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Chaotic genetic patchiness and high relatedness of a poecilogonous polychaete in a heterogeneous estuarine landscape

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Abstract

The genetic structure of benthic marine invertebrates is often described as “chaotic” when genetic structure cannot be explained and barriers to dispersal and gene flow cannot be identified. Here, chaotic patterns of genetic structure for the polychaete Pygospio elegans (Claparède) sampled at 16 locations from the heterogeneous Isefjord–Roskilde Fjord estuary complex in Denmark were found. There was no isolation by distance, and the geography of the estuary complex did not seem to pose a barrier to dispersal and gene flow in this species. We investigated whether characteristics of the environment could be related to the genetic structure and possibly restrict gene flow in this species. Additionally, since P. elegans is poecilogonous, producing larvae with different pelagic developmental periods, we investigated whether observed developmental modes in the samples might clarify the genetic patterns. None of the tested factors explained the population genetic structure. However, a high degree of relatedness among individuals in almost all samples was found. Samples with a larger percentage of young individuals had more related individuals, suggesting that different cohorts could be comprised of individuals with different degrees of relatedness. Relatedness within a site could be increased by limited larval dispersal, collective dispersal of related larvae, sweepstakes reproductive success, or asexual reproduction, but distinguishing between these requires further study. Using a “seascape genetics” approach allowed us to investigate some of the numerous potential factors that could influence population genetic structure in a poecilogonous species.

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References

  • Anger K (1975) On the sewage pollution on inshore benthic communities in the South Kiel Bay. Part 2. Quantitative studies on community structure. Helgol Meeresun 27:408–438

    Article  Google Scholar 

  • Anger V (1984) Reproduction in Pygospio elegans (Spionidae) in relation to its geographical origin and to environmental conditions: a preliminary report. Forts Zool 29:45–51

    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 7:15–17

    Article  CAS  Google Scholar 

  • Banks SC, Piggott MP, Williamson JE, Bove U, Holbrook NJ, Beheregaray LB (2007) Oceanic variability and coastal topography shape genetic structure in a long-dispersing sea urchin. Ecology 88:3055–3064

    Article  Google Scholar 

  • Barber PH, Palumbi SR, Erdmann MV, Moosa MK (2002) Sharp genetic breaks among populations of Haptosquilla pulchella (Stomatopoda) indicate limits to larval transport: patterns, causes, and consequences. Mol Ecol 11:659–674

    Article  CAS  Google Scholar 

  • Becquet V, Lasota R, Pante E, Sokolowski A, Wolowicz M, Garcia P (2013) Effects of fine-scale environmental heterogeneity on local genetic structure in Macoma balthica from the Gulf of Gdañsk (southern Baltic Sea). Hydrobiologia 714:61–70

    Article  CAS  Google Scholar 

  • Bekkevold D, Andre C, Dahlgren TG, Clausen LAW, Torstensen E, Mosegaard H, Carvalho GR, Christensen TB, Norlinder E, Ruzzante DE (2005) Environmental correlates of population differentiation in Atlantic herring. Evolution 59:2656–2668

    Article  Google Scholar 

  • Bendtsen J, Hansen JLS (2013) A model of life cycle, connectivity and population stability of benthic macro-invertebrates in the North Sea/Baltic Sea transition zone. Ecol Model 267:54–65

    Article  Google Scholar 

  • Beukema JJ, Flach EC, Dekker R, Starink M (1999) A long-term study of the recovery of the macrozoobenthos on large defaunated plots on a tidal flat in the Wadden Sea. J Sea Res 42(3):235–254

    Article  Google Scholar 

  • Bierne N, Borsa P, Daguin C, Jollivet D, Viard F, Bonhomme F, David P (2003) Introgression patterns in the mosaic hybrid zone between Mytilus edulis and M. galloprovincialis. Mol Ecol 12:447–461

    Article  CAS  Google Scholar 

  • Bilton DT, Paula J, Bishop JDD (2002) Dispersal, genetic differentiation and speciation in estuarine organisms. Estuar Coast Shelf Sci 55:937–952

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Bolam SG (2004) Population structure and reproductive biology of Pygospio elegans (Polychaeta: Spionidae) on an intertidal sandflat, Firth of Forth, Scotland. Invertebr Biol 123:260–268

    Article  Google Scholar 

  • Bongaerts P, Riginos C, Ridgway T, Sampayo E, van Oppen M, Englebert N, Vermeulen F, Hoegh-Guldberg O (2010) Genetic divergence across habitats in the widespread coral Seriatopora hystrix and its associated Symbiodinium. PLoS One 5:e10871

    Article  Google Scholar 

  • Bonsdorff E (1992) Drifting algae and zoobenthos—effects on settling and community structure. Neth J Sea Res 30:57–62

    Article  Google Scholar 

  • Broquet T, Viard F, Yearsley JM (2013) Genetic drift and collective dispersal can result in chaotic genetic patchiness. Evolution 67(6):1660–1675

    Article  Google Scholar 

  • Buonaccorsi VP, Kimbrell CA, Lynn EA, Vetter RD (2002) Population structure of copper rockfish (Sebastes caurinus) reflects postglacial colonization and contemporary patterns of larval dispersal. Can J Fish Aquat Sci 59:1374–1384

    Article  CAS  Google Scholar 

  • Burford MO, Larson RJ (2007) Genetic heterogeneity in a single year-class from a panmictic population of adult blue rock fish (Sebastes mystinus). Mar Biol 151:451–465

    Article  Google Scholar 

  • Calderón I, Palacín C, Turon X (2009) Microsatellite markers reveal shallow genetic differentiation between cohorts of the common sea urchin Paracentrotus lividus (Lamarck) in northwest Mediterranean. Mol Ecol 18:3036–3049

    Article  Google Scholar 

  • Chapuis MP, Estoup A (2007) Microsatellite null alleles and estimation of population differentiation. Mol Biol Evol 24:621–631

    Article  CAS  Google Scholar 

  • Cohen RA, Pechenik JA (1999) Relationship between sediment organic content, metamorphosis, and postlarval performance in the deposit-feeding polychaete Capitella sp. I. J Exp Mar Biol Ecol 240:1–18

    Article  Google Scholar 

  • Dionne M, Caron F, Dodson JJ, Bernatchez L (2008) Landscape genetics and hierarchical genetic structure in Atlantic salmon: the interaction of gene flow and local adaptation. Mol Ecol 17:2382–2396

    Article  CAS  Google Scholar 

  • Duchene JC (2004) Early recognition of sediment during settlement of Eupolymnia nebulosa (Polychaeta: Terebellidae) larvae. Mar Biol 145:79–85

    Article  Google Scholar 

  • Earl DA, vonHoldt BM (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 2:359–361

    Article  Google Scholar 

  • Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620

    Article  CAS  Google Scholar 

  • Excoffier L, Lischer EHL (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10:564–567

    Article  Google Scholar 

  • Foll M, Gaggiotti OE (2006) Identifying the environmental factors that determine the genetic structure of populations. Genetics 174:875–891

    Article  CAS  Google Scholar 

  • Gaggiotti OE, Bekkevold D, Jørgensen HBH, Foll M, Carvalho GR, André C, Ruzzante DE (2009) Disentangling the effects of evolutionary, demographic, and environmental factors influencing genetic structure of natural populations: Atlantic herring as a case study. Evolution 63–11:2939–2951

    Article  Google Scholar 

  • Galarza JA, Carreras-Carbonell J, Macpherson E et al (2009) The influence of oceanographic fronts and early-life-history traits on connectivity among littoral fish species. Proc Natl Acad Sci USA 106:1473–1478

    Article  CAS  Google Scholar 

  • Galindo HM, Olson DB, Palumbi SR (2006) Seascape genetics: a coupled oceanographic-genetic model predicts population structure of Caribbean corals. Curr Biol 16:1622–1626

    Article  CAS  Google Scholar 

  • Gerlach G, Jueterbock A, Kraemer P, Deppermann J, Harmand P (2010) Calculations of population differentiation based on G(ST) and D: forget G(ST) but not all of statistics! Mol Ecol 19:3845–3852

    Article  Google Scholar 

  • Goudet J (2001) FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3). http://www.unil.ch/izea/softwares/fstat.html

  • Gudmundsson H (1985) Life history patterns of polychaete species of the family Spionidae. J Mar Bio Assoc UK 65:93–111

    Article  Google Scholar 

  • Hardege JD, Bentley MG, Snape L (1998) Sediment selection by juvenile Arenicola marina. Mar Ecol Prog Ser 166:187–195

    Article  Google Scholar 

  • Hedgecock D, Pudovkin AI (2011) Sweepstakes reproductive success in highly fecund marine fish and shellfish: a review and commentary. Bull Mar Sci 87(4):971–1002

    Article  Google Scholar 

  • Hedgecock D, Launey S, Pudovkin AI, Naciri Y, Lapègue S, Bonhomme F (2007) Small effective number of parents (Nb) inferred for a naturally spawned cohort of juvenile European flat oysters Ostrea edulis. Mar Biol 150(6):1173–1182

    Article  Google Scholar 

  • Hogan JD, Thiessen RJ, Heath DD (2010) Variability in connectivity indicated by chaotic genetic patchiness within and among populations of a marine fish. Mar Ecol Prog Ser 417:263–275

    Article  Google Scholar 

  • Iacchei M, Ben-Horin T, Selkoe KA, Bird CE, García-Rodríguez FJ, Toonen RJ (2013) Combined analyses of kinship and FST suggest potential drivers of chaotic genetic patchiness in high gene-flow populations. Mol Ecol 22(13):3476–3494

    Article  Google Scholar 

  • Johannesson K, André C (2006) Life on the margin: genetic isolation and diversity loss in a peripheral marine ecosystem, the Baltic Sea. Mol Ecol 15:2013–2029

    Article  CAS  Google Scholar 

  • Johnson MS, Black R (1982) Chaotic genetic patchiness in an intertidal limpet, Siphonaria sp. Mar Biol 70:157–164

    Article  Google Scholar 

  • Johnson MS, Holborn K, Black R (1993) Fine-scale patchiness and genetic heterogeneity of recruits of the corallivorous gastropod Drupella cornus. Mar Biol 117:91–96

    Article  Google Scholar 

  • Jolly MT, Thiébaut E, Guyard P, Gentil F, Jollivet D (2014) Meso-scale hydrodynamic and reproductive asynchrony affects the source–sink metapopulation structure of the coastal polychaete Pectinaria koreni. Mar Biol 161:367–382

    Article  Google Scholar 

  • Jost L (2008) GST and its relatives do not measure differentiation. Mol Ecol 17:4015–4026

    Article  Google Scholar 

  • Kalinowski ST (2005) HP-RARE 1.0: a computer program for performing rarefaction on measures of allelic richness. Mol Ecol Notes 5:187–189

    Article  CAS  Google Scholar 

  • Kalinowski ST, Wagner AP, Taper ML (2006) ML-RELATE: a computer program for maximum likelihood estimation of relatedness and relationship. Mol Ecol Notes 6(2):576–579

    Article  CAS  Google Scholar 

  • Kelly RP, Palumbi SR (2010) Genetic structure among 50 species of the Northeastern Pacific rocky intertidal community. PLoS One 5(1):e8594

    Article  Google Scholar 

  • Kesäniemi JE, Boström C, Knott KE (2012a) New genetic markers reveal population genetic structure at different spatial scales in the opportunistic polychaete Pygospio elegans. Hydrobiologia 691:223–231

    Article  Google Scholar 

  • Kesäniemi JE, Geuverink E, Knott KE (2012b) Polymorphism in developmental mode and its effect on population genetic structure of a spionid polychaete, Pygospio elegans. Integr Comp Biol 52(1):181–196

    Article  Google Scholar 

  • Kesäniemi JE, Rawson PD, Lindsay SM, Knott KE (2012c) Phylogenetic analysis of cryptic speciation in the polychaete Pygospio elegans. Ecol Evol 2(5):994–1007

    Article  Google Scholar 

  • Kesäniemi JE, Mustonen M, Boström C, Hansen BW, Knott KE (2014) Temporal genetic structure in a poecilogonous polychaete: the interplay of developmental mode and environmental stochasticity. BMC Evol Biol 14:12

    Article  Google Scholar 

  • Kube J, Powilleit M (1997) Factors controlling the distribution of Marenzelleria cf. viridis, Pygospio elegans and Streblospio shrubsoli (Polychaeta: Spionidae) in the southern Baltic Sea, with special attention for the response to an event of hypoxia. Aquat Ecol 31:187–198

    Article  Google Scholar 

  • Lambert R, Retiere C, Lagadeuc Y (1996) Metamorphosis of Pectinaria koreni (Annelida: Polychaeta) and recruitment of an isolated population in the English Channel. J Mar Biol Assoc UK 76:23–36

    Article  Google Scholar 

  • Levin LA (2006) Recent progress in understanding larval dispersal: new directions and digressions. Integr Comp Biol 46:282–297

    Article  CAS  Google Scholar 

  • Middelboe AL, Sand-Jensen K (2000) Long-term changes in macroalgal communities in a Danish estuary. Phycologia 39:245–257

    Article  Google Scholar 

  • Moberg P, Burton R (2000) Genetic heterogeneity among adult and recruit red sea urchins, Strongylocentrotus franciscanus. Mar Biol 136(5):773–784

    Article  CAS  Google Scholar 

  • Morgan TS, Rogers DA, Paterson LGJ, Hawkins EL, Sheader M (1999) Evidence for poecilogony in Pygospio elegans (Polychaeta: Spionidae). Mar Ecol Prog Ser 178:121–132

    Article  Google Scholar 

  • Muths D, Jollivet D, Gentil F, Davoult D (2009) Large-scale genetic patchiness among NE Atlantic populations of the brittle star Ophiothrix fragilis. Aquat Biol 5:117–132

    Article  Google Scholar 

  • Olivier F, Desroy N, Retiere C (1996) Habitat selection and adult recruit interactions in Pectinaria koreni (Malmgren) (Annelida: Polychaeta) post-larval populations: results of flume experiments. J Sea Res 36:217–226

    Article  Google Scholar 

  • Owen EF, Rawson PD (2013) Small-scale spatial and temporal genetic structure of the Atlantic sea scallop (Placopecten magellanicus) in the inshore Gulf of Maine revealed using AFLPs. Mar Biol 160:3015–3025

    Article  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, 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  Google Scholar 

  • Pelc RA, Warner RR, Gaines SD (2009) Geographical patterns of genetic structure in marine species with contrasting life histories. J Biogeogr 36:1881–1890

    Article  Google Scholar 

  • Penant G, Aurelle D, Feral JP, Chenuil A (2013) Planktonic larvae do not ensure gene flow in the edible sea urchin Paracentrotus lividus. Mar Ecol Prog Ser 480:155–170

    Article  Google Scholar 

  • Pinedo S, Sarda R, Rey C, Bhaud M (2000) Effect of sediment particle size on recruitment of Owenia fusiformis in the Bay of Blanes (NW Mediterranean Sea): an experimental approach to explain field distribution. Mar Ecol Prog Ser 203:205–213

    Article  Google Scholar 

  • Pinsky ML, Palumbi SR, Andréfouët S, Purkis SJ (2012) Open and closed seascapes: where does habitat patchiness create populations with high fractions of self-recruitment? Ecol Appl 22:1257–1267

    Article  Google Scholar 

  • Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 115:945–959

    Google Scholar 

  • Qian PY, Rittschof D, Sreedhar B, Chia FS (1999) Macrofouling in unidirectional flow: miniature pipes as experimental models for studying the effects of hydrodynamics on invertebrate larval settlement. Mar Ecol Prog Ser 191:141–151

    Article  Google Scholar 

  • Rasmussen E (1953) Asexual reproduction in Pygospio elegans Claparede (Polychaeta sedentaria). Nature 171:1161–1162

    Article  CAS  Google Scholar 

  • Rasmussen E (1973) Systematics and ecology of the Isefjord marine fauna (Denmark). Ophelia 11:1–495

    Article  Google Scholar 

  • Riginos C, Cunningham CW (2005) Invited review: local adaptation and species segregation in two mussel (Mytilus edulis × Mytilus trossulus) hybrid zones. Mol Ecol 14:381–400

    Article  CAS  Google Scholar 

  • Rosenberg N (2004) DISTRUCT: a program for the graphical display of population structure. Mol Ecol Notes 4(1):137–138

    Article  Google Scholar 

  • Ross PM, Hogg ID, Pilditch CA, Lundquist CJ, Wilkins RJ (2012) Population genetic structure of the New Zealand estuarine clam Austrovenus stutchburyi (Bivalvia: Veneridae) reveals population subdivision and partial congruence with biogeographic boundaries. Estuaries Coasts 35:143–154

    Article  CAS  Google Scholar 

  • Schückel U, Beck M, Kröncke I (2013) Spatial variability in structural and functional aspects of macrofauna communities and their environmental parameters in the Jade Bay (Wadden Sea Lower Saxony, southern North Sea). Helgol Mar Res 67(1):121–136

    Article  Google Scholar 

  • Selkoe KA, Gaines SD, Caselle JE, Warner RR (2006) Current shifts and kin aggregation explain genetic patchiness in fish recruits. Ecology 87(12):3082–3094

    Article  Google Scholar 

  • Selkoe KA, Henzler CM, Gaines SD (2008) Seascape genetics and the spatial ecology of marine populations. Fish Fish 9:363–377

    Article  Google Scholar 

  • Selkoe KA, Watson JR, White C, Horin TB, Iacchei M, Satoshi M, Siegel DA, Gaines SD, Toonen RJ (2010) Taking the chaos out of genetic patchiness: seascape genetics reveals ecological and oceanographic drivers of genetic patterns in three temperate reef species. Mol Ecol 19:3708–3726

    Article  Google Scholar 

  • Simon J-C, Baumann S, Sunnucks P, Hebert PDN, Pierre J-S, Le Gallic J-F, Dedryver C-A (1999) Reproductive mode and population genetic structure of the cereal aphid Sitobion avenae studied using phenotypic and microsatellite markers. Mol Ecol 8:531–545

    Article  CAS  Google Scholar 

  • Sponaugle S, Cowen RK, Shanks A, Morgan SG, Leis JM, Pineda J, Boehlert GW, Kingsford MJ, Lindeman KC, Grimes C, Munro JL (2002) Predicting self-recruitment in marine populations: biophysical correlates and mechanisms. Bull Mar Sci 70:341–375

    Google Scholar 

  • Taylor MS, Hellberg ME (2003) Genetic evidence for local retention of pelagic larvae in a Caribbean reef fish. Science 299:107–109

    Article  CAS  Google Scholar 

  • Thiyagarajan V, Soo L, Qian PY (2005) The role of sediment organic matter composition in larval habitat selection by the polychaete Capitella sp. I. J Exp Mar Biol Ecol 323:70–83

    Article  CAS  Google Scholar 

  • Toonen RJ, Grosberg RK (2011) Causes of chaos: spatial and temporal genetic heterogeneity in the intertidal anomuran crab Petrolisthes cinctipes. In: KoenemannS, Held C, Schubart C (eds) Phylogeography and population genetics in Crustacea, chap 4. Crustacean issues series. CRC Press, Boca Raton, pp 75–107, ISBN: 1439840733

  • Turner EJ, Zimmer-Faust MA, Palmer MA, Luckenbach M, Pentcheff ND (1994) Settlement of oyster Crassostrea virginica larvae: effects of water flow and a water-soluble chemical cue. Limnol Oceanogr 39:1579–1593

    Article  CAS  Google Scholar 

  • Vadopalas B, Leclair LL, Bentzen P (2012) Temporal genetic similarity among year-classes of the Pacific geoduck clam (Panopea generosa Gould 1850): a species exhibiting spatial genetic patchiness. J Shellfish Res 31(3):697–709

    Article  Google Scholar 

  • Vergara-Chen C, González-Wangüemert M, Marcos C, Pérez-Ruzafa Á (2013) Small-scale genetic structure of Cerastoderma glaucum in a lagoonal environment: potential significance of habitat discontinuity and unstable population dynamics. J Mollus Stud 79(3):230–240

    Article  Google Scholar 

  • Wagner AP, Creel S, Kalinowski ST (2006) Estimating relatedness and relationships using microsatellite loci with null alleles. Heredity 97:336–345

    Article  CAS  Google Scholar 

  • Wang J (2014) Marker-based estimates of relatedness and inbreeding coefficients: an assessment of current methods. J Evol Biol 27(3):518–530

    Article  Google Scholar 

  • Warner RR, Cowen RK (2002) Local retention of production in marine populations: evidence, mechanisms, and consequences. Bull Mar Sci 70(1):245–249

    Google Scholar 

  • Waters JM, Roy MS (2004) Phylogeography of a high-dispersal New Zealand sea-star: does upwelling block gene-flow? Mol Ecol 13:2797–2806

    Article  CAS  Google Scholar 

  • Watts PC, Thorpe JP (2006) Influence of contrasting larval developmental types upon the population-genetic structure of cheilostome bryozoans. Mar Biol 149:1093–1101

    Article  Google Scholar 

  • White C, Selkoe KA, Watson J, Siegel DA, Zacherl DC, Toonen RJ (2010) Ocean currents help explain population genetic structure. Proc R Soc B 277:1685–1694

    Article  Google Scholar 

  • Wilke T, Davis GM (2000) Intraspecific mitochondrial sequence diversity in Hydrobia ulvae and Hydrobia ventrosa (Hydrobiidae: Rissooidea: Gastropoda): do their different life histories affect biogeographic patterns and gene flow? Biol J Linn Soc 70:89–105

    Article  Google Scholar 

  • Wing SR, Largier JL, Botsford LW, Quinn JF (1995) Settlement and transport of benthic invertebrates in an intermittent upwelling region. Limnol Oceanogr 40:316–329

    Article  Google Scholar 

  • Yearsley JM, Viard F, Broquet T (2013) The effect of collective dispersal on the genetic structure of a subdivided population. Evolution 63(6):1649–1659

    Article  Google Scholar 

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Acknowledgments

Marina Mustonen is acknowledged for her help in the DNA laboratory. J.E.K. was supported by a personal grant from the Jenny and Antti Wihuri Foundation. This research was supported by the Academy of Finland (Project 258365 to K.E.K.) and by the Danish National Science Research Council (Project 272-07-0485 to B.W.H.).

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Kesäniemi, J.E., Hansen, B.W., Banta, G.T. et al. Chaotic genetic patchiness and high relatedness of a poecilogonous polychaete in a heterogeneous estuarine landscape. Mar Biol 161, 2631–2644 (2014). https://doi.org/10.1007/s00227-014-2535-2

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