Did vicariance and adaptation drive cryptic speciation and evolution of brooding in ophioderma longicauda (Echinodermata: Ophiuroidea), a common atlanto-mediterranean ophiuroid?

Molecular Ecology

Volumn 20, Issue 22, 2011, Pages 4737-4755

  Boissin, E ^a,c   Stohr S ^b   Chenuil, A ^a  

^a AIX MARSEILLE UNIVERSITY   (France)

^b SWEDISH MUSEUM OF NATURAL HISTORY   (Sweden)

^c UNIVERSITY OF PRETORIA   (South Africa)

Author keywords

Direct development; Dispersal; Diversification; Ecological shift; Phylogeny trait association analysis

Indexed keywords

MITOCHONDRIAL DNA; RIBOSOMAL SPACER DNA;

ADAPTATION; ALLELE; ANIMAL; ARTICLE; ATLANTIC OCEAN; DNA SEQUENCE; ECHINODERM; GENE FLOW; GENETIC VARIABILITY; GENETICS; GEOGRAPHY; MEDITERRANEAN SEA; MITOCHONDRION; PHYLOGENY; SPECIES DIFFERENTIATION;

ADAPTATION, BIOLOGICAL; ALLELES; ANIMALS; ATLANTIC OCEAN; DNA, MITOCHONDRIAL; DNA, RIBOSOMAL SPACER; ECHINODERMATA; GENE FLOW; GENETIC SPECIATION; GENETIC VARIATION; GEOGRAPHY; MEDITERRANEAN SEA; MITOCHONDRIA; PHYLOGENY; SEQUENCE ANALYSIS, DNA;

EID: 80054107934     PISSN: 09621083     EISSN: 1365294X     Source Type: Journal    
DOI: 10.1111/j.1365-294X.2011.05309.x     Document Type: Article

References (96)

1. Almada VC, Oliveira RF, Goncalves EJ et al. (2001) Patterns of diversity of the north-eastern Atlantic blenniid fish fauna (Pisces: Blenniidae). Global Ecology and Biogeography, 10, 411-422.
2. Bahri-Sfar L, Lemaire C, Ben Hassine OK, Bonhomme F (2000) Fragmentation of sea bass populations in the western and eastern Mediterranean as revealed by microsatellite polymorphism. Proceedings of the Royal Society of London Series B-Biological Sciences, 267, 929-935.
3. Bandelt HJ, Forster P, Rohl A (1999) Median-joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution, 16, 37-48.
4. Baric S, Sturmbauer C (1999) Ecological parallelism and cryptic species in the genus Ophiothrix derived from mitochondrial DNA sequences. Molecular Phylogenetics and Evolution, 11, 157-162.
5. Belkhir K, Borsa P, Goudet J, Chikhi L, Bonhomme F (2004) GENETIX, logiciel sous WindowsTM pour la génétique des populations. Available from: http://www.univ-montp2.fr/~genetix/genetix.htm. Laboratoire Génome et Populations, CNRS UPR 9060, Université Montpellier II, Montpellier, France.
6. Benavides-Serrato M, O’Hara TD (2008) A new species in the Ophiocoma erinaceus complex from the South-west Pacific Ocean (Echinodermata: Ophiuroidea: Ophiocomidae). Memoirs of Museum Victoria, 65, 51-56.
7. Bickford D, Lohman DJ, Sodhi NS et al. (2007) Cryptic species as a window on diversity and conservation. Trends in Ecology & Evolution, 22, 148-155.
8. Boissin E (2008) Phylogénie, phylogéographie, mode de reproduction et structure démographique dans le complexe d’espèces de l’ophiure hermaphrodite incubante Amphipholis squamata. PhD Thesis, Université Aix-Marseille 2, Marseille, France.
9. Boissin E, Feral JP, Chenuil A (2008a) Defining reproductively isolated units in a cryptic and syntopic species complex using mitochondrial and nuclear markers: the brooding brittle star, Amphipholis squamata (Ophiuroidea). Molecular Ecology, 17, 1732-1744.
10. Boissin E, Hoareau TB, Feral JP, Chenuil A (2008b) Extreme selfing rates in the cosmopolitan brittle star species complex Amphipholis squamata: data from progeny-array and heterozygote deficiency. Marine Ecology-Progress Series, 361, 151-159.
11. Boissin E, Hoareau TB, Berrebi P (2011) Effects of current and historic habitat fragmentation on the genetic structure of the sand goby Pomatoschistus minutus (Osteichthys, Gobiidae). Biological Journal of the Linnean Society, 102, 175-198.
12. Borrero-Pérez GH, González-Wangüemert M, Marcos C, Pérez-Ruzafa A (2011) Phylogeography of the Atlanto-Mediterranean sea cucumber Holothuria (Holothuria) mammata: the combined effects of historical processes and current oceanographical pattern. Molecular ecology, 20, 1964-1975.
13. Borsa P (2002) Allozyme, mitochondrial-DNA, and morphometric variability indicate cryptic species of anchovy (Engraulis encrasicolus). Biological Journal of the Linnean Society, 75, 261-269.
14. Byrne M, Hart MW, Cerra A, Cisternas P (2003) Reproduction and larval morphology of broadcasting and viviparous species in the Cryptasterina species complex. Biological Bulletin, 205, 285-294.
15. Calvo M, Templado J, Oliverio M, Machordom A (2009) Hidden Mediterranean biodiversity: molecular evidence for a cryptic species complex within the reef building vermetid gastropod Dendropoma petraeum (Mollusca: Caenogastropoda). Biological Journal of the Linnean Society, 96, 898-912.
16. Campo D, Molares J, Garcia L et al. (2010) Phylogeography of the European stalked barnacle (Pollicipes pollicipes): identification of glacial refugia. Marine Biology, 157, 147-156.
17. Caputi L, Andreakis N, Mastrototaro F et al. (2007) Cryptic speciation in a model invertebrate chordate. Proceedings of the National Academy of Sciences of the United States of America, 104, 9364-9369.
18. Casu M, Curini-Galletti M (2006) Genetic evidence for the existence of cryptic species in the mesopsammic flatworm Pseudomonocelis ophiocephala (Rhabditophora: Proseriata). Biological Journal of the Linnean Society, 87, 553-576.
19. Chenuil A (2006) Choosing the right molecular genetic markers for studying biodiversity: from molecular evolution to practical aspects. Genetica, 127, 101-120.
20. Chenuil A, Hoareau TB, Egea E et al. (2010) An efficient method to find potentially universal population genetic markers, applied to metazoans. BMC Evolutionary Biology, 10, 17.
21. Chia FS, Gibson G, Qian PY (1996) Poecilogony as a reproductive strategy of marine invertebrates. Oceanologica Acta, 19, 203-208.
22. Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Molecular Ecology, 9, 1657-1659.
23. Domingues VS, Bucciarelli G, Almada VC, Bernardi G (2005) Historical colonization and demography of the Mediterranean damselfish, Chromis chromis. Molecular Ecology, 14, 4051-4063.
24. Domingues VS, Faria C, Stefanni S et al. (2007) Genetic divergence in the Atlantic-Mediterranean Montagu’s blenny, Coryphoblennius galerita (Linnaeus 1758) revealed by molecular and morphological characters. Molecular Ecology, 16, 3592-3605.
25. D’Ortenzio F, d’Alcala MR (2009) On the trophic regimes of the Mediterranean Sea: a satellite analysis. Biogeosciences, 6, 139-148.
26. Drummond AJ, Rambaut A (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evolutionary Biology, doi:10.1186/1471-2148-7-214.
27. Emson RH, Crump RG (1979) Description of a new species of Asterina (Asteroidea), with an account of its ecology. Journal of the Marine Biological Association of the United Kingdom, 59, 77-91.
28. Excoffier L (2004) Patterns of DNA sequence diversity and genetic structure after a range expansion: lessons from the infinite-island model. Molecular Ecology, 13, 853-864.
29. Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes -application to human mitochondrial-DNA reconstruction data. Genetics, 131, 479-491.
30. Excoffier L, Laval G, Schneider S (2005) Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evolutionary Bioinformatics, 1, 47-50.
31. Faucci A, Toonen RJ, Hadfield MG (2007) Host shift and speciation in a coral-feeding nudibranch. Proceedings of the Royal Society B-Biological Sciences, 274, 111-119.
32. Felsenstein J (1985) Confidence-limits on phylogenies -an approach using the bootstrap. Evolution, 39, 783-791.
33. Fenaux L (1972) Evolution saisonniere des gonades chez l’Ophiure Ophioderma longicauda (Retzius), Ophiuroidea. Internationale Revue der gesamten Hydrobiologie und Hydrographie, 27, 257-262.
34. Fetzer I, Arntz WE (2008) Reproductive strategies of benthic invertebrates in the Kara Sea (Russian Arctic): adaptation of reproduction modes to cold water. Marine Ecology-Progress Series, 356, 189-202.
35. Foltz DW, Nguyen AT, Kiger JR, Mah CL (2008) Pleistocene speciation of sister taxa in a North Pacific clade of brooding sea stars (Leptasterias). Marine Biology, 154, 593-602.
36. Fu YX, Li WH (1993) Statistical tests of neutrality of mutations. Genetics, 133, 693-709.
37. Galtier N, Nabholz B, Glemin S, Hurst GDD (2009) Mitochondrial DNA as a marker of molecular diversity: a reappraisal. Molecular Ecology, 18, 4541-4550.
38. Gardner WD, Mishonov A, Richardson MJ (2006) Global POC concentrations from in-situ and satellite data. Deep-Sea Research Part II-Topical Studies in Oceanography, 53, 718-740.
39. Gillespie JM, McClintock JB (2007) Brooding in echinoderms: how can modem experimental techniques add to our historical perspective? Journal of Experimental Marine Biology and Ecology, 342, 191-201.
40. Griffiths AM, Sims DW, Cotterell SP et al. (2010) Molecular markers reveal spatially segregated cryptic species in a critically endangered fish, the common skate (Dipturus batis). Proceedings of the Royal Society B-Biological Sciences, 277, 1497-1503.
41. Guindon S, Lethiec F, Duroux P, Gascuel O (2005) PHYML Online -a web server for fast maximum likelihood-based phylogenetic inference. Nucleic Acids Research, 33, W557-W559.
42. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95 ⁄ 98 ⁄ NT. Nucleic Acids Symposium Series, 41, 95-98.
43. Hart MW, Sunday J (2007) Things fall apart: biological species form unconnected parsimony networks. Biology Letters, 3, 509-512.
44. Hart MW, Byrne M, Johnson SL (2003) Patiriella pseudoexigua (Asteroidea: Asterinidae): a cryptic species complex revealed by molecular and embryological analyses. Journal of the Marine Biological Association of the United Kingdom, 83, 1109-1116.
45. Hendler G (1991) Ophiuroidea. In: Reproduction of Marine Invertebrates (eds Giese AC, Pearse JS, Pearse VB), pp. 355-511. Boxwood Press, Pacific Grove.
46. Hoagland KE, Robertson R (1988) An assessment of poecilogony in marine-invertebrates -phenomenon or fantasy. Biological Bulletin, 174, 109-25.
47. Hoareau TB, Boissin E (2010) Design of phylum-specific hybrid primers for DNA barcoding: addressing the need for efficient COI amplification in the Echinodermata. Molecular Ecology Resources, 10, 960-967.
48. Hunter RL, Halanych KM (2008) Evaluating connectivity in the brooding brittle star Astrotoma agassizii across the drake passage in the Southern Ocean. Journal of Heredity, 99, 137-148.
49. Ives AR, Garland T (2010) Phylogenetic logistic regression for binary dependent variables. Systematic Biology, 59, 9-26.
50. Jolly MT, Viard F, Gentil F, Thiebaut E, Jollivet D (2006) Comparative phylogeography of two coastal polychaete tubeworms in the Northeast Atlantic supports shared history and vicariant events. Molecular Ecology, 15, 1841-1855.
51. Kelly RP, Palumbi SR (2010) Genetic structure among 50 species of the north eastern Pacific rocky intertidal community. PLoS One, 5, 13.
52. Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide-sequences. Journal of Molecular Evolution, 16, 111-120.
53. Krebes L, Blank M, Jurss K, Zettler ML, Bastrop R (2010) Glacial-driven vicariance in the amphipod Gammarus duebeni. Molecular Phylogenetics and Evolution, 54, 372-385.
54. Lanave C, Preparata G, Saccone C, Serio G (1984) A new method for calculating evolutionary substitution rates. Journal of Molecular Evolution, 20, 86-93.
55. Lawrence JM, Herrera J (2000) Stress and deviant reproduction in echinoderms. Zoological Studies, 39, 151-171.
56. Lessios HA (2008) The great American schism: divergence of marine organisms after the rise of the Central American Isthmus. Annual Review of Ecology Evolution and Systematics, 39, 63-91.
57. Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics, 25, 1451-1452.
58. Maddison WP, Maddison DR (2010) Mesquite: a modular system for evolutionary analysis. Version 2.74. Available from: http://mesquiteproject.org.
59. Maggs CA, Castilho R, Foltz D et al. (2008) Evaluating signatures of glacial refugia for North Atlantic benthic marine taxa. Ecology, 89, S108-S122.
60. McCartney MA, Keller G, Lessios HA (2000) Dispersal barriers in tropical oceans and speciation in Atlantic and eastern Pacific sea urchins of the genus Echinometra. Molecular Ecology, 9, 1391-1400.
61. Mercier A, Hamel JF (2008) Depth-related shift in life history strategies of a brooding and broadcasting deep-sea asteroid. Marine Biology, 156, 205-223.
62. Miura O, Torchin ME, Kuris AM, Hechinger RF, Chiba S (2006) Introduced cryptic species of parasites exhibit different invasion pathways. Proceedings of the National Academy of Sciences of the United States of America, 103, 19818-19823.
63. Mortensen T (1921) Studies of the Development and Larval Forms of Echinoderms. G.E.-C. Gad, Copenhagen, 266 pp.
64. Muths D, Davoult D, Gentil F, Jollivet D (2006) Incomplete cryptic speciation between intertidal and subtidal morphs of Acrocnida brachiata (Echinodermata: Ophiuroidea) in the Northeast Atlantic. Molecular Ecology, 15, 3303-3318.
65. Muths D, Jollivet D, Gentil F, Davoult D (2009) Large-scale genetic patchiness among NE Atlantic populations of the brittle star Ophiothrix fragilis. Aquatic Biology, 5, 117-132.
66. Nikula R, Vainola R (2003) Phylogeography of Cerastoderma glaucum (Bivalvia: Cardiidae) across Europe: a major break in the Eastern Mediterranean. Marine Biology, 143, 339-350.
67. Nylander JAA (2004) MrAIC.pl. Program distributed by the author, Evolutionary Biology Centre, Uppsala University, Sweden.
68. Ó Foighil D (1988) Random mating and planktotrophic larval development in the brooding hermaphroditic clam Lasaea australis (Lamarck, 1818). Veliger, 31, 214-221.
69. O’Hara TD, Byrne M, Cisternas PA (2004) The Ophiocoma erinaceus complex: another case of cryptic speciation in Echinoderms. In: Echinoderms: München. Proceedings of the 11th International Echinoderm Conference, Munich, Germany, 6-10 October 2003 (eds Heinzeller T, Nebelsick JH), pp. 537-542. Balkema, Leiden.
70. Palumbi SR (1996) Nucleic acids II: the polymerase chain reaction. In: Molecular Systematics (eds Hillis DM, Moritz C, Mable BK), pp. 205-247. Sinauer Associates, Sunderland, Massachusetts.
71. Parker J, Rambaut A, Pybus OG (2008) Correlating viral phenotypes with phylogeny: accounting for phylogenetic uncertainty. Infection Genetics and Evolution, 8, 239-246.
72. Patarnello T, Volckaert F, Castilho R (2007) Pillars of Hercules: is the Atlantic-Mediterranean transition a phylogeographical break? Molecular Ecology, 16, 4426-4444.
73. Pearse JS, Mooi R, Lockhart SJ, Brandt A (2009) Brooding and species diversity in the Southern Ocean: selection for brooders or speciation within brooding clades? In: Smithsonian at the Poles: Contributions to International Polar Year Science (eds Krupnik I, Lang MA, Miller SE), pp. 181-196. Smithsonian Inst Press, Washington.
74. Provan J, Bennett KD (2008) Phylogeographic insights into cryptic glacial refugia. Trends in Ecology & Evolution, 23, 564-571.
75. Ramos-Onsins SE, Rozas J (2002) Statistical properties of new neutrality tests against population growth. Molecular Biology and Evolution, 19, 2092-2100.
76. Ray N, Currat M, Excoffier L (2003) Intra-deme molecular diversity in spatially expanding populations. Molecular Biology and Evolution, 20, 76-86.
77. Raymond M, Rousset F (1995) Genepop (V.1.2) population genetics software for exact tests and ecumenicism. Journal of Heredity, 86, 248-249.
78. Rogers AR, Harpending H (1992) Population-growth makes waves in the distribution of pairwise genetic-differences. Molecular Biology and Evolution, 9, 552-569.
79. Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics, 19, 1572-1574.
80. Rousset F (1997) Genetic differentiation and estimation of gene flow from F-statistics under isolation by distance. Genetics, 145, 1219-1228.
81. Roy MS, Sponer R (2002) Evidence of a human-mediated invasion of the tropical western Atlantic by the ‘world’s most common brittlestar’. Proceedings of the Royal Society of London Series B-Biological Sciences, 269, 1017-1023.
82. Sponer R, Roy MS (2002) Phylogeographic analysis of the brooding brittle star Amphipholis squamata (Echinodermata) along the coast of New Zealand reveals high cryptic genetic variation and cryptic dispersal potential. Evolution, 56, 1954-1967.
83. Stöhr S, Muths D (2010) Morphological diagnosis of the two genetic lineages of Acrocnida brachiata (Echinodermata: Ophiuroidea), with description of a new species. Journal of the Marine Biological Association of the United Kingdom, 90, 831-843.
84. Stohr S, Boissin E, Chenuil A (2009) Potential cryptic speciation in Mediterranean populations of Ophioderma (Echinodermata: Ophiuroidea). Zootaxa, 2071, 1-20.
85. Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Molecular Biology and Evolution, 24, 1596-1599.
86. Tarnowska K, Chenuil A, Nikula R, Féral J-P, Wołowicz M (2010) Genetic structure of a widespread European bivalve Cerastoderma glaucum and possible bird-aided postglacial colonisation. Marine Ecology Progress Series, 406, 173-184.
87. Thompson JD, Higgins DG, Gibson TJ (1994) Clustal-W -improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research, 22, 4673-4680.
88. Tortonese E (1983) Remarks on the morphology and taxonomy of Ophioderma longicaudum (Retz.) from the Mediterranean. Atti della Societa Italiana di Scienze Naturali e del Museo Civico di Storia Naturale in Milano, 124, 21-28.
89. Tuya F, Ramirez R, Sanchez-Jerez P et al. (2006) Coastal resources exploitation can mask bottom-up mesoscale regulation of intertidal populations. Hydrobiologia, 553, 337-344.
90. Vantrepotte V, Melin F (2010) Temporal variability in SeaWiFS derived apparent optical properties in European seas. Continental Shelf Research, 30, 319-334.
91. Virgilio M, Fauvelot C, Costantini F, Abbiati M, Backeljau T (2009) Phylogeography of the common ragworm Hediste diversicolor (Polychaeta: Nereididae) reveals cryptic diversity and multiple colonization events across its distribution. Molecular Ecology, 18, 1980-1994.
92. Vogler C, Benzie J, Lessios H, Barber P, Worheide G (2008) A threat to coral reefs multiplied? Four species of crown-ofthorns starfish. Biology Letters, 4, 696-699.
93. Walsh PS, Metzger DA, Higuchi R (1991) Chelex-100 as a medium for simple extraction of DNA for PCR-based typing from forensic material. BioTechniques, 10, 506-513.
94. Ward RD, Holmes BH, O’Hara TD (2008) DNA barcoding discriminates echinoderm species. Molecular Ecology Resources, 8, 1202-1211.
95. Waters JM, O’Loughlin PM, Roy MS (2004) Cladogenesis in a starfish species complex from southern Australia: evidence for vicariant speciation? Molecular Phylogenetics and Evolution, 32, 236-245.
96. White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: PCR Protocols, A Guide to Methods and Applications (eds Innis MA, Gelfand DH, Sninsky JJ, White TJ), pp. 315-322. Academic Press, San Diego, California.