Evolutionary Biology

, Volume 41, Issue 1, pp 154–165 | Cite as

Adaptive Evolution of Deep-Sea Amphipods from the Superfamily Lysiassanoidea in the North Atlantic

  • Laura J. Corrigan
  • Tammy Horton
  • Heather Fotherby
  • Thomas A. White
  • A. Rus Hoelzel
Research Article

Abstract

In this study we reconstruct phylogenies for deep sea amphipods from the North Atlantic in order to test hypotheses about the evolutionary mechanisms driving speciation in the deep sea. We sequenced five genes for specimens representing 21 families. Phylogenetic analyses showed incongruence between the molecular data and morphological taxonomy, with some morphologically distinct taxa showing close molecular similarity. Approximate dating of nodes based on available calibration suggested adaptation to the deep sea around the Cretaceous-Palaeogene boundary, with three identified lineages within the deep-sea radiation dating to the Eocene–Oligocene transition. Two of those lineages contained species currently classified in multiple families. We reconstructed ancestral nodes based on the mouthpart characters that define trophic guilds (also used to establish the current taxonomy), and show a consistent transition at the earliest node defining the deep-sea lineage, together with increasing diversification at more recent nodes within the deep-sea lineage. The data suggest that the divergence of species was adaptive, with successive diversification from a non-scavenging ancestor to ‘opportunistic’, ‘obligate’ and ‘specialised’ scavengers. We propose that the North Atlantic species studied provide a strong case for adaptive evolution promoted by ecological opportunity in the deep sea.

Keywords

Deep sea Amphipod Invertebrate Adaptation Phylogenetics Evolution 

Notes

Acknowledgments

We thank the crew and scientists on board James Cook, during the ECOMAR cruises 2007–2010 for collecting the samples. In particular we are very grateful to Ben Boorman, Alan Hughes and Grant Duffy for operating the baited traps and dealing with the samples at sea. This work is supported by NERC Grant NE/C51297X/1. We thank Ulrike Englisch and Charles Coleman at the Museum für Naturkunde in Berlin for the provision of materials for analysis representing the outgroup species. The funding agency played no role in study design, the collection, analysis and interpretation of data, in the writing of the report, or in the decision to submit the article for publication.

Supplementary material

11692_2013_9255_MOESM1_ESM.doc (3 mb)
Supplementary material 1 (DOC 3112 kb)

References

  1. Baker, R. H., & DeSalle, R. (1997). Multiple sources of character information and the phylogeny of Hawaiian Drosophilids. Systematic Biology, 46, 654–673.PubMedCrossRefGoogle Scholar
  2. Barnard, J. L., & Karaman, G. S. (1991). The families and genera of marine gammaridean Amphipoda (except marine gammaroids). Records of the Australian Museum, Supplement 13 (parts 1 and 2), 1–866.Google Scholar
  3. Benson, R. H., Chapman, R. E., & Deck, L. T. (1985). Evidence from the Ostracoda of major events in the South Atlantic and world-wide over the past 80 million years. In: Hsü, K., & Weissert, H. (Eds.), South Atlantic Paleoceanography. Cambridge University Press, Cambridge, pp. 205–241.Google Scholar
  4. Bierne, N., Bonhomme, F., & David, P. (2003). Habitat preference and the marine-speciation paradox. Proceedings of Biological Society, 270, 1399–1406.CrossRefGoogle Scholar
  5. Bousfield, E. L., & Shih, C. (1994). The phyletic classification of amphipod crustaceans: Problems in resolution. Amphipacifica, 1, 76–134.Google Scholar
  6. Chan, K. M. A., & Moore, B. R. (2002). Whole-tree methods for detecting differential diversification rates. Systematic Biology, 51, 855–865.Google Scholar
  7. Chan, K. M. A., & Moore, B. R. (2005). SymmeTree: Whole-tree analysis of differential diversification rates. Bioinformatics, 21, 1709–1710.Google Scholar
  8. Clarke, A., & Johnston, I. A. (1996). Evolution and adaptive radiation of Antarctic fishes. Trends in Ecology & Evolution, 11, 212–218.Google Scholar
  9. Coleman, C. O. (2004). Aquatic amphipods (Crustacea: Amphipoda: Crangonyctidae) in three pieces of Baltic amber. Organisms, Diversity & Evolution, 4, 119–122.CrossRefGoogle Scholar
  10. Coleman, C. O. (2006). An amphipod of the genus Synurella Wrzesniowski, 1877 (Crustacea, Amphipoda, Crangonyctidae) found in Baltic amber. Organisms, Diversity & Evolution, 6, 103–108.CrossRefGoogle Scholar
  11. Coleman, C. O., & Myers, A. A. (2000). New Amphipoda from Baltic amber. Polski Archiwum Hydrobiologii, 47, 457–464.Google Scholar
  12. Cousins, N. J., Horton, T., Wigham, B. D., & Bagley, P. M. (2013). Abyssal scavenging demersal fauna of the sub Antarctic Crozet Plateau, Southern Indian Ocean. African Journal of Marine Science (in press).Google Scholar
  13. Dahl, E. (1979). Deep-sea carrion feeding amphipods: Evolutionary patterns in niche adaptation. Oikos, 33, 167–175.CrossRefGoogle Scholar
  14. De Broyer, C., Nyssen, F., & Dauby, P. (2004). The crustacean scavenger guild in Antarctic shelf, bathyal and abyssal communities. Deep-Sea Research II, 51, 1733–1752.CrossRefGoogle Scholar
  15. Diffenthal, M., & Horton, T. (2007). Stephonyx arabiensis (Crustacea: Amphipoda: Lysianassoidea: Uristidae), a new deep-water scavenger species from the Indian Ocean, with a key to the genus Stephonyx. Zootaxa, 1665(31–4), 1.Google Scholar
  16. Distel, D. D., Baco, A. R., Chuang, E., Morrill, W., Cavanaugh, C., & Smith, C. R. (2000). Do mussels take wooden steps to deep-sea vents? Nature, 403, 725–726.PubMedCrossRefGoogle Scholar
  17. Englisch, U., Coleman, C. O., & Wägele, J. W. (2003). First observations on the phylogeny of the families Gammaridae, Crangonyctidae, Melitidae, Niphargidae, Megaluropidae and Oedicerotidae (Amphipoda, Crustacea), using small subunit rDNA gene sequences. Journal of Natural History, 37, 2461–2486.CrossRefGoogle Scholar
  18. Fišer, C., Sket, B., & Trontelj, P. (2008). A phylogenetic perspective on 160 years of troubled taxonomy of Niphargus (Crustacea: Amphipoda). Zoologica Scripta, 37, 665–680.CrossRefGoogle Scholar
  19. Grassle, J. F. (1989). Species diversity in deep-sea communities. Trends in Ecology & Evolution, 4, 12–15.CrossRefGoogle Scholar
  20. Hargrave, B. T. (1985). Feeding rates of abyssal scavenging amphipods (Eurythenes gryllus) determined in situ by time-lapse photography. Deep-Sea Research, 32, 443–450.CrossRefGoogle Scholar
  21. Havermans, C., Nagy, Z. T., Sonet, G., De Broyer, C., & Martin, P. (2010). Incongruence between molecular phylogeny and morphological classification in amphipod crustaceans: A case study of Antarctic Lysianassoids. Molecular Phylogenetics and Evolution, 55, 202–209.PubMedCrossRefGoogle Scholar
  22. Hessler, R. R., Ingram, C. L., Yayanos, A. A., & Burnett, B. R. (1978). Scavenging amphipods from the floor of the Philippine Trench. Deep-Sea Research, 25, 1029–1047.CrossRefGoogle Scholar
  23. Hessler, R. R., & Sanders, H. L. (1967). Faunal diversity in the deep-sea. Deep Sea Research and Oceanographic Abstracts, 14, 65–70.CrossRefGoogle Scholar
  24. Horton, T., & Thurston, M. (2011). Centromedon zoe (Crustacea: Amphipoda: Lysianassoidea: Uristidae), a new deep-water scavenger species from the North Atlantic, with a key to the genus Centromedon. Zootaxa, 2869, 54–62.Google Scholar
  25. Horton, T., & Thurston, M. (2013). Hirondellea namarensis (Crustacea: Amphipoda: Lysianassoidea: Hirondelleidae), a new deep-water scavenger species from the Mid-Atlantic Ridge. Marine Biology Research, 9, 554–562.CrossRefGoogle Scholar
  26. Horton, T., Thurston, M., & Duffy, G. (2013) Community composition of scavenging amphipods at bathyal depths on the mid-atlantic ridge. Deep-Sea Research II. doi: 10.1016/j.dsr2.2013.01.032i.
  27. Hou, Z., Fu, J., & Li, S. (2007). A molecular phylogeny of the genus Gammarus (Crustacea: Amphipoda) based on mitochondrial and nuclear gene sequences. Molecular Phylogenetics and Evolution, 45, 596–611.PubMedCrossRefGoogle Scholar
  28. Hou, Z., Sket, B., Fišer, C., & Li, S. (2011). Eocene habitat shift from saline to freshwater promoted Tethyan amphipod diversification. Proceedings of the National Academy of Science, 108, 14533–14538.CrossRefGoogle Scholar
  29. Hurley, D. E. (1963). Amphipoda of the family Lysianassidae from the west coast of north and central America. Allan Hancock Foundation Occasional Papers, 25, 1–165.Google Scholar
  30. Ingram, T. (2011). Speciation along a depth gradient in a marine adaptive radiation. Proceedings of Royal Society B, 278, 613–618.CrossRefGoogle Scholar
  31. Ito, A., Wada, H., & Aoki, M. N. (2008). Phylogenetic analysis of caprellid and corophioid amphipods (crustacea) based on the 18S rRNA gene, with special emphasis on the phylogenetic position of phtisicidae. Biological Bulletin, 214, 176–183.PubMedCrossRefGoogle Scholar
  32. Jamieson, A. J., Fujii, T., Mayor, D. J., Solan, M., & Priede, I. G. (2010). Hadal trenches: The ecology of the deepest places on earth. Trends in Ecology & Evolution, 25, 190–197.CrossRefGoogle Scholar
  33. Jazdzewski, K., & Kulicka, R. (2000). A note on amphipod crustaceans in a piece of Baltic amber. Annales Zoologici, 50, 99–100.Google Scholar
  34. Jazdzewski, K., & Kulicka, R. (2002). New fossil amphipod, Palaeogammarus polonicus n. sp., from the Baltic amber. Acta Geologica Polonica, 3, 379–383.Google Scholar
  35. Kaiho, K. (1998). Phylogeny of deep-sea calcareous trochospiral benthic Foraminifera: Evolution and diversification. Micropaleontology, 44, 291–311.CrossRefGoogle Scholar
  36. Lear, C. H., Bailey, T. R., Pearson, P. N., Coxall, H. K., & Rosenthall, Y. (2008). Cooling and ice growth across the Eocene-Oligocene transition. Geology, 36, 251–254.CrossRefGoogle Scholar
  37. Lowry, J. K., & Stoddart, H. E. (1992). A revision of the genus Ichnopus (Crustacea: Amphipoda: Lysianassoidea: Uristidae). Records of the Australian Museum, 44, 185–245.CrossRefGoogle Scholar
  38. Lowry, J. K., & Stoddart, H. E. (1997). Amphipoda Crustacea IV. Families Aristiidae, Cyphocarididae, Endevouridae, Lysianassidae, Scopelocheiridae, Uristidae. Memoirs of the Hourglass Cruises, 10, 148.Google Scholar
  39. Lowry, J. K., & Stoddart, H. E. (2009). Uristidae. In J. K. Lowry & A. A. Myers (Eds.), Amphipoda of the Great Barrier Reef (Vol. 2260, pp. 908–918). Australia: Zootaxa.Google Scholar
  40. Lowry, J. K., & Stoddart, H. E. (2010). The deep-sea scavenging genus Hirondellea (Crustacea: Amphipoda: Lysianassoidea: Hirondelleidae fam. nov.) in Australian waters. Zootaxa, 2329, 37–55.Google Scholar
  41. Macdonald, K. S. I. I. I., Yampolsky, L., & Duffy, J. E. (2005). Molecular and morphological evolution of the amphipod radiation in Lake Baikal. Molecular Phylogenetics and Evolution, 35, 323–343.PubMedCrossRefGoogle Scholar
  42. Marko, P. B. (2002). Fossil calibration of molecular clocks and the divergence times of geminate species pairs separated by the Isthmus of Panama. Molecular Biology and Evolution, 19, 2005–2021.Google Scholar
  43. Martin, J. W., & Davis, G. E. (2001). An updated classification of the recent crustacea. Natural History Museum of Los Angeles County, Science Series 39: vii–124.Google Scholar
  44. Miller, K. G., Fairbanks, R. G., & Mountain, G. S. (1987). Tertiary oxygen isotope synthesis, sea level history, and continental margin erosion. Paleoceanography, 2, 1–19.CrossRefGoogle Scholar
  45. Norris, R. D., Kroon, D., & Klaus, A. (2001). Introduction: Cretaceous–Paleogene climatic evolution of the western North Atlantic, results from ODP Leg 171B, Blake Nose. In: Kroon, D., Norris, R. D., & Klaus, A. (Eds.), Proceedings of ODP, Sci. Results, 171B, 1–11 [Online].Google Scholar
  46. Pagel, M., Meade, A., & Barker, D. (2004). Bayesian estimation of ancestral character states on phylogenies. Systematic Biology, 53, 673–684.PubMedCrossRefGoogle Scholar
  47. Palumbi, S. R. (1994). Genetic divergence, reproductive isolation, and marine speciation. Annual Review of Ecology and Systematics, 25, 547–572.CrossRefGoogle Scholar
  48. Pearson, P. N., McMillan, I. K., Wade, B. S., Jones, T. D., Coxall, H. K., Brown, P. R., et al. (2008). Extinction and environmental change across the Eocene–Oligocene boundary in Tanzania. Geology, 36, 179–182.CrossRefGoogle Scholar
  49. Posada, D. (2008). JModeltest: Phylogenetic model averaging. Molecular Biology and Evolution, 25, 1253–1256.PubMedCrossRefGoogle Scholar
  50. Premke, K., & Graeve, M. (2009). Metabolism and physiological traits of the deep sea amphipoda Eurythenes gryllus. Vie et milieu, 59, 251–260.Google Scholar
  51. Puebla, O. (2009). Ecological speciation in marine v. Freshwater fishes. Journal of Fish Biology, 75, 960–996.PubMedCrossRefGoogle Scholar
  52. Rambaut, A., & Drummond, A. J. (2007). Tracer v1.4, Available from http://beast.bio.ed.ac.uk/Tracer.
  53. Ronquist, F., & Huelsenbeck, J. P. (2003). MrBayes 3: Bayesion Phylogenetic inference under mixed models. Bioinformatics, 19, 1572–1574.PubMedCrossRefGoogle Scholar
  54. Schluter, D. (1996). Ecological causes of adaptive radiation. American Naturalist, 148(Suppl), S40–S64.CrossRefGoogle Scholar
  55. Schluter, D. (2000). Ecological character displacement in adaptive radiation. American Naturalist, 156(Suppl), S4–S16.Google Scholar
  56. Schluter, D., & Grant, P. R. (1984). Determinants of morphological patterns in communities of Darwin’s finches. American Naturalist, 123, 175–196.CrossRefGoogle Scholar
  57. Seehausen, O. (2006). African cichlid fish: A model system in adaptive radiation research. Proceedings of Royal Society B, 273, 1987–1998.CrossRefGoogle Scholar
  58. Shao, K. -T., & Sokal, R. R. (1990). Tree balance. Systematic Zoology, 39, 266–276.Google Scholar
  59. Smith, C. R. (1985). Food for the deep sea: Utilization, dispersal, and flux of nekton falls at the Santa Catalina Basin floor. Deep-Sea Research, 32, 417–442.CrossRefGoogle Scholar
  60. Smith, K. L., & Baldwin, R. J. (1982). Scavenging deep-sea amphipods: Effects of food odor on oxygen consumption and a proposed metabolic strategy. Marine Biology, 68, 287–298.CrossRefGoogle Scholar
  61. Sorenson, M. D. (1999). TreeRot, version 2. Boston: Boston University.Google Scholar
  62. Steeman, M. E., Hebsgaard, M. B., Fordyce, R. E., Ho, S. Y. W., Rabosky, D. L., Nielson, R., et al. (2009). Radiation of extant cetaceans driven by restructuring of the oceans. Systematic Biology, 58, 573–585.PubMedCrossRefGoogle Scholar
  63. Swofford, D. L. (2002). PAUP. Phylogenetic analysis using parsimony (and other methods). Version 4.0b10. Sinauer, Sunderland, Massachusetts.Google Scholar
  64. Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., & Kumar, S. (2011). MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution, 28, 2731–2739.PubMedCrossRefGoogle Scholar
  65. Taylor, M. S., & Hellberg, M. E. (2005). Marine radiations at small geographic scales: Speciation in neotropical reef gobies (Elacatinus). Evolution, 59, 374–385.Google Scholar
  66. Thompson, J. D., Gibson, T. J., Plewniak, F., Jeanmougin, F., & Higgins, D. G. (1997). The CLUSTAL X windows interface: Flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research, 25, 4876–4882.PubMedCentralPubMedCrossRefGoogle Scholar
  67. Thurston, M. H. (1979). Scavenging abyssal amphipods from the North-East Atlantic Ocean. Marine Biology, 51, 55–68.CrossRefGoogle Scholar
  68. Thurston, M. H. (1990). Abyssal necrophagous amphipods (Crustacea: Amphipoda) in the northeast and tropical Atlantic Ocean. Progress in Oceanography, 24, 257–274.CrossRefGoogle Scholar
  69. Wilson, G. D. F., & Hessler, R. R. (1987). Speciation in the Deep Sea. Annual Review of Ecology and Systematics, 18, 185–207.CrossRefGoogle Scholar
  70. Wolff, T. (1970). The concept of the hadal or ultra-abyssal fauna. Deep-Sea Research, 17, 983–1003.Google Scholar
  71. Zachos, J. C., Pagani, M., Sloan, L., Thomas, E., & Billups, K. (2001). Trends, rhythms, and aberrations in global climate change 65 Ma to present. Science, 292, 686–693.PubMedCrossRefGoogle Scholar
  72. Zenkevitch, L. A., & Birstein, J. A. (1960). On the problem of the antiquity of the deep-sea fauna. Deep-Sea Research, 7, 10–23.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2013

Authors and Affiliations

  • Laura J. Corrigan
    • 1
  • Tammy Horton
    • 2
  • Heather Fotherby
    • 1
  • Thomas A. White
    • 1
  • A. Rus Hoelzel
    • 1
  1. 1.School of Biological and Biomedical SciencesDurham UniversityDurhamUK
  2. 2.Ocean Biogeochemistry and Ecosystems, National Oceanography CentreUniversity of SouthamptonSouthamptonUK

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