Marine Biology

, 158:2109 | Cite as

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

  • Sónia C. S. Andrade
  • Jon L. Norenburg
  • Vera N. Solferini
Original Paper

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.

References

  1. 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 18:3885–3902CrossRefGoogle Scholar
  2. Akaike H (1974) A new look at the statistical model identification. IEEE Trans Autom Control 19:716–723CrossRefGoogle Scholar
  3. 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 55:121–131CrossRefGoogle Scholar
  4. 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 25:3389–3402CrossRefGoogle Scholar
  5. 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. CladisticsGoogle Scholar
  6. Avise JC (2000) Phylogeography. The history and formation of species. Harvard University Press, CambridgeGoogle Scholar
  7. 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 18:489–522Google Scholar
  8. Ayres DL, Santos AAS (2007) BioEstat: aplicações estatísticas nas áreas das ciências bio-médicas. Available online at: http://www.mamiraua.org.br/download/
  9. Barton NH, Whitlock MC (1997) The evolution of metapopulations. In: Hanski IA, Gilpin ME (eds) Metapopulation biology. Academic Press, San Diego, pp 183–210CrossRefGoogle Scholar
  10. 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
  11. 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 98:4563–4568CrossRefGoogle Scholar
  12. Bird CE, Holland BS, Bowen BW, Toonen RJ (2007) Contrasting phylogeography in three endemic Hawaiian limpets (Cellana spp.) with similar life histories. Mol Ecol 16:3173–3186CrossRefGoogle Scholar
  13. Bryant EH (1976) A comment on the role of environmental variation in maintaining polymorphisms in natural populations. Evolution 30:188–190CrossRefGoogle Scholar
  14. Casu M, Curini-Galletti M (2004) Sibling species in interstitial flatworms: a case study using Monocelis lineata (Proseriata: Monocelididae). Mar Biol 145:669–679Google Scholar
  15. 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 87:553–576CrossRefGoogle Scholar
  16. 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:e12885CrossRefGoogle Scholar
  17. Chernyshev A (2000) Nemertean larvae of the Ototyphlonemertidae family in the plankton of Peter the Great Bay, Sea of Japan. Russ J Mar Biol 26:48–50CrossRefGoogle Scholar
  18. Chernyshev A (2007) Nemerteans of the genus Ototyphlonemertes (Enopla: Ototyphlonemertidae) from Van Phong Bay (South Vietnam). Russ J Mar Biol 33:196–199CrossRefGoogle Scholar
  19. 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 24:209–230CrossRefGoogle Scholar
  20. Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1659CrossRefGoogle Scholar
  21. Corrêa DD (1948) Ototyphlonemertes from the Brazilian coast. Commun Zool Mus Hist Nat Mont 2:1–12Google Scholar
  22. Corrêa DD (1949) Ecological studies of Brazilian Ototyphlonemertes. Commun Zool Mus Hist Nat Mont 3:1–7Google Scholar
  23. Corrêa DD (1950) Sobre Ototyphlonemertes do Brasil. Bol Fac Filos Ciênc Letras USP (Zool) 15:203–234Google Scholar
  24. Corrêa DD (1953) Sobre a neurofisiologia locomotora de Hoplonemertinos e a taxonomia de Ototyphlonemertes. An Acad Brasil Ci 25:545–555Google Scholar
  25. Corrêa DD (1954) Nemertinos do litoral Brasileiro. Bol Fac Filos Ciênc Letras USP (Zool) 19:1–122Google Scholar
  26. Cowen RK, Lwiza KMM, Sponaugle S, Paris CB, Olson DB (2000) Connectivity of marine populations: open or closed? Science 287:857–859CrossRefGoogle Scholar
  27. Crandall ED, Frey MA, Grosberg RK, Barber PH (2008) Contrasting demographic history and phylogeographical patterns in two Indo-Pacific gastropods. Mol Ecol 17:611–626CrossRefGoogle Scholar
  28. Dawson MN (2001) Phylogeography in coastal marine animals: a solution from California? J Biogeogr 28:723–736CrossRefGoogle Scholar
  29. 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 163:155–163CrossRefGoogle Scholar
  30. 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 151:1799–1812CrossRefGoogle Scholar
  31. 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 17:3306–3322CrossRefGoogle Scholar
  32. 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):47–62Google Scholar
  33. Diesing KM (1863) Nachträge zur Revision der Turbellarien. Sitz ber Math Nat Kl Akad Wiss Wien 46:413–416Google Scholar
  34. Edgar RC (2004) MUSCLE: a multiple sequence alignment method with reduced and space complexity. BMC Bioinform 5:113CrossRefGoogle Scholar
  35. 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) 238:253–277CrossRefGoogle Scholar
  36. Envall M, Norenburg JL (2001) Morphology and systematics in mesopsammic nemerteans of the genus Ototyphlonemertes (Nemertea, Hoplonemertea, Ototyphlonemertidae). Hydrobiologia 456:145–163CrossRefGoogle Scholar
  37. 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 123:105–115CrossRefGoogle Scholar
  38. 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 131:479–491Google Scholar
  39. Excoffier L, Laval G, Schneider S (2005) ARLEQUIN version 3.0: an integrated software package for population genetics data analysis. Evol Biol Online 1:47–50Google Scholar
  40. Fonsêca-Genevois V, Somerfield PJ, Neves MHB, Coutinho R, Moens T (2006) Colonization and early succession on artificial hard substrata by meiofauna. Mar Biol 148:1039–1050CrossRefGoogle Scholar
  41. Fu Y-X (1996) New statistical tests of neutrality for DNA samples from a population. Genetics 143:557–570Google Scholar
  42. Fu Y-X (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147:915–925Google Scholar
  43. Gaylord B, Gaines SD (2000) Temperature or transport? Range limits in marine species mediated solely by flow. Am Nat 155:769–789CrossRefGoogle Scholar
  44. Giere O (2009) Meiobenthology: the microscopic motile fauna of aquatic sediments, 2nd edition. Springer, BerlinGoogle Scholar
  45. Hart MW, Sunday J (2007) Things fall apart: biological species form unconnected parsimony networks. Biol Lett 3:509–512CrossRefGoogle Scholar
  46. Heads M (2005) Towards a panbiogeography of the seas. Biol J Linn Soc 84:675–723CrossRefGoogle Scholar
  47. Higgins RP, Thiel H (1988) Introduction to the study of Meiofauna. Smithsonian Institution Press, WashingtonGoogle Scholar
  48. 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 82:169–187CrossRefGoogle Scholar
  49. Hudson RR (2000) A new statistic for detecting genetic differentiation. Genetics 155:2011–2014Google Scholar
  50. Ibrahim KM, Nichols RA, Hewitt GM (1996) Spatial patterns of genetic variation generated by different forms of dispersal during range expansion. Heredity 77:282–291CrossRefGoogle Scholar
  51. Iwata F (1960) Studies on the comparative embryology of the nemerteans with special references to their interrelationships. Public Akkeshi Mar Biol St 10:1–51Google Scholar
  52. Jägersten G (1972) Evolution of the metazoan life cycle. A comprehensive theory. Academic Press, New York, p 282Google Scholar
  53. Jensen JL, Bohonak AJ, Kelley ST (2005) Isolation by distance, web service. BMC Genet 6:13Google Scholar
  54. Jokiel PL (1990) Long-distance dispersal by rafting: reemergence of an old hypothesis. Endeavour 14:66–73CrossRefGoogle Scholar
  55. 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 78:113–130CrossRefGoogle Scholar
  56. Knowlton N (1993) Sibling species in the sea. Annu Rev Ecol Syst 24:189–216CrossRefGoogle Scholar
  57. Knowlton N (2000) Molecular genetic analyses of species boundaries in the sea. Hydrobiologia 420:73–90CrossRefGoogle Scholar
  58. Kosakovsky Pond SL, Frost SDW, Muse SV (2005) HyPhy: hypothesis testing using phylogenies. Bioinformatics 21:676–679CrossRefGoogle Scholar
  59. 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 59:2139–2158Google Scholar
  60. Librado P, Rosas J (2009) DnaSPv5.0: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452CrossRefGoogle Scholar
  61. 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 39:734–746CrossRefGoogle Scholar
  62. 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 33:193–202CrossRefGoogle Scholar
  63. Mantel N (1967) The detection of disease clustering and a generalized regression approach. Cancer Res 27:209–220Google Scholar
  64. Mateos E, Giribet G (2008) Exploring the molecular diversity of terrestrial nemerteans (Hoplonemertea, Monostilifera, Acteonemertidae) in a continental landmass. Zool Scr 37:235–243CrossRefGoogle Scholar
  65. Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New YorkGoogle Scholar
  66. Norenburg JL, Stricker SA (2002) Chapter 7- Phylum Nemertea. In: Young CM (ed) Atlas of marine invertebrate larvae. Academic Press, San Diego, pp 163–177Google Scholar
  67. 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 42:922–934CrossRefGoogle Scholar
  68. Posada D, Crandall KA (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics 14:817–818CrossRefGoogle Scholar
  69. Posada D, Crandall KA (2001) Evaluation of methods for detecting recombination from DNA sequences using computer simulations. Proc Natl Acad Sci USA 98:13757–13762CrossRefGoogle Scholar
  70. Ray N, Currat M, Excofier L (2003) Intra-deme molecular diversity in spatially expanding populations. Mol Biol Evol 20:76–86CrossRefGoogle Scholar
  71. 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 33:990–1006CrossRefGoogle Scholar
  72. Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–225CrossRefGoogle Scholar
  73. 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 11:243–252CrossRefGoogle Scholar
  74. Rocha LA, Robertson DR, Roman J, Bowen BW (2005) Ecological speciation in tropical reef fishes. Proc R Soc B Biol 272:573–579Google Scholar
  75. 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 8:157CrossRefGoogle Scholar
  76. 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 18:1088–1102Google Scholar
  77. Rogers AR, Harpending H (1992) Population growth makes waves in the distribution of pairwise genetic differences. Mol Biol Evol 9:552–569Google Scholar
  78. 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 365:1–11CrossRefGoogle Scholar
  79. Rousset F (1997) Genetic differentiation and estimation of gene flow from F-statistics under isolation by distance. Genetics 145:1219–1228Google Scholar
  80. 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 19:3708–3726CrossRefGoogle Scholar
  81. Shanks AL, Walters K (1997) Holoplankton, meroplankton, and meiofauna associated with marine snow. Mar Ecol Prog Ser 156:75–86CrossRefGoogle Scholar
  82. Slatkin M (1987) Gene flow and the geographic structure of natural populations. Science 236:787–792CrossRefGoogle Scholar
  83. 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 83:1209–1213CrossRefGoogle Scholar
  84. 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 35:369–377Google Scholar
  85. Stamatakis A (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688–2690CrossRefGoogle Scholar
  86. Stamatakis A, Hoover P, Rougemont J (2008) A fast bootstrapping algorithm for the RaxML web-servers. Syst Biol 57:758–771CrossRefGoogle Scholar
  87. 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 86:201–212CrossRefGoogle Scholar
  88. 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 37:144–152CrossRefGoogle Scholar
  89. Sundberg P, Strand M (2010) Nemertean taxonomy- time to change lane? J Zool Syst Evol Res 48:283–284Google Scholar
  90. Sundberg P, Vodoti ET, Zhou H, Strand M (2009) Polymorphism hides cryptic species in Oerstedia dorsalis (Nemertea, Hoplonemertea). Biol J Linn Soc 98:556–567CrossRefGoogle Scholar
  91. Swedmark B (1964) The interstitial fauna of marine sand. Biol Rev 39:1–42Google Scholar
  92. Tajima F (1983) Evolutionary relationship of DNA sequences in finite populations. Genetics 105:437–460Google Scholar
  93. Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595Google Scholar
  94. 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 132:619–633Google Scholar
  95. Thollesson M (2000) Increasing fidelity in parsimony analysis of dorid nudibranchs by differential weightining, or a tale of two genes. Mol Phylogenet Evol 16:161–172CrossRefGoogle Scholar
  96. Thollesson M, Norneburg JL (2003) Ribbon worm relationships: a phylogeny of the phylum Nemertea. Proc R Soc Lond B 270:407–415Google Scholar
  97. 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 17:5104–5117CrossRefGoogle Scholar
  98. Tulchinsky A, Norenburg JL, Turbeville JM (in prep) Phylogeography of the marine meiofaunal nemertean Ototyphlonemertes parmula (Nemertea, Hoplonemertea) reveals high dispersal and cryptic diversityGoogle Scholar
  99. 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 43:1056–1065CrossRefGoogle Scholar
  100. Venekey V, Fonseca-Genevois VG, Santos PJP (2010) Biodiversity of free-living marine nematodes on the coast of Brazil: a review. Zootaxa 2568:39–66Google Scholar
  101. 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 142:637–642Google Scholar
  102. Winnepenninckx B, Backeljau T, De Watcher R (1993) Extraction of high molecular weight DNA from molluscs. Trends Genet 9:407CrossRefGoogle Scholar
  103. Winston JE, Migotto AE (2005) A new encrusting interstitial marine fauna from Brazil. Invertebr Biol 124:79–87CrossRefGoogle Scholar
  104. Wright S (1977) Evolution and the genetics of populations, vol 3, experimental results and evolutionary deductions. University of Chicago Press, ChicagoGoogle Scholar
  105. Zbawicka M, Wenne R, Skibinski DOF (2003) Mitochondrial DNA variation in populations of the mussel Mytilus trossulus from the Southern Baltic. Hydrobiologia 499:1–12CrossRefGoogle Scholar

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© Springer-Verlag 2011

Authors and Affiliations

  • Sónia C. S. Andrade
    • 1
    • 2
    • 3
  • Jon L. Norenburg
    • 1
  • Vera N. Solferini
    • 2
  1. 1.Department of Invertebrate ZoologyNational Museum of Natural HistoryWashingtonUSA
  2. 2.Departamento de Genética, Evolução e BioagentesUniversidade Estadual de CampinasCampinasBrazil
  3. 3.Museum of Comparative Zoology, Department of Organismic and Evolutionary BiologyHarvard UniversityCambridgeUSA

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