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Mosaic evolution in the middle Miocene planktonic foraminifera Fohsella lineage

  • Weimin Si (a1), William A. Berggren (a1) and Marie-Pierre Aubry (a1)

Recent studies have shown that modes of evolution, namely directional trend, random walk, and stasis, vary across morphologic traits and over the geographic range of a taxon. If so, is it possible that our interpretation of evolutionary modes is actually driven by our selection of traits in a study? In an attempt to answer this question, we have restudied the middle Miocene planktonic foraminifera Fohsella lineage, an iconic example of gradual morphologic evolution. In contrast to previous studies that have focused on the gross morphology as embodied by the edge view of tests, we analyze here multiple phenotypic traits chosen because their biologic and ecologic significance is well understood in living populations. We find that traits in the lineage did not evolve in concert. The timing and geographic pattern of changes in shape, coiling direction, size, and ecology were different. The evolution of this lineage is a mosaic combination of different evolutionary modes for different traits. We suggest that overemphasis on the evolution of some single trait, such as the edge-view outline, from narrow geographic ranges has significantly underestimated the dynamic evolutionary history of this group.

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Alroy, J. 2000. Understanding the dynamics of trends within evolving lineages. Paleobiology 26:319329.
Arnold, J. 1983. Phyletic evolution in the Globorotalia crassaformis (Galloway and Wissler) lineage—a preliminary report. Paleobiology 9:390397.
Birch, H., Coxall, H. K., Pearson, P. N., Kroon, D., and O’Regan, M.. 2013. Planktonic foraminifera stable isotopes and water column structure: disentangling ecological signals. Marine Micropaleontology 101:127145.
Blow, W. H., and Banner, F.. 1966. The morphology, taxonomy and biostratigraphy of Globorotalia barisanensis LeRoy, Globorotalia fohsi Cushman and Ellisor, and related taxa. Micropaleontology 12:286302.
Bolli, H. M. 1950. The direction of coiling in the evolution of some Globorotaliidae. Contributions from the Cushman Foundation for Foraminiferal Research 1:8289.
Bolli, H. M., and Saunders, J. B.. 1985. Oligocene to Holocene low latitude planktic foraminifera. Pp. 212215 in H. M. Bolli, J. B. Saunders, and K. Perch-Nielsen, eds. Plankton stratigraphy Vol. 1. Cambridge University Press, Cambridge.
Darling, K. F., and Wade, C. M.. 2008. The genetic diversity of planktic foraminifera and the global distribution of ribosomal RNA genotypes. Marine Micropaleontology 67:216238.
Darling, K. F., Kucera, M., Pudsey, C. J., and Wade, C. M.. 2004. Molecular evidence links cryptic diversification in polar planktonic protists to Quaternary climate dynamics. Proceedings of the National Academy of Sciences USA 101:76577662.
de Vargas, C., Renaud, S., Hilbrecht, H., and Pawlowski, J.. 2001. Pleistocene adaptive radiation in Globorotalia truncatulinoides: genetic, morphologic, and environmental evidence . Paleobiology 27:104125.
Eisenach, A. R., and Kelly, D. C.. 2006. Coiling preferences and evolution in the middle Miocene Fohsella chronocline. Marine Micropaleontology 60:243257.
Eldredge, N., Thompson, J. N., Brakefield, P. M., Gavrilets, S., Jablonski, D., Jackson, J. B., Lenski, R. E., Lieberman, B. S., McPeek, M. A., and Miller, W.. 2005. The dynamics of evolutionary stasis. Paleobiology 31:133145.
Fairbanks, R. G., Wiebe, P. H., and Be, A. W.. 1980. Vertical distribution and isotopic composition of living planktonic foraminifera in the Western North Atlantic. Science 207:6163.
Flower, B. P., and Kennett, J. P.. 1994. The middle Miocene climatic transition—East Antarctic ice-sheet development, deep-ocean circulation and global carbon cycling. Palaeogeography, Palaeoclimatology, Palaeoecology 108:537555.
Grey, M., Haggart, J. W., and Smith, P. L.. 2008. Variation in evolutionary patterns across the geographic range of a fossil bivalve. Science 322:12381241.
Hayashi, H., Idemitsu, K., Wade, B. S., Idehara, Y., Kimoto, K., Nishi, H., and Matsui, H.. 2013. Middle Miocene to Pleistocene planktonic foraminiferal biostratigraphy in the eastern equatorial Pacific Ocean. Paleontological Research 17:91109.
Hemleben, C., Spindler, M., and Anderson, O. R.. 1989. Modern planktonic foraminifera. Springer-Verlag, New York.
Hodell, D. A., and Vayavananda, A.. 1993. Middle Miocene paleoceanography of the western equatorial Pacific (DSDP site 289) and the evolution of Globorotalia (Fohsella). Marine Micropaleontology 22:279310.
Holbourn, A., Kuhnt, W., Frank, M., and Haley, B. A.. 2013. Changes in Pacific Ocean circulation following the Miocene onset of permanent Antarctic ice cover. Earth and Planetary Science Letters 365:3850.
Holbourn, A., Kuhnt, W., Lyle, M., Schneider, L., Romero, O., and Andersen, N.. 2014. Middle Miocene climate cooling linked to intensification of eastern equatorial Pacific upwelling. Geology 42:1922.
Hopkins, M. J., and Lidgard, S.. 2012. Evolutionary mode routinely varies among morphological traits within fossil species lineages. Proceedings of the National Academy of Sciences USA 109:2052020525.
Huber, B. T., Bijma, J., and Darling, K.. 1997. Cryptic speciation in the living planktonic foraminifer Globigerinella siphonifera (d’Orbigny). Paleobiology 23:3362.
Hull, P. M., and Norris, R. D.. 2009. Evidence for abrupt speciation in a classic case of gradual evolution. Proceedings of the National Academy of Sciences USA 106:2122421229.
Hunt, G. 2006. Fitting and comparing models of phyletic evolution: random walks and beyond. Paleobiology 32:578601.
Hunt, G., Hopkins, M. J., and Lidgard, S.. 2015. Simple versus complex models of trait evolution and stasis as a response to environmental change. Proceedings of the National Academy of Sciences 112:48854890.
Keller, G. 1985. Depth stratification of planktonic foraminifers in the Miocene ocean. Geological Society of America Memoirs 163:177196.
Kennett, J. P., and Srinivasan, M.. 1983. Neogene planktonic foraminifera: a phylogenetic atlas. Hutchinson Ross, Stroudsburg, Pa.
Kirkpatrick, M., and Barton, N. H.. 1997. Evolution of a species’ range. American Naturalist 150:123.
Kučera, M., and Kennett, J. P.. 2002. Causes and consequences of a middle Pleistocene origin of the modern planktonic foraminifer Neogloboquadrina pachyderma sinistral. Geology 30:539542.
Lazarus, D., Hilbrecht, H., Spencer-Cervato, C., and Thierstein, H.. 1995. Sympatric speciation and phyletic change in Globorotalia truncatulinoides . Paleobiology 21:2851.
Malmgren, B. A., Berggren, W. A., and Lohmann, G. P.. 1983. Evidence for punctuated gradualism in the Late Neogene Globorotalia tumida lineage of planktonic-foraminifera. Paleobiology 9:377389.
Miller, K. G., Baluyot, R., Wright, J. D., Kopp, R. E., and Browning, J. V.. 2017. Closing an early Miocene astronomical gap with Southern Ocean δ18O and δ13C records: implications for sea level change, Paleoceanography 32:10.1002/2016PA003074.
Nathan, S. A., and Leckie, R. M.. 2009. Early history of the Western Pacific Warm Pool during the middle to late Miocene (~13.2–5.8 Ma): role of sea-level change and implications for equatorial circulation. Palaeogeography, Palaeoclimatology, Palaeoecology 274:140159.
Norris, R. D. 1991. Parallel evolution in the keel structure of planktonic foraminifera. Journal of Foraminiferal Research 21:319331.
Norris, R. D. 2000. Pelagic species diversity, biogeography, and evolution. Paleobiology 26:236258.
Norris, R. D., Corfield, R. M., and Cartlidge, J. E.. 1993. Evolution of depth ecology in the planktic foraminifera lineage Globorotalia (Fohsella). Geology 21:975978.
Norris, R. D., Corfield, R. M., and Cartlidge, J. E.. 1996. What is gradualism? Cryptic speciation in globorotaliid foraminifera. Paleobiology 22:386405.
Olsson, R. K. 1971. The logarithmic spire in planktonic foraminifera: its use in taxonomy, evolution, and paleoecology. Gulf Coast Association of Geological Societies Transactions 21:419432.
Pearson, P. N., and Ezard, T. H. G.. 2014. Evolution and speciation in the Eocene planktonic foraminifer Turborotalia . Paleobiology 40:130143.
Schmidt, D. N., Renaud, S., Bollmann, J., Schiebel, R., and Thierstein, H. R.. 2004. Size distribution of Holocene planktic foraminifer assemblages: biogeography, ecology and adaptation. Marine Micropaleontology 50:319338.
Sheets, H. D., and Mitchell, C. E.. 2001. Why the null matters: statistical tests, random walks and evolution. Genetica 112:105125.
Stewart, J. A., Wilson, P. A., Edgar, K. M., Anand, P., and James, R. H.. 2012. Geochemical assessment of the palaeoecology, ontogeny, morphotypic variability and palaeoceanographic utility of “Dentoglobigerinavenezuelana . Marine Micropaleontology 84:7486.
Tabachnick, R. E., and Bookstein, F. L.. 1990. The structure of individual variation in Miocene Globorotalia . Evolution 44:416434.
Ujiié, Y., and Asami, T.. 2014. Temperature is not responsible for left-right reversal in pelagic unicellular zooplanktons. Journal of Zoology 293:1624.
van Sebille, E., Scussolini, P., Durgadoo, J. V., Peeters, F. J., Biastoch, A., Weijer, W., Turney, C., Paris, C. B., and Zahn, R.. 2015. Ocean currents generate large footprints in marine palaeoclimate proxies. Nature Communication 6:6521. doi: 10.1038/ncomms7521.
Wright, J. D., Miller, K. G., and Fairbanks, R. G.. 1992. Early and middle Miocene stable isotopes: implications for deepwater circulation and climate. Paleoceanography 7:357389.
Zelditch, M. L., Swiderski, D. L., and Sheets, H. D.. 2004. Geometric morphometrics for biologists: a primer. Elsevier, Amsterdam.
Zhang, Y. G., Pagani, M., and Liu, Z.. 2014. A 12-million-year temperature history of the tropical Pacific Ocean. Science 344:8487.
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