Invertebrate Systematics Invertebrate Systematics Society
Systematics, phylogeny and biogeography
RESEARCH ARTICLE

DNA barcoding in Nautilus pompilius (Mollusca : Cephalopoda): evolutionary divergence of an ancient species in modern times

Rachel C. Williams A , Stephen J. Newman B and William Sinclair A C D

A Centre for Wildlife Conservation, Faculty of Science and Natural Resources, University of Cumbria, Penrith, CA11 0AH, United Kingdom.

B Western Australian Fisheries and Marine Research Laboratories, Department of Fisheries, Government of Western Australia, PO Box 20, North Beach, WA 6920, Australia.

C Centre for Environmental Management, CQUniversity, Rockhampton, Qld 4702, Australia.

D Corresponding author. Email: billy.sinclair@cumbria.ac.uk

Invertebrate Systematics 26(6) 548-560 http://dx.doi.org/10.1071/IS12023
Submitted: 11 April 2012  Accepted: 13 September 2012   Published: 19 December 2012

Abstract

DNA barcoding studies to elucidate the evolutionary and dispersal history of the current populations of Nautilus pompilius allow us to develop a greater understanding of their biology, their movement and the systematic relationships between different groups. Phylogenetic analyses were conducted on Australian N. pompilius, and COI sequences were generated for 98 discrete accessions. Sequences from samples collected across the distribution were sourced from GenBank and included in the analyses. Maximum likelihood revealed three distinct clades for N. pompilius: (1) populations sourced from west Australia, Indonesia and the Philippines; (2) populations collected from east Australia and Papua New Guinea; (3) western Pacific accessions from Vanuatu, American Samoa and Fiji, supporting previous findings on the evolutionary divergence of N. pompilius. A minimum spanning tree revealed 49 discrete haplotypes for the 128 accessions, from a total of 16 discrete sampling locations. Population similarity reflects oceanic topographic features, with divergence between populations across the N. pompilius range mirroring geographical separation. This illustrates the success of DNA barcoding as a tool to identify geographic origin, and looks to the future role of such technology in population genetics and evolutionary biology.

Additional keywords: coxI, conservation, population genetics.


References

Barrett, R. D. H., and Hebert, P. D. N. (2005). Identifying spiders through DNA barcodes. Canadian Journal of Zoology 83, 481–491.
Identifying spiders through DNA barcodes.CrossRef | 1:CAS:528:DC%2BD2MXmsFylsrk%3D&md5=5d97848a5e3ec787af951584a43f7920CAS | open url image1

Bonacum, J., Landman, N. H., Mapes, R. H., White, M. M., White, A. J., and Irlam, J. (2011). Evolutionary radiation of present-day Nautilus and Allonautilus. American Malacological Bulletin 29, 77–93.
Evolutionary radiation of present-day Nautilus and Allonautilus.CrossRef | open url image1

Bonnaud, L., Ozouf-Costaz, C., and Boucher-Rodoni, R. (2004). A molecular and karyological approach to the taxonomy of Nautilus. Comptes Rendus Biologies 327, 133–138.
A molecular and karyological approach to the taxonomy of Nautilus.CrossRef | 1:CAS:528:DC%2BD2cXhslegsLs%3D&md5=634d0d51fcec508329dbe551ec28f8f3CAS | open url image1

Caputo, V., Giovannotti, M., Nisi Cerioni, P., Splendiani, A., Marconi, M., and Tagliavini, J. (2009). Mitochondrial DNA variation of an isolated population of the Adriatic brook lamprey Lampetra zanandreai (Agnatha: Petromyzontidae): phylogeographic and phylogenetic inferences. Journal of Fish Biology 75, 2344–2351.
Mitochondrial DNA variation of an isolated population of the Adriatic brook lamprey Lampetra zanandreai (Agnatha: Petromyzontidae): phylogeographic and phylogenetic inferences.CrossRef | 1:CAS:528:DC%2BC3cXislantr8%3D&md5=91d0bc6b7a5aa4ba8795d6b7803f8e11CAS | open url image1

Carlson, B. A., McKibben, J. N., and DeGruy, M. V. (1984). Telemetric investigation of vertical migration of Nautilus belauensis in Palau. Pacific Science 38, 183–188. open url image1

Carlson, B., Awai, M., and Arnold, J. (1992). Hatching and early growth of Nautilus belauensis and implications on the distribution of the genus. The Nautilus 1, 587–592. open url image1

Chesser, R. K. (1991). Influence of gene flow and breeding tactics on gene diversity within populations. Genetics 129, 573–583.
| 1:STN:280:DyaK38%2FnslCjsQ%3D%3D&md5=5386ce5a08d54436e3bfe73729c872aaCAS | open url image1

Crook, R. J., Hanlon, R. T., and Basil, J. A. (2009). Memory of visual and topographical features suggests spatial learning in Nautilus (Nautilus pompilius). Journal of Comparative Psychology 123, 264–274.
Memory of visual and topographical features suggests spatial learning in Nautilus (Nautilus pompilius).CrossRef | open url image1

Doguzhaeva, L. A., Summesberger, H., Mutvei, H., and Brandstaetter, F. (2007). The mantle, ink sac, ink, arm hooks and soft body debris associated with the shells in Late Triassic coleoid cephalopod Phragmoteuthis from the Austrian Alps. Palaeoworld 16, 272–284.
The mantle, ink sac, ink, arm hooks and soft body debris associated with the shells in Late Triassic coleoid cephalopod Phragmoteuthis from the Austrian Alps.CrossRef | open url image1

Dunstan, A., Alanis, O., and Marshall, J. (2010). Nautilus pompilius fishing and population decline in the Philippines: a comparison with an unexploited Australian Nautilus population. Fisheries Research 106, 239–247.
Nautilus pompilius fishing and population decline in the Philippines: a comparison with an unexploited Australian Nautilus population.CrossRef | open url image1

Frankham, R., Ballou, J. D., and Briscoe, D. A. (2004). ‘A Primer of Conservation Genetics.’ (Cambridge University Press: Cambridge, UK.)

Genin, A., Dayton, P. K., Lonsdale, P. F., and Spiess, F. N. (1986). Corals on seamount peaks provide evidence of current acceleration over deep-sea topography. Nature 322, 59–61.
Corals on seamount peaks provide evidence of current acceleration over deep-sea topography.CrossRef | open url image1

Greenfest-Allen, E., Landman, N. H., and Saunders, W. B. (2010). Nautilus and Allonautilus: annotated bibliography of references published since 1987. In ‘Nautilus: the Biology and Paleobiology of a Living Fossil’. (Eds W. B. Saunders, and N. H. Landman.) pp. xxxix–lxxvii. (Springer: New York.)

Griffiths, A. M., Koizumi, I., Bright, D., and Stevens, J. R. (2009). A case of isolation by distance and short-term temporal stability of population structure in brown trout (Salmo trutta) within the River Dart, southwest England. Evolutionary Applications 2, 537–554.
A case of isolation by distance and short-term temporal stability of population structure in brown trout (Salmo trutta) within the River Dart, southwest England.CrossRef | open url image1

Harrison, J. C., and Langdale, J. A. (2006). A step by step guide to phylogeny reconstruction. The Plant Journal 45, 561–572.
A step by step guide to phylogeny reconstruction.CrossRef | 1:CAS:528:DC%2BD28XislWit7o%3D&md5=7592855fd5913cc877d656de2941a71cCAS | open url image1

Hebert, P. D. N., Cywinska, A., Ball, S. L., and DeWaard, J. R. (2003a). Biological identifications through DNA barcodes. Proceedings of the Royal Society of London. Series B. Biological Sciences 270, 313.
Biological identifications through DNA barcodes.CrossRef | 1:CAS:528:DC%2BD3sXktVWiu7g%3D&md5=bacde07336013937477a1e8839a85156CAS | open url image1

Hebert, P. D. N., Ratnasingham, S., and de Waard, J. R. (2003b). Barcoding animal life: cytochrome c oxidase subunit 1 divergences among closely related species. Proceedings of the Royal Society of London. Series B. Biological Sciences 270, 96–99.
Barcoding animal life: cytochrome c oxidase subunit 1 divergences among closely related species.CrossRef | open url image1

Hewitt, G. (2004). Genetic consequences of climatic oscillations in the Quaternary. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 359, 183–195.
Genetic consequences of climatic oscillations in the Quaternary.CrossRef | 1:STN:280:DC%2BD2c3gsVSjuw%3D%3D&md5=8b4e794e4f855100e25da612e7ac68a5CAS | open url image1

Hindar, K., Jonsson, B., Ryman, N., and Ståhl, G. (1991). Genetic relationships among landlocked, resident, and anadromous brown trout, Salmo trutta L. Heredity 66, 83–91.
Genetic relationships among landlocked, resident, and anadromous brown trout, Salmo trutta L.CrossRef | open url image1

Holland, C. H. (1987). The nautiloid cephalopods: a strange success. Journal of the Geological Society 144, 1–15.
The nautiloid cephalopods: a strange success.CrossRef | open url image1

House, M. R. (2010). Geographic distribution of Nautilus shells. In ‘Nautilus: the Biology and Paleobiology of a Living Fossil’. (Eds W. B. Saunders, and N. H. Landman.) pp. 53–64. (Springer: New York.)

Jereb, P., and Roper, C. F. E. (2005). ‘Cephalopods of the World: Chambered Nautiluses and Sepioids (Nautilidae, Sepiidae, Sepiolidae, Sepiadariidae, Idiosepiidae, and Spirulidae).’ (Food and Agriculture Organization of the United Nations: Rome.)

Kanie, Y., Fukuda, Y., Nakayama, H., Seki, K., and Hattori, M. (1980). Implosion of living Nautilus under increased pressure. Paleobiology 6, 44–47. open url image1

Kobayashi, T. (1954). A contribution towards Paleo-Flumenology, science of the oceanic currents of the past, with a description of a Miocene Aturia from central Japan. Japanese Journal of Geology and Geography 25, 35–56. open url image1

Kröger, B., Vinther, J., and Fuchs, D. (2011). Cephalopod origin and evolution: a congruent picture emerging from fossils, development and molecules. BioEssays 33, 602–613. open url image1

Kuhls, K., Keilonat, L., Ochsenreither, S., Schaar, M., Schweynoch, C., Presber, W., and Schonian, G. (2007). Multilocus microsatellite typing (MLMT) reveals genetically isolated populations between and within the main endemic regions of visceral leishmaniasis. Microbes and Infection 9, 334–343.
Multilocus microsatellite typing (MLMT) reveals genetically isolated populations between and within the main endemic regions of visceral leishmaniasis.CrossRef | 1:CAS:528:DC%2BD2sXivVShsrk%3D&md5=26c4b1d5b2b5fff0ede8c77000ed21a2CAS | open url image1

Madsen, T., Stille, B., and Shine, R. (1996). Inbreeding depression in an isolated population of adders Vipera berus. Biological Conservation 75, 113–118.
Inbreeding depression in an isolated population of adders Vipera berus.CrossRef | open url image1

Maloof, A. C., Porter, S. M., Moore, J. L., Dudas, F. O., Bowring, S. A., Higgins, J. A., Fike, D. A., and Eddy, M. P. (2010). The earliest Cambrian record of animals and ocean geochemical change. Bulletin of the Geological Society of America 122, 1731–1774.
The earliest Cambrian record of animals and ocean geochemical change.CrossRef | 1:CAS:528:DC%2BC3MXht1Ggt70%3D&md5=b1b4c351362f9b84a60212d83987ef76CAS | open url image1

Manda, Š. (2008). Palaeoecology and palaeogeographic relations of the Silurian phragmoceratids (Nautiloidea, Cephalopoda) of the Prague Basin (Bohemia). Bulletin of Geosciences 83, 39–62.
Palaeoecology and palaeogeographic relations of the Silurian phragmoceratids (Nautiloidea, Cephalopoda) of the Prague Basin (Bohemia).CrossRef | open url image1

Mapes, R. H., Landman, N. H., Cochran, K., Goiran, C., de Forges, B. R., and Renfro, A. (2010). Early taphonomy and significance of naturally submerged Nautilus shells from the New Caledonia region. Palaios 25, 597–610.
Early taphonomy and significance of naturally submerged Nautilus shells from the New Caledonia region.CrossRef | open url image1

Maravelias, C. D. (1999). Habitat selection and clustering of a pelagic fish: effects of topography and bathymetry on species dynamics. Canadian Journal of Fisheries and Aquatic Sciences 56, 437–450.
Habitat selection and clustering of a pelagic fish: effects of topography and bathymetry on species dynamics.CrossRef | open url image1

Mitchell, H. (1975). Sea-surface topography around Australia. Surveys in Geophysics 2, 117–129.
Sea-surface topography around Australia.CrossRef | open url image1

Moltschaniwskyj, N. A., Hall, K., Lipinski, M. R., Marian, J. E. A. R., Nishiguchi, M., Sakai, M., Shulman, D., Sinclair, B., Sinn, D., and Staudinger, M. (2007). Ethical and welfare considerations when using cephalopods as experimental animals. Reviews in Fish Biology and Fisheries 17, 455–476.
Ethical and welfare considerations when using cephalopods as experimental animals.CrossRef | open url image1

Neumann, G. (1960). On the effect of bottom topography on ocean currents. Ocean Dynamics 13, 132–141. open url image1

Nunes, F., Norris, R., and Knowlton, N. (2009). Implications of isolation and low genetic diversity in peripheral populations of an amphi-Atlantic coral. Molecular Ecology 18, 4283–4297.
Implications of isolation and low genetic diversity in peripheral populations of an amphi-Atlantic coral.CrossRef | 1:STN:280:DC%2BD1MjhsFKisA%3D%3D&md5=e509510bc9bdfff9990130d5cc180585CAS | open url image1

O’dor, R. K., and Webber, D. M. (1991). Invertebrate athletes: trade-offs between transport efficiency and power density in cephalopod evolution. The Journal of Experimental Biology 160, 93–112. open url image1

O’dor, R., Forsythe, J., Webber, D., Wells, J., and Wells, M. (1993). Activity levels of Nautilus in the wild. Nature 362, 626–628.
Activity levels of Nautilus in the wild.CrossRef | open url image1

Palumbi, S. R. (1994). Genetic divergence, reproductive isolation, and marine speciation. Annual Review of Ecology and Systematics 25, 547–572.
Genetic divergence, reproductive isolation, and marine speciation.CrossRef | open url image1

Rypien, K. L., Andras, J. P., and Harvell, C. (2008). Globally panmictic population structure in the opportunistic fungal pathogen Aspergillus sydowii. Molecular Ecology 17, 4068–4078.
Globally panmictic population structure in the opportunistic fungal pathogen Aspergillus sydowii.CrossRef | open url image1

Santos, S., Hrbek, T., Farias, I. P., Schneider, H., and Sampaio, I. (2006). Population genetic structuring of the king weakfish, Macrodon ancylodon (Sciaenidae), in Atlantic coastal waters of South America: deep genetic divergence without morphological change. Molecular Ecology 15, 4361–4373.
Population genetic structuring of the king weakfish, Macrodon ancylodon (Sciaenidae), in Atlantic coastal waters of South America: deep genetic divergence without morphological change.CrossRef | 1:CAS:528:DC%2BD2sXmvVSlsw%3D%3D&md5=6dbff0ef0800e48d2fd42053e099825fCAS | open url image1

Santos, X., Brito, J. C., Caro, J., Abril, A. J., Lorenzo, M., Sillero, N., and Pleguezuelos, J. M. (2009). Habitat suitability, threats and conservation of isolated populations of the smooth snake (Coronella austriaca) in the southern Iberian Peninsula. Biological Conservation 142, 344–352.
Habitat suitability, threats and conservation of isolated populations of the smooth snake (Coronella austriaca) in the southern Iberian Peninsula.CrossRef | open url image1

Saunders, W. B., and Landman, N. H. (2010). ‘Nautilus: the Biology and Paleobiology of a Living Fossil.’ (Springer Verlag: New York.)

Saunders, W. B., and Spinosa, C. (1979). Nautilus movement and distribution in Palau, western Caroline Islands. Science 204, 1199–1201.
Nautilus movement and distribution in Palau, western Caroline Islands.CrossRef | 1:STN:280:DC%2BC3cvivVSmtw%3D%3D&md5=6867fbce9babc8826aa6696a4fcf650aCAS | open url image1

Saunders, W. B., and Wehman, D. A. (1977). Shell strength of Nautilus as a depth limiting factor. Paleobiology 3, 83–89. open url image1

Schlögl, J., Chirat, R., Balter, V., Joachimski, M. M., Hudackova, N., and Quillévéré, F. (2011). Aturia from the Miocene Paratethys: An exceptional window on nautilid habitat and lifestyle. Palaeogeography, Palaeoclimatology, Palaeoecology 308, 330–338.
Aturia from the Miocene Paratethys: An exceptional window on nautilid habitat and lifestyle.CrossRef | open url image1

Schneider, S., Roessli, D., and Excoffier, L. (2005). Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evolutionary Bioinformatics Online 1, 47–50. open url image1

Shigeno, S., Takenori, S., and Boletzky, S. V. (2010). The origins of cephalopod body plans: a geometrical and developmental basis for the evolution of vertebrate-like organ systems. In ‘Cephalopods – Present and Past’. (Eds K. Tanabe, Y. Shigeta, T. Sasaki and H. Hirano.) pp. 23–34. (Tokai University Press: Tokyo.)

Silva, I. C., Mesquita, N., and Paula, J. (2010). Lack of population structure in the fiddler crab Uca annulipes along an East African latitudinal gradient: genetic and morphometric evidence. Marine Biology 157, 1113–1126.
Lack of population structure in the fiddler crab Uca annulipes along an East African latitudinal gradient: genetic and morphometric evidence.CrossRef | open url image1

Sinclair, B., Briskey, L., Aspden, W., and Pegg, G. (2007). Genetic diversity of isolated populations of Nautilus pompilius (Mollusca, Cephalopoda) in the Great Barrier Reef and Coral Sea. Reviews in Fish Biology and Fisheries 17, 223–235.
Genetic diversity of isolated populations of Nautilus pompilius (Mollusca, Cephalopoda) in the Great Barrier Reef and Coral Sea.CrossRef | open url image1

Sinclair, W., Newman, S., Vianna, G., Williams, S., and Aspden, W. (2011). Spatial subdivision and genetic diversity in populations on the east and west coasts of Australia: the multi-faceted case of Nautilus pompilius (Mollusca, Cephalopoda). Reviews in Fisheries Science 19, 52–61.
Spatial subdivision and genetic diversity in populations on the east and west coasts of Australia: the multi-faceted case of Nautilus pompilius (Mollusca, Cephalopoda).CrossRef | open url image1

Smith, M. R., and Caron, J. B. (2010). Primitive soft-bodied cephalopods from the Cambrian. Nature 465, 469–472.
Primitive soft-bodied cephalopods from the Cambrian.CrossRef | 1:CAS:528:DC%2BC3cXmsF2hsrs%3D&md5=eb9f3f1f7e3119b3b7115279c44d4c12CAS | open url image1

Strugnell, J., Jackson, J., Drummond, A. J., and Cooper, A. (2006a). Divergence time estimates for major cephalopod groups: evidence from multiple genes. Cladistics 22, 89–96.
Divergence time estimates for major cephalopod groups: evidence from multiple genes.CrossRef | open url image1

Strugnell, J., Norman, M., and Cooper, A. (2006b). DNA from beach-washed shells of the ram’s horn squid, Spirula spirula. Bulletin of Marine Science 78, 389–391. open url image1

Suzuki, T., Fukuta, H., Nagato, H., and Umekawa, M. (2000). Arginine kinase from Nautilus pompilius, a living fossil. The Journal of Biological Chemistry 275, 23884.
Arginine kinase from Nautilus pompilius, a living fossil.CrossRef | 1:CAS:528:DC%2BD3cXls12lsrs%3D&md5=a227df03473c9b13cdc64fbd9ec2c6faCAS | open url image1

Tanabe, K., and Hamada, T. (1978). Keeping record of a drifted living Nautilus pompilius specimen caught off Kagoshima Bay and its significance. Kaiyo Kagaku 10, 1011–1017. open url image1

Thornhill, D. J., Mahon, A. R., Norenburg, J. L., and Halanych, K. M. (2008). Open-ocean barriers to dispersal: a test case with the Antarctic Polar Front and the ribbon worm Parborlasia corrugatus (Nemertea: Lineidae). Molecular Ecology 17, 5104–5117.
Open-ocean barriers to dispersal: a test case with the Antarctic Polar Front and the ribbon worm Parborlasia corrugatus (Nemertea: Lineidae).CrossRef | 1:CAS:528:DC%2BD1MXps1Cjsg%3D%3D&md5=45bd1a5eb80dd09c018dcb42ca8c46cbCAS | open url image1

Tittensor, D. P., Worm, B., and Myers, R. A. (2006). ‘Macroecological Changes in Exploited Marine Systems.’ (University of Chicago Press: Chicago, IL.)

Trinkel, M., Funston, P., Hofmeyr, M., Hofmeyr, D., Dell, S., Packer, C., and Slotow, R. (2010). Inbreeding and density-dependent population growth in a small, isolated lion population. Animal Conservation 13, 374–382.
Inbreeding and density-dependent population growth in a small, isolated lion population.CrossRef | open url image1

Wani, R. (2004). Experimental fragmentation patterns of modern Nautilus shells and the implications for fossil cephalopod taphonomy. Lethaia 37, 113–123.
Experimental fragmentation patterns of modern Nautilus shells and the implications for fossil cephalopod taphonomy.CrossRef | open url image1

Wani, R., and Ikeda, H. (2006). Planispiral cephalopod shells as a sensitive indicator of modern and ancient bottom currents: new data from flow experiments with modern Nautilus pompilius. Palaios 21, 289.
Planispiral cephalopod shells as a sensitive indicator of modern and ancient bottom currents: new data from flow experiments with modern Nautilus pompilius.CrossRef | open url image1

Wiemers, M., and Fiedler, K. (2007). Does the DNA barcoding gap exist? A case study in blue butterflies (Lepidoptera: Lycaenidae). Frontiers in Zoology 4, .
Does the DNA barcoding gap exist? A case study in blue butterflies (Lepidoptera: Lycaenidae).CrossRef | 1:CAS:528:DC%2BD2sXjsFehu7k%3D&md5=f1a11ae4a2fcb1079ed79386961b4e7fCAS | open url image1

Wieters, E. A., Gaines, S. D., Navarrete, S. A., Blanchette, C. A., and Menge, B. A. (2008). Scales of dispersal and the biogeography of marine predator–prey interactions. American Naturalist 171, 405–417.
Scales of dispersal and the biogeography of marine predator–prey interactions.CrossRef | open url image1

Wray, C. G., Landman, N. H., Saunders, W. B., and Bonacum, J. (1995). Genetic divergence and geographic diversification in Nautilus. Paleobiology 21, 220–228. open url image1


Full Text PDF (744.8 KB) Export Citation