Skip to main content
Log in

Worms without borders: genetic diversity patterns in four Brazilian Ototyphlonemertes species (Nemertea, Hoplonemertea)

  • Original Paper
  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

Understanding the evolutionary processes from recent demographic history is especially difficult for interstitial organisms due to their poorly known natural history. In this study, the genetic variation and population history of the four Ototyphlonemertes (Diesing in Sitz ber Math Nat Kl Akad Wiss Wien 46:413–416, 1863) species were evaluated from samples collected along the Brazilian coast (between 27°31′S and 13°00′W) in 2006. The mitochondrial region cytochrome c oxidase subunit 3 (COX3) is analyzed to assess the genetic variation of these dioecious species. Although these species have a sympatric distribution along the coast, our data suggest that their levels of differentiation and their demographic histories differ sharply. There is strong evidence of gene flow among demes in O. erneba and O. evelinae, and their level of structuring is much lower than for the other two species. Indeed, the COX3 fragment reveals cryptic lineages in O. lactea and O. parmula. The results seem to contradict the high genetic structuring and low intrapopulational variability expected with the ecological constriction and habitat discontinuity faced by these organisms, meaning that there might be gene flow among populations or their dispersal capability has been underestimated.

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
Fig. 3
Fig. 4

Similar content being viewed by others

Notes

  1. This O. fila designation was changed to O. parmula after this manuscript was accepted.

References

  • Abellán P, Millán A, Ribera I (2009) Parallel habitat-driven differences in the phylogeographical structure of two independent lineages of Mediterranean saline water beetles. Mol Ecol 18:3885–3902

    PubMed  Google Scholar 

  • Akaike H (1974) A new look at the statistical model identification. IEEE Trans Autom Control 19:716–723

    Google Scholar 

  • Albuquerque EF, Pinto APB, Perez ADQ, Veloso VG (2007) Spatial and temporal changes in interstitial meiofauna on a sandy ocean beach of south America. Braz J Oceanogr 55:121–131

    Google Scholar 

  • Altschul S, Madden T, Schaffer A, Zhang J, Zhang Z, Miller W, Lipman D (1997) Gapped Blast and Psi-blast: a new generation of protein database search programs. Nucl Acids Res 25:3389–3402

    CAS  PubMed  PubMed Central  Google Scholar 

  • Andrade SCS, Strand M, Schwartz M, Chen H, Kajihara H, Döhren J, Sun S, Junoy J, Thiel M, Norenburg JL, Turbeville JM, Giribet G, Sundberg P (submitted) Disentangling ribbon worm relationships: multi-locus analysis supports traditional classification of the phylum Nemertea. Cladistics

  • Avise JC (2000) Phylogeography. The history and formation of species. Harvard University Press, Cambridge

    Google Scholar 

  • Avise JC, Arnold J, Ball RM, Bermingham E, Lamb T, Neigel JE, Reeb CA, Saunders NC (1987) Intraspecific phylogeography: the mitochondrial DNA bridge between population genetics and systematics. Annu Rev Ecol Syst 18:489–522

    Google Scholar 

  • Ayres DL, Santos AAS (2007) BioEstat: aplicações estatísticas nas áreas das ciências bio-médicas. Available online at: http://www.mamiraua.org.br/download/

  • Barton NH, Whitlock MC (1997) The evolution of metapopulations. In: Hanski IA, Gilpin ME (eds) Metapopulation biology. Academic Press, San Diego, pp 183–210

    Google Scholar 

  • Beerli P (2008) Migrate version 3.0: a maximum likelihood and Bayesian estimator of gene flow using the coalescent. Distributed over the internet at http://popgen.scs.edu/migrate.html

  • Beerli P, Felsenstein J (2001) Maximum likelihood estimation of a migration matrix and effective population sizes in n subpopulations by using a coalescent approach. Proc Natl Acad Sci USA 98:4563–4568

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bird CE, Holland BS, Bowen BW, Toonen RJ (2007) Contrasting phylogeography in three endemic Hawaiian limpets (Cellana spp.) with similar life histories. Mol Ecol 16:3173–3186

    CAS  PubMed  Google Scholar 

  • Bryant EH (1976) A comment on the role of environmental variation in maintaining polymorphisms in natural populations. Evolution 30:188–190

    PubMed  Google Scholar 

  • Casu M, Curini-Galletti M (2004) Sibling species in interstitial flatworms: a case study using Monocelis lineata (Proseriata: Monocelididae). Mar Biol 145:669–679

    Google Scholar 

  • Casu M, Curini-Galletti M (2006) Genetic evidence for the existence of cryptic species in the mesopsammic flatworm Pseudomonocelis ophiocephala (Rhabditophora: Proseriata). Biol J Linn Soc 87:553–576

    Google Scholar 

  • Chen H, Strand M, Norenburg JL, Sun S, Kajihara H, Chernyshev AV, Maslakova SA, Sundberg P (2010) Statistical parsimony networks and species assemblages in cephalotrichid nemerteans (Nemertea). PloS ONE 5:e12885

    PubMed  PubMed Central  Google Scholar 

  • Chernyshev A (2000) Nemertean larvae of the Ototyphlonemertidae family in the plankton of Peter the Great Bay, Sea of Japan. Russ J Mar Biol 26:48–50

    Google Scholar 

  • Chernyshev A (2007) Nemerteans of the genus Ototyphlonemertes (Enopla: Ototyphlonemertidae) from Van Phong Bay (South Vietnam). Russ J Mar Biol 33:196–199

    Google Scholar 

  • Cirano M, Mata MM, Campos EJD, Deiró NFR (2006) A circulação oceânica de larga-escala na região Oeste do Atlântico Sul com base no modelo de citrculação global OCCAM. Rev Bras Geof 24:209–230

    Google Scholar 

  • Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1659

    CAS  PubMed  Google Scholar 

  • Corrêa DD (1948) Ototyphlonemertes from the Brazilian coast. Commun Zool Mus Hist Nat Mont 2:1–12

    Google Scholar 

  • Corrêa DD (1949) Ecological studies of Brazilian Ototyphlonemertes. Commun Zool Mus Hist Nat Mont 3:1–7

    Google Scholar 

  • Corrêa DD (1950) Sobre Ototyphlonemertes do Brasil. Bol Fac Filos Ciênc Letras USP (Zool) 15:203–234

    Google Scholar 

  • Corrêa DD (1953) Sobre a neurofisiologia locomotora de Hoplonemertinos e a taxonomia de Ototyphlonemertes. An Acad Brasil Ci 25:545–555

  • Corrêa DD (1954) Nemertinos do litoral Brasileiro. Bol Fac Filos Ciênc Letras USP (Zool) 19:1–122

    Google Scholar 

  • Cowen RK, Lwiza KMM, Sponaugle S, Paris CB, Olson DB (2000) Connectivity of marine populations: open or closed? Science 287:857–859

    CAS  PubMed  Google Scholar 

  • Crandall ED, Frey MA, Grosberg RK, Barber PH (2008) Contrasting demographic history and phylogeographical patterns in two Indo-Pacific gastropods. Mol Ecol 17:611–626

    PubMed  Google Scholar 

  • Dawson MN (2001) Phylogeography in coastal marine animals: a solution from California? J Biogeogr 28:723–736

    Google Scholar 

  • De Wolf H, Backeljau T, Verhagen R (1998) Spatio-temporal genetic structure and gene flow between two distinct shell morphs of the planktonic periwinkle Littorina striata (Mollusca: Prosobranchia). Mar Ecol Prog Ser 163:155–163

    Google Scholar 

  • Derycke S, Backeljau T, Vlaeminck C, Vierstraete A, Vanfleteren J, Vincx M, Moens T (2007) Spatiotemporal analysis of population genetic structure in Geomonhystera disjuncta (Nematoda, Monhysteridae) reveals high levels of molecular diversity. Mar Biol 151:1799–1812

    Google Scholar 

  • Derycke S, Remerie T, Backeljau T, Vierstraete A, Vanfleteren J, Vincx M, Moens T (2008) Phylogeography of the Rhabditis (Pellioditis) marina species complex: evidence for long-distance dispersal, and for range expansions and restricted gene flow in the northeast Atlantic. Mol Ecol 17:3306–3322

    CAS  PubMed  Google Scholar 

  • Di Domenico M, Lana PD, Garraffoni ARS (2009) Distribution patterns of interstitial polychaetes in sandy beaches of southern Brazil. Mar Ecol Evol Persp 30(1):47–62

    Google Scholar 

  • Diesing KM (1863) Nachträge zur Revision der Turbellarien. Sitz ber Math Nat Kl Akad Wiss Wien 46:413–416

    Google Scholar 

  • Edgar RC (2004) MUSCLE: a multiple sequence alignment method with reduced and space complexity. BMC Bioinform 5:113

    Google Scholar 

  • Envall M (1996) Ototyphlonemertes correae sp. nov. and a redescription of O. duplex Bürger 1895 (Nemertea, Monostilifera, Ototyphlonemertidae), with a phylogenetic consideration of the genus. J Zool (Lond) 238:253–277

    Google Scholar 

  • Envall M, Norenburg JL (2001) Morphology and systematics in mesopsammic nemerteans of the genus Ototyphlonemertes (Nemertea, Hoplonemertea, Ototyphlonemertidae). Hydrobiologia 456:145–163

    Google Scholar 

  • Envall M, Sundberg P (1998) Phylogenetic relationships and genetic distances between some monostiliferous interstitial nemerteans (Ototyphlonemertes, Hoplonemertea, Nemertea) indicated from the 16S rRNA gene. Zool J Linn Soc 123:105–115

    Google Scholar 

  • Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction sites. Genetics 131:479–491

    CAS  PubMed  PubMed Central  Google Scholar 

  • Excoffier L, Laval G, Schneider S (2005) ARLEQUIN version 3.0: an integrated software package for population genetics data analysis. Evol Biol Online 1:47–50

    CAS  Google Scholar 

  • Fonsêca-Genevois V, Somerfield PJ, Neves MHB, Coutinho R, Moens T (2006) Colonization and early succession on artificial hard substrata by meiofauna. Mar Biol 148:1039–1050

    Google Scholar 

  • Fu Y-X (1996) New statistical tests of neutrality for DNA samples from a population. Genetics 143:557–570

    CAS  PubMed  PubMed Central  Google Scholar 

  • Fu Y-X (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147:915–925

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gaylord B, Gaines SD (2000) Temperature or transport? Range limits in marine species mediated solely by flow. Am Nat 155:769–789

    PubMed  Google Scholar 

  • Giere O (2009) Meiobenthology: the microscopic motile fauna of aquatic sediments, 2nd edition. Springer, Berlin

  • Hart MW, Sunday J (2007) Things fall apart: biological species form unconnected parsimony networks. Biol Lett 3:509–512

    CAS  PubMed  PubMed Central  Google Scholar 

  • Heads M (2005) Towards a panbiogeography of the seas. Biol J Linn Soc 84:675–723

    Google Scholar 

  • Higgins RP, Thiel H (1988) Introduction to the study of Meiofauna. Smithsonian Institution Press, Washington

    Google Scholar 

  • Hohenlohe PA (2004) Limits to gene flow in marine animals with planktonic larvae: models of Littorina species around Point Conception, California. Biol J Linn Soc 82:169–187

    Google Scholar 

  • Hudson RR (2000) A new statistic for detecting genetic differentiation. Genetics 155:2011–2014

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ibrahim KM, Nichols RA, Hewitt GM (1996) Spatial patterns of genetic variation generated by different forms of dispersal during range expansion. Heredity 77:282–291

    Google Scholar 

  • Iwata F (1960) Studies on the comparative embryology of the nemerteans with special references to their interrelationships. Public Akkeshi Mar Biol St 10:1–51

    Google Scholar 

  • Jägersten G (1972) Evolution of the metazoan life cycle. A comprehensive theory. Academic Press, New York, p 282

    Google Scholar 

  • Jensen JL, Bohonak AJ, Kelley ST (2005) Isolation by distance, web service. BMC Genet 6:13

    PubMed  PubMed Central  Google Scholar 

  • Jokiel PL (1990) Long-distance dispersal by rafting: reemergence of an old hypothesis. Endeavour 14:66–73

    Google Scholar 

  • Jollivet D, Dixon LRJ, Desbruyeres D, Dixon DR (1998) Ribosomal (rDNA) variation in a deep sea hydrothermal vent polychaete, Alvinella pompejana, from 13 degrees N on the East Pacific Rise. J Mar Biol Assoc UK 78:113–130

    CAS  Google Scholar 

  • Knowlton N (1993) Sibling species in the sea. Annu Rev Ecol Syst 24:189–216

    Google Scholar 

  • Knowlton N (2000) Molecular genetic analyses of species boundaries in the sea. Hydrobiologia 420:73–90

    CAS  Google Scholar 

  • Kosakovsky Pond SL, Frost SDW, Muse SV (2005) HyPhy: hypothesis testing using phylogenies. Bioinformatics 21:676–679

    Google Scholar 

  • Lee T, O’Foighil D (2005) Placing the Floridian marine genetic disjunction into a regional evolutionary context using the scorched mussel, Brachidontes exustus, species complex. Evolution 59:2139–2158

    CAS  PubMed  Google Scholar 

  • Librado P, Rosas J (2009) DnaSPv5.0: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452

    CAS  PubMed  Google Scholar 

  • Magoulas A, Castilho R, Caetano S, Marcato S, Patarnello T (2006) Mitochondrial DNA reveals a mosaic pattern of phylogeographical structure in Atlantic and Mediterranean populations of anchovy (Engraulis encrasicolus). Mol Phylogenet Evol 39:734–746

    CAS  PubMed  Google Scholar 

  • Mahon AR, Thornhill DJ, Norenburg JL, Halanych KM (2010) DNA uncovers Antarctic nemertean biodiversity and exposes a decades-old cold case of asymmetric inventory. Polar Biol 33:193–202

    Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Mateos E, Giribet G (2008) Exploring the molecular diversity of terrestrial nemerteans (Hoplonemertea, Monostilifera, Acteonemertidae) in a continental landmass. Zool Scr 37:235–243

    Google Scholar 

  • Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New York

    Google Scholar 

  • Norenburg JL, Stricker SA (2002) Chapter 7- Phylum Nemertea. In: Young CM (ed) Atlas of marine invertebrate larvae. Academic Press, San Diego, pp 163–177

    Google Scholar 

  • Paulay G, Meyer C (2002) Diversification in the tropical Pacific: comparisons between marine and terrestrial systems and the importance of founder speciation. Integr Comp Biol 42:922–934

    PubMed  Google Scholar 

  • Posada D, Crandall KA (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics 14:817–818

    CAS  PubMed  Google Scholar 

  • Posada D, Crandall KA (2001) Evaluation of methods for detecting recombination from DNA sequences using computer simulations. Proc Natl Acad Sci USA 98:13757–13762

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ray N, Currat M, Excofier L (2003) Intra-deme molecular diversity in spatially expanding populations. Mol Biol Evol 20:76–86

    CAS  PubMed  Google Scholar 

  • Reid DG, Lal K, Mackenzie-Dodds J, Kaligis F, Littlewood DTJ, Williams ST (2006) Comparative phylogeography and species boundaries in Echinolittorina snails in the central Indo-West Pacific. J Biogeogr 33:990–1006

    Google Scholar 

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

    PubMed  Google Scholar 

  • Rocha LA, Bass AL, Robertson DR, Bowen BW (2002) Adult habitat preferences, larval dispersal and the comparative phylogeography of three Atlantic surgeonfishes (Teleostei: Acanthuridae). Mol Ecol 11:243–252

    CAS  PubMed  Google Scholar 

  • Rocha LA, Robertson DR, Roman J, Bowen BW (2005) Ecological speciation in tropical reef fishes. Proc R Soc B Biol 272:573–579

    Google Scholar 

  • Rocha RA, Rocha CR, Robertson DR, Bowen BW (2008) Comparative phylogeography of Atlantic reef fishes indicates both origin and accumulation of diversity in the Caribbean. BMC Evol Biol 8:157

    PubMed  PubMed Central  Google Scholar 

  • Rocha-Olivares A, Fleeger JW, Foltz DW (2001) Decoupling of molecular and morphological evolution in deep lineages of a meiobenthic harpacticoid copepod. Mol Biol Evol 18:1088–1102

    CAS  PubMed  Google Scholar 

  • Rogers AR, Harpending H (1992) Population growth makes waves in the distribution of pairwise genetic differences. Mol Biol Evol 9:552–569

    CAS  PubMed  Google Scholar 

  • Rogers AD, Thorpe JP, Gibson R, Norenburg JL (1998) Genetic differentiation of populations of the common intertidal nemerteans Lineus ruber and Lineus viridis (Nemertea, Anopla). Hydrobiologia 365:1–11

    Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Selkoe KA, Watson JR, White C, Horin TB, Iacchei M, Mitarai S, 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

    PubMed  Google Scholar 

  • Shanks AL, Walters K (1997) Holoplankton, meroplankton, and meiofauna associated with marine snow. Mar Ecol Prog Ser 156:75–86

    Google Scholar 

  • Slatkin M (1987) Gene flow and the geographic structure of natural populations. Science 236:787–792

    CAS  PubMed  Google Scholar 

  • Somerfield PJ, Fonseca-Genevois VG, Rodrigues ACL, Castro FJV, Santos GA (2003) Factors affecting meiofaunal community structure in the Pina Basin, an urbanized embayment on the coast of Pernambuco, Brazil. Mar Biol Assoc UK 83:1209–1213

    Google Scholar 

  • Souza-Santos LP, Ribeiro VSS, Santos PJP, Fonseca-Genevois V (2003) Seasonality of intertidal meiofauna on a tropical sandy beach in Tamandare Bay (Northeast Brazil). J Coast Res Special Issue 35:369–377

    Google Scholar 

  • Stamatakis A (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688–2690

    CAS  PubMed  Google Scholar 

  • Stamatakis A, Hoover P, Rougemont J (2008) A fast bootstrapping algorithm for the RaxML web-servers. Syst Biol 57:758–771

    PubMed  Google Scholar 

  • Strand M, Sundberg P (2005a) Delimiting species in the hoplonemertean genus Tetrastemma (phylum Nemertea): morphology is not concordant with phylogeny as evidenced from mtDNA sequences. Biol J Linn Soc 86:201–212

    Google Scholar 

  • Strand M, Sundberg P (2005b) Genus Tetrastemma Ehrenberg, 1831 (Phylum Nemertea)—A natural group? Phylogenetic relationships inferred from partial 18S rRNA sequences. Mol Phylogenet Evol 37:144–152

    CAS  PubMed  Google Scholar 

  • Sundberg P, Strand M (2010) Nemertean taxonomy- time to change lane? J Zool Syst Evol Res 48:283–284

    Google Scholar 

  • Sundberg P, Vodoti ET, Zhou H, Strand M (2009) Polymorphism hides cryptic species in Oerstedia dorsalis (Nemertea, Hoplonemertea). Biol J Linn Soc 98:556–567

    Google Scholar 

  • Swedmark B (1964) The interstitial fauna of marine sand. Biol Rev 39:1–42

    Google Scholar 

  • Tajima F (1983) Evolutionary relationship of DNA sequences in finite populations. Genetics 105:437–460

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595

    CAS  PubMed  PubMed Central  Google Scholar 

  • Templeton AR, Crandall KA, Sing CF (1992) A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping and DNA sequence data. III. Cladogram estimation. Genetics 132:619–633

    CAS  PubMed  PubMed Central  Google Scholar 

  • Thollesson M (2000) Increasing fidelity in parsimony analysis of dorid nudibranchs by differential weightining, or a tale of two genes. Mol Phylogenet Evol 16:161–172

    CAS  PubMed  Google Scholar 

  • Thollesson M, Norneburg JL (2003) Ribbon worm relationships: a phylogeny of the phylum Nemertea. Proc R Soc Lond B 270:407–415

    CAS  Google Scholar 

  • Thornhill DJ, Mahon AR, Norenburg JL, Halanych KM (2008) Open-ocean barriers to dispersal: a test case with the Antarctic Polar Front and the ribbon worm Parborlasia corrugatus (Nemertea: Lineidae). Mol Ecol 17:5104–5117

    CAS  PubMed  Google Scholar 

  • Tulchinsky A, Norenburg JL, Turbeville JM (in prep) Phylogeography of the marine meiofaunal nemertean Ototyphlonemertes parmula (Nemertea, Hoplonemertea) reveals high dispersal and cryptic diversity

  • Turbeville JM, Smith DM (2007) The partial mitochondrial genome of the Cephalothrix rufifrons (Nemertea, Palaeonemertea): Characterization and implications for the phylogenetic position of Nemertea. Mol Phylogenet Evol 43:1056–1065

    CAS  PubMed  Google Scholar 

  • Venekey V, Fonseca-Genevois VG, Santos PJP (2010) Biodiversity of free-living marine nematodes on the coast of Brazil: a review. Zootaxa 2568:39–66

    Google Scholar 

  • Westheide W, Haß-Cordes E, Krabusch M, Müller MCM (2003) Ctenodrilus serratus (Polychaeta: Ctenodrilidae) is a truly amphi-Atlantic meiofauna species—evidence from molecular data. Mar Biol 142:637–642

    CAS  Google Scholar 

  • Winnepenninckx B, Backeljau T, De Watcher R (1993) Extraction of high molecular weight DNA from molluscs. Trends Genet 9:407

    CAS  PubMed  Google Scholar 

  • Winston JE, Migotto AE (2005) A new encrusting interstitial marine fauna from Brazil. Invertebr Biol 124:79–87

    Google Scholar 

  • Wright S (1977) Evolution and the genetics of populations, vol 3, experimental results and evolutionary deductions. University of Chicago Press, Chicago

    Google Scholar 

  • Zbawicka M, Wenne R, Skibinski DOF (2003) Mitochondrial DNA variation in populations of the mussel Mytilus trossulus from the Southern Baltic. Hydrobiologia 499:1–12

    CAS  Google Scholar 

Download references

Acknowledgments

The authors are thankful to all colleagues and friends from the V.N.S laboratory who helped with the fieldwork. The comments of K. Jörger, G. Giribet, and two anonymous reviewers also greatly improved the manuscript. We are grateful to staff in the Invertebrate Zoology Department (NMNH, Smithsonian Institution), especially Barbara Littman, Cynthia Santos and Jen Hammock; and to Jeff Hunt, Andrea Ormos and other members of the LAB (NMNH, Smithsonian Institution). We are in debt to Gonzalo Giribet and his laboratory at the Museum of Comparative Zoology, Harvard University, for hosting S.C.S.A. during the last stages of data collection. We are also grateful to the staff of the Research Computing cluster odyssey facility from the Faculty of Arts and Sciences located at Harvard University. S.C.S.A. was supported for this work by a fellowship from CNPq and partly by a Smithsonian Institution Postdoctoral Fellowship. This work was supported by FAPESP grant 05/56347 to V.N.S. and FAEP grant 519/292 to S.C.S.A.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Sónia C. S. Andrade.

Additional information

Communicated by S. Uthicke.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Andrade, S.C.S., Norenburg, J.L. & Solferini, V.N. Worms without borders: genetic diversity patterns in four Brazilian Ototyphlonemertes species (Nemertea, Hoplonemertea). Mar Biol 158, 2109–2124 (2011). https://doi.org/10.1007/s00227-011-1718-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00227-011-1718-3

Keywords

Navigation