Marine Biology

, Volume 157, Issue 6, pp 1357–1366 | Cite as

Phylogeography of the rock-pool copepod Tigriopus brevicornis (Harpacticoida) in the northern North Atlantic, and its relationship to other species of the genus

  • Lisa Handschumacher
  • María Björk Steinarsdóttir
  • Suzanne Edmands
  • Agnar Ingólfsson
Original Paper


We investigated relationships among North Atlantic Tigriopus brevicornis populations and their relationships to Mediterranean T. fulvus and North American T. californicus, using crossing experiments and mitochondrial DNA sequencing. All T. brevicornis populations tested were interfertile, while interspecific crosses produced either no offspring or offspring that did not survive past the larval stage, with the exception of a few T. brevicornis × T. californicus crosses that produced mature adults. DNA sequencing of a fragment of mitochondrial cytochrome oxidase I (COI) showed that samples of T. brevicornis from Iceland, the Faroes, Ireland, Scotland and Nova Scotia formed a single shallow clade. In contrast, T. brevicornis from more southern populations in France and Portugal formed a clade with substantially greater branch lengths. Tigriopus brevicornis was monophyletic, and T. brevicornis plus Mediterranean T. fulvus were together also monophyletic. The phylogeography of T. brevicornis closely mirrored that found in T. californicus, with substantially reduced interpopulation divergence at northern latitudes. The known distribution of T. brevicornis in Iceland and the Faroes is shown and dispersal mechanisms and habitat selection briefly discussed.


Nova Scotia Glacial Maximum Rocky Shore Faroe Island Chart Data 
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This project has been mainly financed by grants to AI from the Icelandic Research Fund and by the Sáttmálasjóður Trust Fund, which we acknowledge with gratitude. Thanks go to the students in the course Marine Ecology in the fall of 2004 for collecting samples and for taking part in investigations on habitats. We would like to single out especially Gunnar Þór Hallgrímsson, Yann Kolbeinsson and Freydís Vigfúsdóttir. Ólafur P. Ólafsson also deserves thanks for collecting specimens in Iceland, and Jörundur Svavarsson for collecting animals in Norway. The molecular portions of the study were financed by grants to SE from the US National Science Foundation (DEB-0316807 and DEB-0743472). Thanks go to J. P. McFarlane and Vanessa Knutson for assistance with initial sequencing efforts. The manuscript was greatly improved by the constructive criticism of three anonymous reviewers.


  1. Anonymous (2008) Sjávarfallatöflur 2008. Tide tables, vol 52. Sjómælingar Íslands, ReykjavíkGoogle Scholar
  2. Battaglia B (1982) Genetic variation and speciation events in marine copepods. In: Barrigozzi C (ed) Mechanisms of speciation. A.R.Liss, New York, pp 377–392Google Scholar
  3. Battaglia B, Bisol PM, Fava G, Rodino E, Varotto V (1985) Genetic variability and geographical differentiation in some benthic invertebrates from the Kerguelen Region. In: Gray JS, Christensen ME (eds) Marine biology of polar regions and effects of stress in marine organisms. Wiley, New York, pp 299–305Google Scholar
  4. Bradford JM (1967) The genus Tigriopus Norman (Copepoda: Harpacticoida) in New Zealand with a description of a new species. Trans Roy Soc NZ Zool 10:51–59Google Scholar
  5. Burton RS (1997) Genetic evidence for long term persistence of marine invertebrate populations in an ephemeral environment. Evolution 51:993–998CrossRefGoogle Scholar
  6. Burton RS, Lee B-N (1994) Nuclear and mitochondrial gene genealogies and allozyme polymorphism across a major phylogeographic break in the copepod Tigriopus californicus. Proc Natl Acad Sci USA 91:5197–5201CrossRefPubMedGoogle Scholar
  7. Carli A, Fiori A (1977) Morphological analysis of the two Tigriopus species found along the European coasts. Natura 68:101–110Google Scholar
  8. Carli A, Mariottini GL, Pane L (1995) Influence of nutrition on fecundity and survival in Tigriopus fulvus Fischer (Copepoda, Harpacticoida). Aquaculture 134:113–119CrossRefGoogle Scholar
  9. Davenport J, Barnett PRO, McAllen RJ (1997) Environmental tolerance to three species of the harpacticoid copepod genus Tigriopus. J mar biol Ass UK 77:3–16CrossRefGoogle Scholar
  10. Denis F, Ravallec R, Pavillon J-F, van Wormhoudt A (2009) Genetic differentiation of Atlantic populations of the intertidal copepod Tigriopus brevicornis. Sci Mar 73:579–587CrossRefGoogle Scholar
  11. Edmands S (1999) Heterosis and outbreeding depression in interpopulation crosses spanning a wide range of divergence. Evolution 53:1757–1768CrossRefGoogle Scholar
  12. Edmands S (2001) Phylogeography of the intertidal copepod Tigriopus californicus reveals substantially reduced population differentiation at northern latitudes. Mol Ecol 10:1743–1750CrossRefPubMedGoogle Scholar
  13. Edmands S (2002) Does parental divergence predict reproductive compatibility? Trends Ecol Evol 17:520–527CrossRefGoogle Scholar
  14. Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase from diverse metazoan invertebrates. Mol Mar Biol Biotechnol 3:294–299PubMedGoogle Scholar
  15. Ganz HH, Burton RS (1995) Genetic differentiation and reproductive incompatibility among Baja California populations of the copepod Tigriopus californicus. Mar Biol 123:821–827CrossRefGoogle Scholar
  16. Harrison JS, Peterson DL, Swain JR, Edmands S (2004) Microsatellite DNA markers for the intertidal copepod Tigriopus californicus. Mol Ecol Notes 4:736–738CrossRefGoogle Scholar
  17. Ingólfsson A (1992) The origin of the rocky shore fauna of Iceland and the Canadian Maritimes. J Biogeogr 19:705–712CrossRefGoogle Scholar
  18. Ingólfsson A (1996) The distribution of intertidal macrofauna on the coasts of Iceland in relation to temperature. Sarsia 81:29–44Google Scholar
  19. Ingólfsson A (2009) A marine refugium in Iceland during the last glacial maximum: fact or fiction? Zoologica Scripta 38:663–665CrossRefGoogle Scholar
  20. Ingólfsson A, Steinarsdóttir MB (2006) First records of two remarkable copepods (Copepoda, Harpacticoida) in the upper littoral fringe of eastern North America. Crustaceana 79:257–261CrossRefGoogle Scholar
  21. Johannesson K (1988) The paradox of Rockall: why is a brooding gastropod (Littorina saxatilis) more widespread than one having a planktonic dispersal stage (L. littorea)? Mar Biol 88:507–513CrossRefGoogle Scholar
  22. Jung S-O, Lee Y-M, Park T-J, Park HG, Hagiwara A, Leung KMY, Dahms H-U, Lee W, Lee J-S (2006) The complete mitochondrial genome of the intertidal copepod Tigriopus sp. (Copepoda, Harpactidae) from Korea and phylogenetic considerations. J Exp Mar Biol Ecol 333:251–262CrossRefGoogle Scholar
  23. Ki J-S, Lee K-Y, Park HG, Chullasorn S, Dahms H-U, Lee J-S (2008) Phylogeogaphy of the copepod Tigriopus japonicus along the Northwest Pacific rim. J Plankton Res 31:209–221CrossRefGoogle Scholar
  24. Lang K (1948) Monographie der Harpacticiden. Håkan Ohlssons boktryckeri, Lund, p 1682Google Scholar
  25. Lee B-N (1993) Genetic structure of Tigriopus californicus population inferred from mitochondrial cytochrome oxidase I sequences. Dissertation, University of HoustonGoogle Scholar
  26. Maggs CA, Castilho R, Foltz D, Henzler C, Jolly MT, Kelly J, Olsen J, Perez KE, Stam W, Vaainola R, Viard F, Wares J (2008) Evaluating signatures of glacial refugia for North Atlantic benthic species. Ecology 89(Supplement):108–122CrossRefGoogle Scholar
  27. McAllen R (1999) Enteromorpha intestinalis—a refugium for the supralittoral pool harpacticoid Tigriopus brevicornis. J Mar Biol Ass UK 79:1125–1126CrossRefGoogle Scholar
  28. McAllen R (2001) Hanging on in there—position maintenance by the high-shore rockpool harpacticoid copepod Tigriopus brevicornis. J Nat Hist 35:1821–1929CrossRefGoogle Scholar
  29. Petersen Æ (1998) Íslenskir fuglar. Vaka-Helgafell, Reykjavík, p 312Google Scholar
  30. Powlik JJ (1999) Habitat characters of Tigriopus californicus (Copepoda: Harpacticoida), with notes on the dispersal of supralittoral fauna. J Mar Biol Ass UK 79:85–92CrossRefGoogle Scholar
  31. Saiki RK, Gelfand DH, Stoffel S, Scharf SJ, Higuchi R, Horn GT, Mullis KB, Erlich HA (1988) Primer-directed enzymatic amplification of DNA with a thermostable DNA polymerase. Science 239:487–491CrossRefPubMedGoogle Scholar
  32. Sejrup HP, Hjelstuen BO, Dahlgren KIT, Haflidason H, Kuijpers A, Nygard A, Praeg D, Stoker MS, Vorren TO (2005) Pleistocene glacial history of the NW European margin. Mar Petrol Geol 22:1111–1129CrossRefGoogle Scholar
  33. Soyer J, Thiriotquievreux C, Colomines JC (1987) Description de deux espéces jumelles du groupe Tigriopus angulatus (Copepoda, Harpacticoida) dans les archipels Crozet et Kerguelen (Terres Australes et Antarctiques Francaises). Zool Scripta 16:143–154CrossRefGoogle Scholar
  34. Swanson GA (1984) Dissemination of amphipods by waterfowl. J Wildl Manag 48:988–991CrossRefGoogle Scholar
  35. Swofford DL (2003) PAUP*. Phylogenetic analysis using parsimony (*and other methods). Version 4. Sinauer Associates, SunderlandGoogle Scholar
  36. Vilela MH (1992) Mass culture and nutritional quality of the marine copepod Tigriopus brevicornis (Muller). Biol Inst Nac Invert Pescas Lisboa 17:49–63Google Scholar
  37. Waller CL, Worland MR, Convey P, Barnes DKA (2006) Ecophysiological strategies of Antarctic intertidal invertebrates faced with freezing stress. Polar Biol 29:1077–1083CrossRefGoogle Scholar
  38. Wares JP, Cunningham CW (2001) Phylogeography and historical ecology of the North Atlantic intertidal. Evolution 55:2455–2469PubMedGoogle Scholar
  39. Willett CS, Burton RS (2004) Evolution of interacting proteins in the mitochondrial electron transport system in a marine copepod. Mol Biol Evol 21(3):443–453CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  • Lisa Handschumacher
    • 1
  • María Björk Steinarsdóttir
    • 2
  • Suzanne Edmands
    • 1
  • Agnar Ingólfsson
    • 2
  1. 1.Department of Biological SciencesUniversity of Southern CaliforniaLos AngelesUSA
  2. 2.Institute of BiologyUniversity of IcelandReykjavíkIceland

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