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

Reconstructing a radiation: the chiton genus Mopalia in the north Pacific

Ryan P. Kelly A B C E and Douglas J. Eernisse D
+ Author Affiliations
- Author Affiliations

A Columbia University, New York, USA.

B American Museum of Natural History, New York, USA.

C Present address: Stanford University, Hopkins Marine Station, Pacific Grove, California, USA.

D California State University, Fullerton, California, USA.

E Corresponding author. Email: rpk@stanford.edu

Invertebrate Systematics 22(1) 17-28 https://doi.org/10.1071/IS06021
Submitted: 13 June 2006  Accepted: 13 December 2007   Published: 18 March 2008

Abstract

The chiton genus Mopalia Gray, 1847 is highly speciose despite showing little morphological differentiation. Many of the 24 extant species are conspicuous, large-bodied and ecologically important today, but pre-Pleistocene fossils for the genus are rare. Here, we use a combined analysis of four gene regions (16S and COI mtDNA, 18S and 28S rDNA) to estimate the phylogenetic relationships for Mopalia species and use the inferred phylogeny to analyse the group’s biogeography and patterns of speciation. We then use these molecular data to distinguish between two alternative interpretations of the fossil record, as there is a large temporal gap between the oldest fossils tentatively identified as Mopalia and the next oldest fossils (Miocene versus Plio-Pleistocene). Based on the estimated substitution rates from a wide variety of other marine animals, we conclude that the observed rates in Mopalia are consistent with a Miocene origin for the genus. Given this age for the group and assuming a molecular clock, most speciation events in Mopalia are inferred to have occurred on average ~5 Mya. The phylogenetic results indicate that most of the speciation events leading to extant species must have occurred along the western North American coast, though there appear to have been multiple spreading events across the Pacific. When considered along with results for the many other near-shore taxa that have similar distributions to Mopalia, our findings suggest the emergence of a coherent historical biogeography of the northern Pacific.

Additional keywords: Mollusca, neogene, phylogeny, polyplacophora, speciation.


Acknowledgements

RPK acknowledges R. Desalle for financial and intellectual support and for bench space at AMNH, and financial support provided by the Columbia University Department of Ecology, Evolution, and Environmental Biology, The National Science Foundation GK-12 Fellowship (No. DGE0231875 to Columbia University), The University of Washington’s Friday Harbor Marine Laboratories, The Lerner-Gray Grants for Marine Research, and the American Museum of Natural History. An earlier version of this study was first presented as part of RPK’s dissertation research, and the author gratefully acknowledges the support of his dissertation committee: Rob Desalle, Andrew Baker, Chris Raxworthy, Shahid Naeem, and DJE. DJE acknowledges support from the California State University, Fullerton and the Sea of Cortez Expedition and Education Project, Stanford University and the Instituto Nacional de Ecología in Mexico, for allowing participation as part of this expedition that made these Mexican comparisons possible, and likewise L. Lovell, Scripps Institution of Oceanography, for the loan of specimens dredged off the Pacific coast of Mexico. Much of the analysis and writing were completed while DJE was completing a sabbatical jointly supported by CSUF and a fellowship from the National Evolutionary Synthesis Center (NESCent), NSF #EF-0423641. We thank especially A. Draeger for helping to identify problematic specimens and for collecting all of our subtidal samples in the Monterey area. Others who have contributed to our collecting efforts for this study include B. Allen, A. Baldwin, R. Clark, C. Colt, G. Eckert, G. & S. Jeffrey, H. Keller, J. Manke, C. McGary, J. Pearse, M. Poulson, L. Rogers-Bennett, and T. Stebbins. Our studies benefited from the cooperation of the Reserve Managers at the Landels-Hill Big Creek, Kenneth S. Norris Rancho Marino, and Bodega Marine Reserves of the University of California Natural Reserve System. We thank H. Chaney, F. Hochberg, and P. Valentich-Scott who have greatly assisted us in curation of our specimen vouchers at the Santa Barbara Museum of Natural History, and J. Feinstein, Ambrose Monell Cryo Collection of the American Museum of Natural History, for help curating frozen tissue vouchers. DJE is grateful to several scientists consulted during revisions of this manuscript, including D. Zwickl for advice on phylogenetic analysis, C. Cunningham for help with molecular rates calculations, and G. Vermeij, L. Marinkovich, C. Powell, II, K. Amano, H. Saito, A. Oleinik, J. Barron, M. Lyle, L. Groves, and G. Kennedy for considerable help with interpreting the fossil record of Mopalia. We are grateful to J. Sullivan, M. Manier, E. Jacobs-Palmer, S. Palumbi, M. Whitlock, S. Otto, B. Sidlauskas, members of the NESCent Journal Club, and several anonymous reviewers, whose comments improved the manuscript significantly.


References


Amano K., Vermeij G. J. (1998) Origin and biogeographic history of Ceratostoma (Gastropoda: Muricidae). Venus (Tokyo) 57, 209–223.

Amano K., Vermeij G. J. (2003) Evolutionary adaptation and geographic spread of the Cenozoic buccinid genus Lirabuccinum in the North Pacific. Journal of Paleontology 77, 863–872.
CrossRef |

Barron J. A. (2003) Planktonic marine diatom record of the past 18 My: appearances and extinctions in the Pacific and Southern Oceans. Diatom Research 18, 203–224.

Bremer K. (1994) Branch support and tree stability. Cladistics 10, 295–304.
CrossRef |

Briggs J. C. (2006) Proximate sources of marine biodiversity. Journal of Biogeography 33, 1–10.
CrossRef |

Collin R. (2003) Worldwide patterns in mode of development in calyptraeid gastropods. Marine Ecology Progress Series 247, 103–122.
CrossRef |

Collins T. M., Frazier K., Palmer A. R., Vermeij G. J., Brown W. M. (1996) Evolutionary history of Northern Hemisphere Nucella (Gastropoda, Muricidae): molecular, morphological, and paleontological evidence. Evolution 50, 2287–2304.
CrossRef |

Dawson M. N. (2001) Phylogeography in coastal marine animals: a solution from California? Journal of Biogeography 28, 723–736.
CrossRef |

Dawson M. N., Jacobs D. K. (2001) Molecular evidence for cryptic species of Aurelia aurita (Cnidaria, Scyphozoa). The Biological Bulletin 200, 92–96.
CrossRef | PubMed |

Dawson M. N., Louie K. D., Barlow M., Jacobs D. K., Swift C. C. (2002) Comparative phylogeography of sympatric sister species, Clevelandia ios and Eucyclogobius newberryi (Teleostei, Gobiidae), across the California Transition Zone. Molecular Ecology 11, 1065–1075.
CrossRef | PubMed |

Durham J. W., and MacNeil F. S. (1967). Cenozoic migrations of marine invertebrates through the Bering Strait region. In ‘The Bering Land Bridge’. (Ed. D. M. Hopkins.) pp. 326–349. (Stanford University Press: Stanford, CA, USA.)

Eernisse D. J., Clark R. N., and Draeger A. (2007). Chitons (Mollusca: Polyplacophora). In ‘Light’s Manual of Intertidal Invertebrates of the Central California Coast’. (Eds S. F. Light, R. I. Smith and J. T. Carlton.) pp. 701–713. (University of California Press: Berkeley, CA, USA.)

Estes J. A., Steinberg P. D. (1988) Predation, herbivory, and kelp evolution. Paleobiology 14, 19–36.

Estes J. A., Lindberg D. A., Wray C. (2005) Evolution of large body size in abalones (Haliotis): patterns and implications. Paleobiology 14, 19–36.

Folmer O., Black M., Hoeh W., Lutz R., Vrijenhoek R. (1994) DNA Primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3, 294–299.
PubMed |


Gladenkov A. Y., Oleinik A. E., Marincovich L., Barinov K. B. (2002) A refined age for the earliest opening of Bering Strait. Palaeogeography, Palaeoclimatology, Palaeoecology 183, 321–328.
CrossRef |

Hellberg M. E. (1998) Sympatric sea shells along the sea’s shore: the geography of speciation in the marine gastropod Tegula. Evolution 52, 1311–1324.
CrossRef |

Hellberg M. E. (2006) No variation and low synonymous substitution rates in coral mtDNA despite high nuclear variation. BMC Evolutionary Biology 6, 24.
CrossRef | PubMed |

Hellberg M. E., Vacquier V. D. (1999) Rapid evolution of fertilization selectivity and lysin cDNA sequences in teguline gastropods. Molecular Biology and Evolution 16, 839–848.
PubMed |


Hendry A. P., Wenburg J. K., Bentzen P., Volk E. C., Quinn T. P. (2000) Rapid evolution of reproductive isolation in the wild: evidence from introduced salmon. Science 290, 516–518.
CrossRef | PubMed |

Herbert T. D., Schuffert J. D., Andreasen D., Heusser L., Lyle M., Mix A., Ravelo A. C., Stott L. D., Herguera J. C. (2001) Collapse of the California Current during glacial maxima linked to climate change on land. Science 293, 71–76.
CrossRef | PubMed |

Hickman C. S. (2003). Evidence for abrupt Eocene–Oligocene molluscan faunal change in the Pacific Northwest. In ‘From Greenhouse to Icehouse: The Marine Eocene–Oligocene Transition’. (Eds D. R. Prothero, L. C. Ivany and E. A. Nesbitt.) pp. 71–87. (Columbia University Press: New York, USA.)

Hillis D. M., Dixon M. T. (1991) Ribosomal DNA: molecular evolution and phylogenetic inference. The Quarterly Review of Biology 66, 411–543.
CrossRef | PubMed |

Huelsenbeck J. P., Ronquist F. (2001) MRBAYES: Bayesian inference of phylogeny. Bioinformatics 17, 754–755.
CrossRef | PubMed |

Huelsenbeck J. P., Larget B., Miller R. E., Ronquist F. (2002) Potential applications and pitfalls of Bayesian inference of phylogeny. Systematic Biology 51, 673–688.
CrossRef | PubMed |

Itoigawa J. (1993) Miocene palaeogeography of the Mizunami Group of the Tono region, central Japan. Palaeogeography, Palaeoclimatology, Palaeoecology 100, 209–215.
CrossRef |

Itoigawa J., Nishimoto H. (1975) Miocene Polyplacophora assemblage from the Mizunami group, central Japan (first report). Bulletin of the Mizunami Fossil Museum 2, 35–50.

Itoigawa J., Shibata H., Nishimoto H., Okumura Y. (1981) Miocene fossils of the Mizunami group, central Japan 2. Molluscs, part 1. Bulletin of the Mizunami Fossil Museum 3A, 1–53.

Itoigawa J., Shibata H., Nishimoto H., Okumura Y. (1982) Miocene fossils of the Mizunami group, central Japan 2. Molluscs, part 2. Bulletin of the Mizunami Fossil Museum 3B, 303–310.

Jablonski D., Roy K., and Valentine J. W. (2003). Evolutionary macroecology and the fossil record. In ‘Macroecology: Concepts and Consequences’. (Eds T. M. Blackburn and K. J. Gaston.) pp. 368–390. (Blackwell Science: Oxford, UK.)

Jacobs D. K., Haney T. A., Louie K. D. (2004) Genes, diversity, and geologic process on the Pacific Coast. Annual Review of Earth and Planetary Sciences 32, 601–652.
CrossRef |

Jones A. G., Moore G. I., Kvarnemo C., Walker D., Avise J. C. (2003) Sympatric speciation as a consequence of male pregnancy in seahorses. Proceedings of the National Academy of Sciences of the United States of America 100, 6598–6603.
CrossRef | PubMed |

Kelly R. P., Sarkar I. N., Eernisse D. J., Desalle R. (2007) DNA barcoding using chitons (genus Mopalia). Molecular Ecology Notes 7, 177–183.
CrossRef |

Knowlton N. (2000) Molecular genetic analyses of species boundaries in the sea. Hydrobiologia 420, 73–90.
CrossRef |

Lessios H. A., Kessing B. D., Pearse J. S. (2001) Population structure and speciation in tropical seas: global phylogeography of the sea urchin Diadema. Evolution 55, 955–975.
CrossRef | PubMed |

Levin L. A. (2006) Recent progress in understanding larval dispersal: new directions and digressions. Integrative and Comparative Biology 46, 282–297.
CrossRef |

Losos J. B., Glor R. E. (2003) Phylogenetic comparative methods and the geography of speciation. Trends in Ecology & Evolution 18, 220–227.
CrossRef |

Lyle M., Barron J. A., Bralower T. J., Huber M., Olivarez Lyle A., Ravelo A. C., Rea D. K., Wilson P. A. (in press) The Pacific Ocean and the Cenozoic evolution of climate. Reviews of Geophysics ,

Maddison D. R., and Maddison W. P. (2003). ‘MacClade: Analysis of Phylogeny and Character Evolution, Version 4.06.’ (Sinauer: Sunderland, MA, USA.)

Marincovich L., Gladenkov A. Y. (1999) Evidence for an early opening of the Bering Strait. Nature 397, 149–151.
CrossRef |

Marko P. B. (1998) Historical allopatry and the biogeography of speciation in the prosobranch snail genus Nucella. Evolution 52, 757–774.
CrossRef |

McCartney M. A., Keller G., Lessios H. A. (2000) Dispersal barriers in tropical oceans and speciation in Atlantic and eastern Pacific sea urchins of the genus Echinometra. Molecular Ecology 9, 1391–1400.
CrossRef | PubMed |

Meyer C. P. (2003) Molecular systematics of cowries (Gastropoda: Cypraeidae) and diversification patterns in the tropics. Biological Journal of the Linnean Society 79, 401–459.
CrossRef |

Ogasawar K. (2003) Mollusca: Polyplacophora and allied taxa. Palaeontological Society of Japan Special Papers 41, 277–278.

Oleinik A. E., and Marincovich L.Jr (2003). Biotic response to the Eocene–Oligocene Transition: gastropod assemblages in the high-latitude North Pacific. In ‘From Greenhouse to Icehouse: The Marine Eocene–Oligocene Transition’. (Eds D. R. Prothero, L. C. Ivany and E. A. Nesbitt.) pp. 36–56. (Columbia University Press: New York, USA.)

Palumbi S. R. (1996). Nucleic acids II: the polymerase chain reaction. In ‘Molecular Systematics’. (Eds D. M. Hillis, C. Moritz and B. K. Mable.) pp. 205–247. (Sinauer Associates: Sunderland, MA, USA.)

Posada D., Crandall K. A. (1998) ModelTest: testing the model of DNA substitution. Bioinformatics 14, 817–818.
CrossRef | PubMed |

Reid D. G. (1996). ‘Systematics and Evolution of Littorina.’ (Dorset Press: Dorchester, UK.)

Ronquist F., Huelsenbeck J. P. (2003) MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572–1574.
CrossRef | PubMed |

Roy K., Jablonski D., Valentine J. W. (1995) Thermally anomalous assemblages revisited: patterns in the extraprovincial latitudinal range shifts of Pleistocene marine mollusks. Geology 23, 1071–1074.
CrossRef |

Saito H., Okutani T. (1991) Taxonomy of Japanese species of the genera Mopalia and Plaxiphora (Polyplacophora: Mopaliidae). The Veliger 34, 172–194.

Sanderson M. J. (2002) Estimating absolute rates of molecular evolution and divergence times: a penalized likelihood approach. Molecular Biology and Evolution 19, 101–109.
PubMed |


Schroth W., Jarms G., Streit B., Schierwater B. (2002) Speciation and phylogeography in the cosmopolitan marine moon jelly, Aurelia sp. BMC Evolutionary Biology 2,
CrossRef | PubMed |

Squires R. L. (2003). Turnovers in marine gastropod faunas during the Eocene–Oligocene Transition. In ‘From Greenhouse to Icehouse: the Eocene–Miocene Transition’. (Eds D. R. Prothero, L. C. Ivany and E. A. Nesbitt.) pp. 14–35. (Columbia University Press: New York, USA.)

Sullivan J., Joyce P. (2005) Model selection in phylogenetics. Annual Review of Ecology and Systematics 36, 445–466.
CrossRef |

Swofford D. L. (2003). ‘PAUP*. Phylogenetic Analysis Using Parsimony (*and Other Methods), Version 4.0.’ (Sinauer Associates: Sunderland, MA, USA.)

Tamura K., Dudley J., Nei M., Kumar S. (2007) MEGA4: Molecular Evolutionary Genetics Analysis, software version 4.0. Molecular Biology and Evolution 24, 1596–1599.
CrossRef | PubMed |

Valentine J. W. (1980) Camalu: A Pleistocene terrace fauna from Baja California. Journal of Paleontology 54, 1310–1318.

Vermeij G. J. (2001). Community assembly in the sea: geologic history of the living shore biota. In ‘Marine Community Ecology’. (Eds M. D. Bertness, S. D. Gaines and M. E. Hay.) pp. 39–60. (Sinauer Associates: Sunderland, MA, USA.)

Vermeij G. J. (2005). Invasion as expectation: a historical fact of life. In ‘Species Invasions: Insights into Ecology, Evolution, and Biogeography’. (Eds D. F. Sax, J. J. Stachowicz and S. D. Gaines.) pp. 309–339. (Sinauer Associates, Inc.: Sunderland, MA, USA.)

Wares J. P., Cunningham C. W. (2001) Phylogeography and historical ecology of the North Atlantic intertidal. Evolution 55, 2455–2469.
PubMed |


Zwickl D. J. (2006). Genetic algorithm approaches for the phylogenetic analysis of large biological sequence datasets under the maximum likelihood criterion. PhD Thesis, University of Texas, Austin, TX, USA.








Rent Article (via Deepdyve) Supplementary MaterialSupplementary Material (74 KB) Export Citation Cited By (12)