

    Andrew J. Pemberton

Authors
  1. Andrew J. Pemberton
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Lars J. Hansson
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Sean F. Craig
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Roger N. Hughes
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. John D. D. Bishop
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Andrew J. Pemberton.

Additional information

Communicated by M. Wahl.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Electronic supplementary material (DOC 1.8 MB)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Pemberton, A.J., Hansson, L.J., Craig, S.F. et al. Microscale genetic differentiation in a sessile invertebrate with cloned larvae: investigating the role of polyembryony. Mar Biol 153, 71–82 (2007). https://doi.org/10.1007/s00227-007-0785-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00227-007-0785-y

Keywords

Search

Navigation