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Patterns of morphological diversity among and within arcid bivalve species pairs separated by the Isthmus of Panama

  • Peter B. Marko (a1) and Jeremy B. C. Jackson (a1) (a2)

Abstract

Geminate species are morphologically similar sister-species found on either side of the Isthmus of Panama. The existence of all geminates in the tropical Eastern Pacific ocean and the Caribbean Sea is most often explained by vicariance: closure of the Central American Seaway 3.1 to 3.5 Ma simultaneously isolated populations of species with amphi-American distributions. In this paper, we test the potential of morphological measurements for discriminating between Recent geminate species pairs from three genera (Arca, Arcopsis, and Barbatia) in the bivalve family Arcidae and examine the prospects for distinguishing nominal species in the fossil record. Fourteen morphological variables were used to characterize shell shape and multivariate methods were used to discriminate between five Recent species pairs. Collection sites were also used as a priori groups for discrimination to describe patterns of intraspecific morphological variation and to evaluate differences among samples from different geographic regions.

On average, 84 percent of specimens within geminate pairs are classified correctly following five separate discriminant analyses with nominal species as the grouping variable. Although all but one arcid species pair are discriminated with high statistical significance, some collection sites within species are highly morphologically distinct. Overall, a large proportion of specimens from each collection locality (79 percent on average) can be classified correctly to site although no single site possessed a multivariate centroid that was significantly different from all other conspecific centroids. The distinctiveness of some collection sites, however, raises the possibility that some nominal species may harbor cryptic species, indicating the need for wider geographic surveys of both molecular and morphological variation within geminate species pairs.

The eigenvalue coefficients derived from the Recent samples of one geminate pair (Arca mutabilis and A. imbricata) were used to assess the potential for identifying arcid species in the fossil record. Discriminant analyses of fossil Arca indicate that the forms that characterize Recent A. mutabilis and A. imbricata are present in the fossil record as far back as the Late Early Miocene, in the Cantaure Formation of Venezuela. Because a deep water connection between the Eastern Pacific and Western Atlantic existed until the Middle Miocene, the morphological differences associated with Recent A. mutabilis and A. imbricata likely existed well before the rising Isthmus affected ocean circulation patterns in tropical America. Therefore, despite great overall morphological similarity, these putative geminate species likely have a time of divergence that is at least four times older than final seaway closure. The geographic distribution of fossils also suggests that morphological forms associated with each Recent species had amphi-American distributions both before and after isthmus formation but are now geographically restricted to either side of the isthmus in the Recent fauna.

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Abbott, R. T. 1974. American Seashells (second edition). Van Nostrand Reinhold Co., New York, 662 p.
Allmon, W. D. 1992. Role of nutrients and temperature in extinction of turritelline gastropods in the northwestern Atlantic and northeastern Pacific. Palaeogeography, Palaeoclimatology, Palaeoecology, 92:4154.
Allmon, W. D., Rosenberg, G., Portell, R. W., and Schindler, K. S. 1993. Diversity of Atlantic coastal plain mollusks since the Pliocene. Science, 260:16261629.
Bartsch, P. 1931. The West American mollusks of the genus Acar. Proceedings of the United States National Museum, volume 80, Art. 9, No. 2909.
Bermingham, E., and Lessios, H. A. 1993. Rate variation of proteins and mitochondrial DNA evolution as revealed by sea urchins separated by the Isthmus of Panama. Proceedings of the National Academy of Sciences U.S.A., 90:27342738.
Bermingham, E., McCafferty, S. S., and Martin, A. P. 1997. Fish biogeography and molecular clocks: perspectives from the Panamanian Isthmus, p. 113128. In Kocher, T. D. and Stepien, C. A. (eds.), Molecular Systematics of Fishes. Academic Press, New York.
Bookstein, F. L. 1990. Introduction to methods for landmark data, p. 215226. In Rohlf, F. J. and Bookstein, F. L. (eds.), Proceedings of the Michigan Morphometrics Workshop. Special Publication No. 2 of The University of Michigan Museum of Zoology, Ann Arbor.
Bookstein, F. L. 1991. Morphometric Tools for Landmark Data. Geometry and Biology. Cambridge Univ. Press, Cambridge.
Budd, A. F., Johnson, K. G., and Potts, D. C. 1994. Recognizing morphospecies in colonial reef corals: I. Landmark-based methods. Paleobiology, 20:484505.
Budd, A. F., Johnson, K. G., and Stemann, T. A. 1996. Plio-Pleistocene turnover and extinctions in the Caribbean reef coral fauna, p. 168204. In Jackson, J. B. C., Budd, A. F., and Coates, A. G. (eds.), Evolution and Environment in Tropical America. University of Chicago Press, Chicago.
Brusca, R. C. 1980. Common intertidal invertebrates of the Gulf of California (second edition). University of Arizona Press, Tucson, 513 p.
Coates, A. G., and Obando, J. A. 1996. The geologic evolution of the Central American isthmus, p. 2156. In Jackson, J. B. C., Budd, A. F., and Coates, A. G. (eds.), Evolution and Environment in Tropical America. University of Chicago Press, Chicago.
Coates, A. G., Jackson, J. B. C., Collins, L. S., Cronin, T. M., Dowsett, H. J., Bybell, L. M., Jung, P., and Obando, J. A. 1992. Closure of the Isthmus of Panama: the near-shore marine record of Costa Rica and Panama. Geological Society of America Bulletin, 104:814828.
Collins, T. M. 1996. Molecular comparisons of transisthmian species pairs: rates and patterns of evolution, p. 303334. In Jackson, J. B. C., Budd, A. F., and Coates, A. G. (eds.), Evolution and Environment in Tropical America. University of Chicago Press, Chicago.
Collins, L. S., and Coates, A. G. (eds.). 1999. The Neogene of the Isthmus of Panama: a paleobiotic survey of the Caribbean coast. Bulletins of American Paleontology, 357.
Collins, L. S., Budd, A. F., and Coates, A. G. 1996. Earliest evolution associated with closure of the Tropical American Seaway. Proceedings of the National Academy of Sciences U.S.A., 93:60696072.
Cunningham, C. W., and Collins, T. M. 1994. Developing model systems for molecular biogeography: vicariance and interchange in marine invertebrates, p. 406433. In Schierwater, B., Streit, B., Wagner, G. P., and DeSalle, R. (eds.), Molecular Ecology and Evolution: Approaches and Applications. Birkhauser Verlag, Basel.
Cronin, T. M. 1985. Speciation and stasis in marine ostracoda: climatic modulation of evolution. Science, 227:6063.
Cronin, T. M., and Dowsett, H. J. 1996. Biotic and oceanographic response to the Pliocene closing of the Central American Isthmus, p. 76104. In Jackson, J. B. C., Budd, A. F., and Coates, A. G. (eds.), Evolution and Environment in Tropical America. The University of Chicago Press, Chicago.
Díaz De Gamero, M. L. 1974. Microfauna y edad de la Formación Cantaure, Península de Paraguaná, Venezuela. Asoc. Venez. Geol. Min. Petr., Bol. Informativo, 13:4147.
Duffy, J. E. 1996. Resource-associated population subdivision in a symbiotic coral-reef shrimp. Evolution, 50:360373.
Duque-Caro, H. 1990. Neogene stratigraphy, palaeoceanography, and paleobiology in northwest South America and the evolution of the Panama seaway. Palaeogeography, Palaeoclimatology, Palaeoecology, 777:203234.
Gibson-Smith, J., and Gibson-Smith, W. 1979. The genus Strombina (Mollusca: Gastropoda) in Venezuela, with descriptions of a new Recent and some fossil species. Asoc. Venez. Geol. Min. Petr., Bol. Informativo, 17:4970.
Gunther, A. 1868. An account of the fishes of the states of Central America, based on the collections made by Capt. J. M. Dow, F. Godman, Esq., and O. Salvin, Esq. Transactions of the Zoological Society of London, 6:377402.
Harland, W. B., Armstrong, R. L., Cox, A. V., Craig, L. E., Smith, A. G., and Smith, D. G. 1990. A Geologic Time Scale, 1989. Cambridge University Press, Cambridge.
Hellberg, M. E. 1998. Sympatric sea shells along the sea's shore: the geography of speciation in the marine gastropod Tegula. Evolution, 52:13111324.
Hora, S. C., and Wilcox, J. B. 1982. Estimation of error rates in several population discriminant analyses. Journal of Marketing Research, 19:5761.
Humphries, C. J., and Parenti, L. R. 1986. Cladistic biogeography. Clarendon Press, Oxford.
Hunter, V. F., and Bartok, P. 1974. The age and correlation of the Tertiary sediments of the Paraguaná Península, Venezuela. Asoc. Venez. Geol. Min. Petr., Bol. Informativo, 17:143154.
Hutcheson, H. J., Oliver, J. H. Jr., Houck, M. A., and Strauss, R. E. 1995. Multivariate morphometric discrimination of nymphal and adult forms of the blacklegged tick (Acari: Ixodidae): a principal vector of the agent of lyme disease in eastern North America. Journal of Medical Entomology, 32:827842.
Jablonski, D. 2000. Micro- and macroevolution: scale and hierarchy in evolutionary biology and paleobiology, p. 1552. In Erwin, D. H. and Wing, S. L. (eds.), Deep Time: Paleobiology's Perspective. Supplement to Vol. 26 of Paleobiology, The Paleontological Society, Lawrence.
Jackson, J. B. C., and Cheetham, A. H. 1990. Evolutionary significance of morphospecies: a test with cheilostome Bryozoa. Science, 248:521636.
Jackson, J. B. C., and Cheetham, A. H. 1994. Phylogeny reconstruction and the tempo of speciation in cheilostome Bryozoa. Paleobiology, 20:407423.
Jackson, J. B. C., and Cheetham, A. H. 1999. Tempo and mode of speciation in the sea. Trends in Ecology and Evolution, 14:7277.
Jackson, J. B. C., and Johnson, K. G. 2000. Life in the last few million years, p. 221235. In Erwin, D. H. and Wing, S. L. (eds.), Deep Time: Paleobiology's Perspective. Supplement to Vol. 26 of Paleobiology, The Paleontological Society, Lawrence.
Jackson, J. B. C., Jung, P., and Fortunato, H. 1996. Paciphilia revisited: Transisthmian evolution of the Strombina group (Gastropoda: Columbellidae), p. 234270. In Jackson, J. B. C., Budd, A. F., and Coates, A. G. (eds.), Evolution and Environment in Tropical America. University of Chicago Press, Chicago.
Jackson, J. B. C., Jung, P., Coates, A. G., and Collins, L. S. 1993. Diversity and extinction of tropical American mollusks and emergence of the Isthmus of Panama. Science, 260:16241626.
Jackson, J. B. C., Todd, J., Fortunato, H., and Jung, P. 1999. Diversity and assemblages of Neogene Caribbean Mollusca in lower Central America, p. 193230. In Collins, L. S. and Coates, A. G. (eds.), A Paleobiotic Survey of Caribbean Faunas from the Neogene of the Isthmus of Panama, Pt. I, Bulletin of American Paleontology, 357.
Jones, M. L. 1972. Introduction to a symposium on the biological effects of a sea level canal across Panama. Bulletin of the Biological Society of Washington, viviii.
Jordan, D. S. 1908. The law of geminate species. American Naturalist, 42:7380.
Jung, P. 1989. Revision of the Strombina-group (Gastropoda: Columbellidae), fossil and living. Schweizerische Palaontologische Abhandlung, 111:1298.
Keen, A. M. 1974. Sea Shells of Tropical West America. Stanford University Press.
Keigwin, L. D. 1982. Isotopic paleooceanography of the Caribbean and east Pacific: Role of Panama uplift in late Neogene time. Science, 217:350352.
Kessing, B. D. 1991. Strongylocetroid sea urchin mitochondrial DNA: Phylogenetic relationships and patterns of molecular evolution. , .
Knowlton, N. 1993. Sibling species in the sea. Annual Review of Ecology and Systematics, 24:189216.
Knowlton, N., and Weigt, L. A. 1998. New dates and new rates for divergence across the Isthmus of Panama. Proceedings of The Royal Society of London Series B-Biological Sciences, 265:22572263.
Knowlton, N., Weigt, L. A., Solorzano, L. A., Mills, D. K., and Bermingham, E. 1993. Divergence in proteins, mitochondrial DNA, and reproductive compatibility across the Isthmus of Panama. Science, 260:16291632.
Kowalewski, M., Dyreson, E., Marcot, J. D., Vargas, J. A., Flessa, K. W., and Hallman, D. P. 1997. Phenetic discrimination of biometric simpletons: Paleobiological implications of morphospecies in the lingulide brachiopod Glottidia. Paleobiology, 23:444469.
Kwast, K. E., Foltz, D. W., and Stickle, W. B. 1990. Population genetics and systematics of the Leptasterias hexactis (Echinodermata: Asteroidea) species complex. Marine Biology, 105:477489.
Lessios, H. A. 1981. Divergence in allopatry: Molecular and morphological differentiation between sea urchins separated by the isthmus of Panama. Evolution, 35:618634.
Lessios, H. A. 1998. The first stage of speciation as seen in organisms separated by the Isthmus of Panama, p. 186201. In Howard, D. and Berlocher, S. (eds.), Endless Forms: Species and Speciation. Oxford University Press, Oxford.
Lessios, H. A., and Cunningham, C. W. 1990. Gametic incompatibility between species of the sea urchin Echinometra on the two sides of the Isthmus of Panama. Evolution, 44:933941.
Lessios, H. A., and Weinberg, J. R. 1994. Genetic and morphological divergence among morphotypes of the isopod Excirolana on the two sides of the Isthmus of Panama. Evolution, 48:530548.
Mayr, E. 1954. Geographic speciation in tropical echinoids. Evolution, 8:118.
Mayr, E. 1963. Animal species and evolution. Harvard University Press, Cambridge, 797 p.
Mayr, E., Linsley, E. G., and Usinger, R. L. 1953. Methods and principles of systematic zoology. McGraw-Hill, New York.
Marko, P. B. 1998. Historical allopatry and the biogeography of speciation in the prosobranch snail genus Nucella. Evolution, 52:757774.
Mastro, E., Chow, V., and Hedgecock, D. 1982. Littorina scutulata and Littorina plena: Sibling species status of two prosobranch gastropod species confirmed by electrophoresis. The Veliger, 24:239246.
Michaux, B. 1989. Morphological variation of species through time. Biological Journal of the Linnean Society, 38:239255.
Murphy, P. G. 1978. Colisella austrodigitalis sp. nov.: A sibling species of limpet (Acmaeidae) discovered by electrophoresis. Biological Bulletin, 155:193206.
Olsson, A. A. 1961. Molluscs of the tropical eastern Pacific, particularly from the southern half of the Panamic-Pacific faunal province (Panama to Peru). Panamic-Pacific Pelecypoda. Paleontological Research Institution, Ithaca, New York, 574 p.
Olsson, A. A. 1972. Origin of the existing Panamic biotas in terms of their geological history and their separation by the isthmian land bridge. Bulletin of the Biological Society of Washington, 2:117124.
Palmer, A. R. 1985. Quantum changes in gastropod shell morphology need not reflect speciation. Evolution, 39:699705.
Palmer, A. R., Gayron, S. D., and Woodruff, D. S. 1990. Reproductive, morphological, and genetic evidence for two cryptic species of Northeastern Pacific Nucella. The Veliger, 33:325338.
Petuch, E. J. 1981. A relict Neogene caenogastropod fauna from northern South America. Malacologia, 20:307347.
Reis, S. F., Pessoa, L. M., and Strauss, R. E. 1990. Application of size-free canonical discriminant analysis to studies of geographic differentiation. Revista Brasiliana Genetica, 13:509520.
Reyment, R. 1990. Reification of classical multivariate analysis in morphometry, p. 123144. In Rohlf, F. J. and Bookstein, F. L. (eds.), Proceedings of the Michigan Morphometrics Workshop. Special Publication No. 2 of The University of Michigan Museum of Zoology, Ann Arbor.
Roopnarine, P. D. 1996a. Systematics, biogeography, and extinction of chionine bivalves (Early Oligocene—Recent) in the late Neogene of tropical America. Malacologia, 38:103142.
Roopnarine, P. D. 1996b. A re-evaluation of evolutionary stasis between the bivalve species Chione erosa and Chione cancellata (Bivalvia: Veneridae). Journal of Paleontology, 69:280287.
Rosenblatt, R. H. 1963. Some aspects of speciation in marine shore fishes. Association of Systematists Publication No. 5:171180.
Rubinoff, I. 1963. Morphological comparisons of shore fishes separated by the Isthmus of Panama. Unpublished Ph.D. dissertation, Harvard University, Cambridge.
Schneider, J. A. 1995. Phylogenetic relationships of transisthmian Cardiidae (Bivalvia) and the use of fossils in reinterpreting the geminate species concept. Geological Society of America Abstracts with Programs, 27(6):A52.
Smith, A. B. 1994. Systematics and the fossil record: documenting evolutionary patterns. Blackwell Scientific Publications.
Stanley, S. M. 1986. Anatomy of a regional mass extinction: Plio-Pleistocene decimation of the Western Atlantic bivalve fauna. Palaios, 1:1736.
Stanley, S. M., and Yang, X. 1987. Approximate evolutionary stasis for bivalve morphology over millions of years: a multivariate study. Paleobiology, 13:113139.
Strauss, R. E., and Bookstein, F. L. 1982. The truss: body form reconstructions in morphometrics. Systematic Zoology, 31:113135.
Teranes, J. L., Geary, D. H., and Bemis, B. E. 1996. The oxygen isotopic record of seasonality in Neogene bivalves from the Central American Isthmus, p. 105129. In Jackson, J. B. C., Budd, A. F., and Coates, A. G. (eds.), Evolution and Environment in Tropical America. The University of Chicago Press, Chicago.
Trussell, G. C., and Smith, D. L. 2000. Induced defenses in response to an invading crab predator: an explanation of historical and geographic change. Proceedings of the National Academy of Sciences U.S.A., 97:21232127.
Vermeij, G. J. 1978. Biogeography and adaptation. Harvard University Press, Cambridge, 416 p.
Vermeij, G. J., and Petuch, E. J. 1986. Differential extinction in tropical American molluscs: endemism, architecture, and the Panama land bridge. Malacologia, 27:2941.
Weinberg, J. R., and Starczak, V. R. 1989. Morphological divergence of Eastern Pacific and Caribbean isopods: effects of a land barrier and the Panama Canal. Marine Biology, 103:143152.
Woodring, W. P. 1966. The Panama land bridge as a sea barrier. Proceedings of the American Philosophical Society, 110:425433.

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