Multilocus evidence for globally distributed cryptic species and distinct populations across ocean gyres in a mesopelagic copepod

Molecular Ecology

Volumn 23, Issue 22, 2014, Pages 5462-5479

  Andrews, Kimberly R ^a,b   Norton, Emily L ^a   Fernandez Silva, Iria ^c,d   Portner, Elan ^a   Goetze, Erica ^a  

^a UNIVERSITY OF HAWAII   (United States)

^b DURHAM UNIVERSITY   (United Kingdom)

^c UNIVERSITY OF HAWAII   (United States)

^d CALIFORNIA ACADEMY OF SCIENCES   (United States)

Author keywords

connectivity; holoplankton; marine; microsatellites; pelagic; zooplankton

Indexed keywords

COPEPODA; HALOPTILUS LONGICORNIS;

MICROSATELLITE DNA; MITOCHONDRIAL DNA;

ANIMAL; ANIMAL DISPERSAL; ATLANTIC OCEAN; COPEPOD; DNA SEQUENCE; EVOLUTION; GENE FLOW; GENETICS; GENOTYPE; MOLECULAR GENETICS; PACIFIC OCEAN; POPULATION GENETICS; SYMPATRY;

ANIMAL DISTRIBUTION; ANIMALS; ATLANTIC OCEAN; BIOLOGICAL EVOLUTION; COPEPODA; DNA, MITOCHONDRIAL; GENE FLOW; GENETICS, POPULATION; GENOTYPE; MICROSATELLITE REPEATS; MOLECULAR SEQUENCE DATA; PACIFIC OCEAN; SEQUENCE ANALYSIS, DNA; SYMPATRY;

EID: 84936796841     PISSN: 09621083     EISSN: 1365294X     Source Type: Journal    
DOI: 10.1111/mec.12950     Document Type: Article

References (107)

1. Ambler JW, Miller CB, (1987) Vertical habitat-partitioning by copepodites and adults of subtropical oceanic copepods. Marine Biology, 94, 561-577.
2. Andersen NM, Cheng L, Damgaard J, Sperling FAH, (2000) Mitochondrial DNA sequence variation and phylogeography of oceanic insects (Hemiptera: Gerridae: Halobates spp.). Marine Biology, 136, 421-430.
3. Andrews KR, Karczmarski L, Au WWL, et al,. (2010) Rolling stones and stable homes: social structure, habitat diversity, and population genetics of the Hawaiian spinner dolphin (Stenella longirostris). Molecular Ecology, 19, 732-748.
4. Angel MV, (1992) Pelagic biodiversity. In: Diversity of Oceanic Life: An Evaluative Review (ed., Peterson NA,), pp. 35-68. The Center for Strategic and International Studies, Washington, District of Columbia.
5. ST-outlier method. BMC Bioinformatics, 9, 1-5.
6. Avise JC, (2004) Molecular Markers, Natural History, and Evolution. Sinauer Associates, Inc, Sunderland, Massachusetts.
7. Ball RM, Neigel JE, Avise JC, (1990) Gene genealogies within the organismal pedigrees of random-mating populations. Evolution, 44, 360-370.
8. Balloux F, Brunner H, Lugon-Moulin N, Hausser J, Goudet J, (2000) Microsatellites can be misleading: an empirical and simulation study. Evolution, 54, 1414-1422.
9. Beaugrand G, Reid PC, Ibanez F, Lindley JA, Edwards M, (2002) Reorganization of North Atlantic marine copepod biodiversity and climate. Science, 296, 1692-1694.
10. Beaugrand G, Luczak C, Edwards M, (2009) Rapid biogeographical plankton shifts in the North Atlantic Ocean. Global Change Biology, 15, 1790-1803.
11. Belkhir K, Borsa P, Chikhi L, Raufaste N, Bonhomme F, (1996-2004) GENETIX 4.05, Logiciel Sous Windows TM Pour La Génétique Des Populations. Laboratoire Génome, Populations, Interactions, CNRS UMR 5000. Université de Montpellier II, Montpellier, France.
12. Birky CW, Maruyama T, Fuerst P, (1983) An approach to population and evolutionary genetic theory for genes in mitochondria and chloroplasts, and some results. Genetics, 103, 513-527.
13. Blanco-Bercial L, Alvarez-Marques F, Bucklin A, (2011) Comparative phylogeography and connectivity of sibling species of the marine copepod Clausocalanus (Calanoida). Journal of Experimental Marine Biology and Ecology, 404, 108-115.
14. Blanco-Bercial L, Cornils A, Copley N, Bucklin A, (2014) DNA barcoding of marine copepods: assessment of analytical approaches to species identification. PLoS currents, 6, 1-24.
15. Bouckaert R, Heled J, Kuhnert D, et al,. (2014) BEAST 2: a software platform for bayesian evolutionary analysis. PLoS computational biology, 10, e1003537.
16. Boutin-Ganache I, Raposo M, Raymond M, Deschepper CF, (2001) M13-tailed primers improve the readability and usability of microsatellite analyses performed with two different allele-sizing methods. BioTechniques, 31, 24-28.
17. Bowen BW, Bass AL, Soares L, Toonen RJ, (2005) Conservation implications of complex population structure: lessons from the loggerhead turtle (Caretta caretta). Molecular Ecology, 14, 2389-2402.
18. Bradford-Grieve JM, (1999) The marine fauna of New Zealand: pelagic calanoid Copepoda: Bathypontiidae, Arietellidae, Augaptilidae, Heterorhabdidae, Lucicutiidae, Metridinidae, Phyllopodidae, Centropagidae, Pseudodiaptomidae, Temoridae, Candaciidae, Pontellidae, Sulcanidae, Acartiidae, Tortanidae. NIWA Biodiversity Memoir, 111, 1-268.
19. Bucklin A, Kaartvedt S, Guarnieri M, Goswami U, (2000) Population genetics of drifting (Calanus spp.) and resident (Acartia clausi) plankton in Norwegian fjords. Journal of Plankton Research, 22, 1237-1251.
20. Buonaccorsi VP, McDowell JR, Graves JE, (2001) Reconciling patterns of inter-ocean molecular variance from four classes of molecular markers in blue marlin (Makaira nigricans). Molecular Ecology, 10, 1179-1196.
21. Chapuis MP, Estoup A, (2007) Microsatellite null alleles and estimation of population differentiation. Molecular Biology and Evolution, 24, 621-631.
22. Chen G, Hare MP, (2008) Cryptic ecological diversification of a planktonic estuarine copepod, Acartia tonsa. Molecular Ecology, 17, 1451-1468.
23. Chen G, Hare MP, (2011) Cryptic diversity and comparative phylogeography of the estuarine copepod Acartia tonsa on the US Atlantic coast. Molecular Ecology, 20, 2425-2441.
24. Churchill CKC, Alejandrino A, Valdes A, Foighil DO, (2013) Parallel changes in genital morphology delineate cryptic diversification of planktonic nudibranchs. Proceedings of the Royal Society B-Biological Sciences, 280, 1-5.
25. Churchill CKC, Valdés Á, Foighil DÓ, (2014) Afro-Eurasia and the Americas present barriers to gene flow for the cosmopolitan neustonic nudibranch Glaucus atlanticus. Marine Biology, 161, 899-910.
26. Darling KF, Wade CA, (2008) The genetic diversity of planktic foraminifera and the global distribution of ribosomal RNA genotypes. Marine Micropaleontology, 67, 216-238.
27. Darling KF, Kucera M, Wade CM, (2007) Global molecular phylogeography reveals persistent Arctic circumpolar isolation in a marine planktonic protist. Proceedings of the National Academy of Sciences, USA, 104, 5002-5007.
28. Dawson MN, (2005) Incipient speciation of Catostylus mosaicus (Scyphozoa, Rhizostomeae, Catostylidae), comparative phylogeography and biogeography in south-east Australia. Journal of Biogeography, 32, 515-533.
29. Dawson MN, Jacobs DK, (2001) Molecular evidence for cryptic species of Aurelia aurita (Cnidaria, Scyphozoa). Biological Bulletin, 200, 92-96.
30. DiBattista JD, Rocha LA, Craig MT, Feldheim KA, Bowen BW, (2012) Phylogeography of two closely related Indo-Pacific butterflyfishes reveals divergent evolutionary histories and discordant results from mtDNA and microsatellites. Journal of Heredity, 103, 617-629.
31. Dooh RT, Adamowicz SJ, Hebert PDN, (2006) Comparative phylogeography of two North American 'glacial relict' crustaceans. Molecular Ecology, 15, 4459-4475.
32. Earl DA, Vonholdt BM, (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conservation Genetics Resources, 4, 359-361.
33. Eble JA, Toonen RJ, Sorenson L, et al,. (2011) Escaping paradise: larval export from Hawaii in an Indo-Pacific reef fish, the yellow tang Zebrasoma flavescens. Marine Ecology Progress Series, 428, 245-258.
34. Echelle AA, Hackler JC, Lack JB, et al,. (2010) Conservation genetics of the alligator snapping turtle: cytonuclear evidence of range-wide bottleneck effects and unusually pronounced geographic structure. Conservation Genetics, 11, 1375-1387.
35. Estoup A, Jarne P, Cornuet JM, (2002) Homoplasy and mutation model at microsatellite loci and their consequences for population genetics analysis. Molecular Ecology, 11, 1591-1604.
36. Evanno G, Regnaut S, Goudet J, (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Molecular Ecology, 14, 2611-2620.
37. Excoffier L, Laval LG, Schneider S, (2005) Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evolutionary Bioinformatics Online, 1, 47-50.
38. Fernandez-Silva I, Toonen RJ, (2013) Optimizing selection of microsatellite loci from 454 pyrosequencing via post-sequencing bioinformatic analyses. Methods in Molecular Biology (Clifton, N.J.) 1006, 101-120.
39. Fernandez-Silva I, Whitney J, Wainwright B, et al,. (2013) Microsatellites for next-generation ecologists: a post-sequencing bioinformatics pipeline. PLoS ONE, 8, 1-7.
40. Fleminger A, (1986) The Pleistocene equatorial barrier between the Indian and Pacific Oceans and a likely cause for Wallace's line. In: Pelagic biogeography (eds Pierrot-Bults AC, van der Spoel S, Aahuraner BJ, Johnson RK), pp. 84-97. UNESCO Technical Papers in Marine Science, Paris, France. no. 49.
41. Fleminger A, Hulseman K, (1974) Systematics and distribution of four sibling species comprising the genus Pontellina Dana (Copepoda, Calanoida). Fishery Bulletin, 72, 63-120.
42. Fu YX, (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics, 147, 915-925.
43. Gaither MR, Rocha LA, (2013) Origins of species richness in the Indo-Malay-Philippine biodiversity hotspot: evidence for the centre of overlap hypothesis. Journal of Biogeography, 40, 1638-1648.
44. Gaither MR, Toonen RJ, Sorenson L, Bowen BW, (2010) Isolation and characterization of microsatellite markers for the Crimson Jobfish, Pristipomoides filamentosus (Lutjanidae). Conservation Genetics Resources, 2, 169-172.
45. Goetze E, (2003) Cryptic speciation on the high seas; global phylogenetics of the copepod family Eucalanidae. Proceedings of the Royal Society B-Biological Sciences, 270, 2321-2331.
46. Goetze E, (2005) Global population genetic structure and biogeography of the oceanic copepods Eucalanus hyalinus and E. spinifer. Evolution, 59, 2378-2398.
47. Goetze E, (2010) Species discovery in marine planktonic invertebrates through global molecular screening. Molecular Ecology, 19, 952-967.
48. Goetze E, (2011) Population differentiation in the open sea: insights from the pelagic copepod Pleuromamma xiphias. Integrative and Comparative Biology, 51, 580-597.
49. Goudet J, (2001) FSTAT, a program to estimate and test gene diversities and fixation indices, http://www.unil.ch/izea/softwares/fstat.html.
50. Hayward TL, (1981) Mating and the depth distribution of an oceanic copepod. Limnology and Oceanography, 26, 374-377.
51. Hedrick PW, (1999) Highly variable loci and their interpretation in evolution and conservation. Evolution, 53, 313-318.
52. Hirai J, Shimode S, Tsuda A, (2013) Evaluation of ITS2-28S as a molecular marker for identification of calanoid copepods in the subtropical western North Pacific. Journal of Plankton Research, 35, 644-656.
53. Huang HT, Knowles LL, (2009) What is the danger of the anomaly zone for empirical phylogenetics? Systematic Biology, 58, 527-536.
54. Kienast M, Kienast SS, Calvert SE, et al,. (2006) Eastern Pacific cooling and Atlantic overturning circulation during the last deglaciation. Nature, 443, 846-849.
55. Lawrence KT, Liu ZH, Herbert TD, (2006) Evolution of the eastern tropical Pacific through Plio-Pleistocene glaciation. Science, 312, 79-83.
56. Longhurst AR, (2007) Ecological geography of the sea. 2nd edn. Academic Press, San Diego, CA, USA.
57. Lukoschek V, Waycott M, Keogh JS, (2008) Relative information content of polymorphic microsatellites and mitochondrial DNA for inferring dispersal and population genetic structure in the olive sea snake, Aipysurus laevis. Molecular Ecology, 17, 3062-3077.
58. Lyrholm T, Leimar O, Johanneson B, Gyllensten U, (1999) Sex-biased dispersal in sperm whales: contrasting mitochondrial and nuclear genetic structure of global populations. Proceedings of the Royal Society of London Series B-Biological Sciences, 266, 347-354.
59. Machida RJ, Hashiguchi Y, Nishida M, Nishida S, (2009) Zooplankton diversity analysis through single-gene sequencing of a community sample. BMC Genomics, 10, 1-7.
60. Maddison WP, (1997) Gene trees in species trees. Systematic Biology, 46, 523-536.
61. Marrone F, Lo Brutto S, Hundsdoerfer AK, Arculeo M, (2013) Overlooked cryptic endemism in copepods: systematics and natural history of the calanoid subgenus Occidodiaptomus Borutzky 1991 (Copepoda, Calanoida, Diaptomidae). Molecular Phylogenetics and Evolution 66, 190-202.
62. Mauchline J, (1998) The Biology of Calanoid Copepods. Academic Press, San Diego, California.
63. McGowan JA, Walker PW, (1979) Structure in the copepod community of the North Pacific central gyre. Ecological Monographs, 49, 195-226.
64. Meglécz E, Costedoat C, Dubut V, et al,. (2010) QDD: a user-friendly program to select microsatellite markers and design primers from large sequencing projects. Bioinformatics, 26, 403-404.
65. Miller KG, Kominz MA, Browning JV, et al,. (2005) The phanerozoic record of global sea-level change. Science, 310, 1293-1298.
66. Milligan PJ, Stahl EA, Schizas NV, Turner JT, (2011) Phylogeography of the copepod Acartia hudsonica in estuaries of the northeastern United States. Hydrobiologia, 666, 155-165.
67. Miyamoto H, Machida RJ, Nishida S, (2010) Genetic diversity and cryptic speciation of the deep sea chaetognath Caecosagitta macrocephala (Fowler, 1904). Deep-Sea Research. Part II, Topical Studies in Oceanography, 57, 2211-2219.
68. Mori T, (1964) The pelagic Copepoda from the neighboring waters of Japan. 2nd edn. Soyo Company, Tokyo.
69. Muths D, Tessier E, Gouws G, et al,. (2011) Restricted dispersal of the reef fish Myripristis berndti at the scale of the SW Indian Ocean. Marine Ecology Progress Series, 443, 167-180.
70. Neigel JE, Avise JC, (1986) Phylogenetic relationships of mitochondrial DNA under various demographic models of speciation. In: Evolutionary Processes and Theory (eds, Nevo E, Karlin S,), pp. 515-534. Academic Press, New York.
71. Nelson RJ, Carmack EC, McLaughlin FA, Cooper GA, (2009) Penetration of Pacific zooplankton into the western Arctic Ocean tracked with molecular population genetics. Marine Ecology Progress Series, 381, 129-138.
72. Norris RD, (2000) Pelagic species diversity, biogeography, and evolution. Paleobiology, 26, 236-258.
73. Norton E, Goetze E, (2013) Equatorial dispersal barriers and limited population connectivity among oceans in a planktonic copepod. Limnology and Oceanography, 58, 1581-1596.
74. ST and microsatellite polymorphism in the marine fish, walleye pollock (Theragra chalcogramma): implications for resolving weak population structure. Molecular Ecology, 13, 1799-1814.
75. Paffenhöfer GA, Mazzocchi MG, (2003) Vertical distribution of subtropical epiplanktonic copepods. Journal of Plankton Research, 25, 1139-1156.
76. Palumbi SR, (1992) Marine speciation on a small planet. Trends in Ecology & Evolution, 7, 114-118.
77. Papadopoulos LN, Peijnenburg K, Luttikhuizen PC, (2005) Phylogeography of the calanoid copepods Calanus helgolandicus and C. euxinus suggests Pleistocene divergences between Atlantic, Mediterranean, and Black Sea populations. Marine Biology, 147, 1353-1365.
78. Papetti C, Zane L, Bortolotto E, Bucklin A, Patarnello T, (2005) Genetic differentiation and local temporal stability of population structure in the euphausiid Meganyctiphanes norvegica. Marine Ecology Progress Series, 289, 225-235.
79. Patarnello T, Papetti C, Zane L, (2010) Genetics of northern krill (Meganyctiphanes norvegica Sars). In: Advances in Marine Biology, Vol 57 (ed., Tarling GA,), pp. 41-57. Academic Press, San Diego, CA, USA.
80. Paytan A, Lyle M, Mix A, Chase Z, (2004) Climatically driven changes in oceanic processes throughout the equatorial Pacific. Paleoceanography, 19, 1-6.
81. Peijnenburg KTCA, Goetze E, (2013) High evolutionary potential of marine zooplankton. Ecology & Evolution, 3, 2765-2783.
82. Peijnenburg KTCA, Breeuwer JAJ, Pierrot-Bults AC, Menken SBJ, (2004) Phylogeography of the planktonic chaetognath Sagitta setosa reveals isolation in European seas. Evolution, 58, 1472-1487.
83. Peijnenburg KTCA, van Haastrecht EK, Fauvelot C, (2005) Present-day genetic composition suggests contrasting demographic histories of two dominant chaetognaths of the North-East Atlantic, Sagitta elegans and S-setosa. Marine Biology, 147, 1279-1289.
84. Peijnenburg KTCA, Fauvelot C, Breeuwer AJ, Menken SBJ, (2006) Spatial and temporal genetic structure of the planktonic Sagitta setosa (Chaetognatha) in European seas as revealed by mitochondrial and nuclear DNA markers. Molecular Ecology, 15, 3319-3338.
85. Posada D, (2008) jModelTest: phylogenetic model averaging. Molecular Biology and Evolution, 25, 1253-1256.
86. Pritchard JK, Stephens M, Donnelly P, (2000) Inference of population structure using multilocus genotype data. Genetics, 155, 945-959.
87. Rea DK, Pisias NG, Newberry T, (1991) Late Pleistocene paleoclimatology of the central equatorial Pacific: flux patterns of biogenic sediments. Paleoceanography, 6, 227-244.
88. Roe HSJ, (1984) The diel migrations and distributions within a mesopelagic community in the North East Atlantic. 4. The Copepods. Progress in Oceanography, 13, 353-388.
89. Rozen S, Skaletsky HJ, (2000) Primer3 on the WWW for general users and for biologist programmers. In: Bioinformatics Methods and Protocols: Methods in Molecular Biology (eds, Krawetz S, &, Misener S,), pp. 365-386. Humana Press, Totowa, New Jersey.
90. Sars G, (1902) An Account of the Crustacea of Norway with Short Descriptions and Figures of All the Species. Bergen Museum, Bergen, Norway.
91. Schrey AW, Heist EJ, (2003) Microsatellite analysis of population structure in the shortfin mako (Isurus oxyrinchus). Canadian Journal of Fisheries and Aquatic Sciences, 60, 670-675.
92. Schroth W, Jarms G, Streit B, Schierwater B, (2002) Speciation and phylogeography in the cosmopolitan marine moon jelly, Aurelia sp. Bmc Evolutionary Biology, 2, 1-10.
93. Seears HA, Darling KF, Wade CM, (2012) Ecological partitioning and diversity in tropical planktonic foraminifera. Bmc Evolutionary Biology, 12, 1-15.
94. Sexton PF, Norris RD, (2008) Dispersal and biogeography of marine plankton: long-distance dispersal of the foraminifer Truncorotalia truncatulinoides. Geology, 36, 899-902.
95. Shaw PW, Arkhipkin AI, Al-Khairulla H, (2004) Genetic structuring of Patagonian toothfish populations in the Southwest Atlantic Ocean: the effect of the Antarctic Polar Front and deep-water troughs as barriers to genetic exchange. Molecular Ecology, 13, 3293-3303.
96. van der Spoel S, Heyman RP, (1983) A Comparative Atlas of Zooplankton: Biological Patterns in the Oceans. Wetenschappelijke Uitgeverij Bunge, Utrecht, the Netherlands.
97. Stamatakis A, Hoover P, Rougemont J, (2008) A rapid bootstrap algorithm for the RAxML web servers. Systematic Biology, 57, 758-771.
98. Tajima F, (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics, 123, 585-595.
99. Takahata N, (1989) Gene genealogy in 3 related populations: consistency probability between gene and population trees. Genetics, 122, 957-966.
100. Thum RA, Harrison RG, (2009) Deep genetic divergences among morphologically similar and parapatric Skistodiaptomus (Copepoda: Calanoida: Diaptomidae) challenge the hypothesis of Pleistocene speciation. Biological Journal of the Linnean Society, 96, 150-165.
101. Van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P, (2004) MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Molecular Ecology Notes, 4, 535-538.
102. de Vargas C, Norris R, Zaninetti L, Gibb SW, Pawlowski J, (1999) Molecular evidence of cryptic speciation in planktonic foraminifers and their relation to oceanic provinces. Proceedings of the National Academy of Sciences, USA, 96, 2864-2868.
103. Weiner A, Aurahs R, Kurasawa A, Kitazato H, Kucera M, (2012) Vertical niche partitioning between cryptic sibling species of a cosmopolitan marine planktonic protist. Molecular Ecology, 21, 4063-4073.
104. Whitlock MC, (1992) Temporal fluctuations in demographic parameters and the genetic variances among populations. Evolution, 46, 608-615.
105. Wilson AC, Cann RL, Carr SM, et al,. (1985) Mitochondrial DNA and two perspectives on evolutionary genetics. Biological Journal of the Linnean Society, 26, 375-400.
106. Wright S, (1931) Evolution in mendelian populations. Genetics, 16, 97-159.
107. Yebra L, Bonnet D, Harris RP, Lindeque PK, Peijnenburg KTCA, (2011) Barriers in the pelagic: population structuring of Calanus helgolandicus and C. euxinus in European waters. Marine Ecology Progress Series, 428, 135-149.