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Pleistocene adaptive radiation in Globorotalia truncatulinoides: genetic, morphologic, and environmental evidence

Published online by Cambridge University Press:  08 February 2016

Colomban de Vargas ,
Sabrina Renaud ,
Heinz Hilbrecht  and
Jan Pawlowski
Colomban de Vargas
Affiliation:
Département de Zoologie et Biologie Animale, Université de Genève, CH-1224 Chěne-Bougeries, Switzerland
Sabrina Renaud
Affiliation:
Geological Institute, ETH, CH-8092 Zürich, Switzerland
Heinz Hilbrecht
Affiliation:
Geological Institute, ETH, CH-8092 Zürich, Switzerland
Jan Pawlowski
Affiliation:
Département de Zoologie et Biologie Animale, Université de Genève, CH-1224 Chěne-Bougeries, Switzerland
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Abstract

Globorotalia truncatulinoides is an extant species of planktic foraminiferans commonly used for stratigraphic and paleoenvironmental analyses. It originated ∼2.8 m.y. ago in subtropical areas of the South Pacific, spread to all subtropical and temperate regions of the world ocean, and expanded its range to southern subantarctic waters between 500 and 200 Ka. The wide geographic distribution of G. truncatulinoides is associated with a latitudinal morphological variability considered as an ecophenotypic variation within a single species. Here, we present the first molecular, morphological, and ecological evidence that G. truncatulinoides corresponds to a complex of four genetic species adapted to particular hydrographic conditions. The different species are separated by significant genetic distances in several ribosomal genes (SSU, ITS-1, 5.8S, ITS-2). Species 1 and species 2 characterize subtropical waters, species 3 is abundant exclusively in the Subantarctic Convergence, while species 4 inhabits subantarctic waters. By using an absolute molecular clock, we deduce the time of divergence between the subtropical and frontal/subantarctic species at ∼300 Ka, which is in agreement with stratigraphic data and suggests an adaptive radiation of the species allowing it to colonize the nutrient-rich and cold subantarctic waters. This genetic dichotomy is associated with a morphological differentiation identified using outline analysis. Species of the same regions are more similar in test shape but can be distinguished by coiling direction. The evolutionary patterns recognized here by combining DNA and morphological analyses from plankton-tow specimens mirror and allow a new interpretation of the data available from Recent sediments. They highlight the importance of adaptation and heterochronic processes, leading to cryptic speciation, in planktic foraminifera.

Type
Articles
Information
Paleobiology , Volume 27 , Issue 1 , Winter 2001 , pp. 104 - 125
Copyright
Copyright © The Paleontological Society 

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References

Literature Cited

Bolli, H. M., and Saunders, J. B.Late Middle Eocene to Recent planktonic foraminiferal biostratigraphy. Pp. 144–262in Bolli, H. M., Saunders, J. B., and Perch-Nielsen, K., eds. Plankton stratigraphy. Cambridge University Press, Cambridge.Google Scholar
Crampton, J. S. 1995. Elliptic Fourier shape analysis of fossil bivalves: some practical considerations. Lethaia 28:179–186.CrossRefGoogle Scholar
Darling, K., Wade, C. M., Kroon, D., Brown, A. J. Leigh, and Bijma, J. 1999. The diversity and distribution of modern planktic foraminiferal small subunit ribosomal RNA genotypes and their potential as tracers of present and past ocean circulations. Paleoceanography 14:3–12.CrossRefGoogle Scholar
Darling, K., Wade, C. M., Stewart, I. A., Kroon, D., Dingle, R., and Brown, A. J. Leigh 2000. Molecular evidence for genetic mixing of Arctic and Antarctic subpolar populations of planktonic foraminifers. Nature 405:43–47.CrossRefGoogle ScholarPubMed
DeLong, E. F., Wu, K. Y., Prézelin, B. B., and Jovine, R. V. M. 1994. High abundance of Archaea in Antarctic marine picoplankton. Nature 371:695–697.CrossRefGoogle ScholarPubMed
Deuser, W. G., Ross, E. H., Hemleben, C., and Spindler, M. 1981. Seasonal changes in species composition, number, mass, size, and isotopic composition of planktonic foraminifera settling into the deep Sargasso Sea. Palaeogeography, Palaeoclimatology, Palaeoecology 33:103–127.CrossRefGoogle Scholar
de Vargas, C., and Pawlowski, J. 1998. Molecular versus taxonomic rates of evolution in planktonic foraminifera. Molecular Phylogenetics and Evolution 9:463–469.CrossRefGoogle ScholarPubMed
de Vargas, C., Zaninetti, L., Hilbrecht, H., and Pawlowski, J. 1997. Phylogeny and rates of molecular evolution of planktonic foraminifera: SSU rDNA sequences compared to the fossil record. Journal of Molecular Evolution 45:285–294.CrossRefGoogle ScholarPubMed
de Vargas, C., Norris, R., Zaninetti, L., Gibb, S. W., and Pawlowski, J. 1999. Molecular evidence of cryptic speciation in planktonic foraminifers and their relation to oceanic provinces. Proceedings of the National Academy of Sciences USA 96:2864–2868.CrossRefGoogle ScholarPubMed
de Vargas, E., Bonzon, M., Rees, N., Pawlowski, J., and Zaninetti, L.In press. A molecular approach to biodeversity and biogeography in the planktonic foraminifera Globigerinella siphonifera (d'Orbigny). Marine Micropaleontology.Google Scholar
Ehrlich, R., and Weinberg, B. 1970. An exact method for characterization of grain shape. Journal of Sedimentary Petrology 40:205–212.Google Scholar
Fairbanks, R. G., and Wiebe, P. H. 1980. Foraminifera and chlorophyll maximum: vertical distribution, seasonal succession, and paleoceanographic significance. Science 209:1524–1526.CrossRefGoogle ScholarPubMed
Ferris, M. J., and Palenik, B. 1998. Niche adaptation in ocean cyanobacteria. Nature 396:226–228.CrossRefGoogle Scholar
Fuhrman, J. A., and Campbell, L. 1998. Microbial biodiversity. Nature 393:410–411.CrossRefGoogle Scholar
Galtier, N., and Gouy, M. 1996. SEAVIEW and PHYLO_WIN: two graphic tools for sequence alignment and molecular phylogeny. Computer Applications in the Biosciences 12:543–548.Google ScholarPubMed
Giovannoni, S. J., Britschgi, T. B., Moyer, C. L., and Field, K. G. 1990. Genetic diversity in Sargasso Sea bacterioplankton. Nature 344:60–63.CrossRefGoogle Scholar
Healy-Williams, N. 1983. Fourier shape analysis of Globorotalia truncatulinoides from late Quaternary sediments in the southern Indian Ocean. Marine Micropaleontology 8:1–15.CrossRefGoogle Scholar
Healy-Williams, N., and Williams, D. F. 1981. Fourier analysis of test shape of planktonic foraminifera. Nature 289:485–487.CrossRefGoogle Scholar
Healy-Williams, N., Ehrlich, R., and Williams, D. F. 1985. Morphometric and stable isotopic evidence for subpopulations of Globorotalia truncatulinoides. Journal of Foraminiferal Research 15:242–253.CrossRefGoogle Scholar
Hemleben, C., Spindler, M., Breitinger, I., and Deuser, W. G. 1985. Field and laboratory studies on the ontogeny and ecology of some globorotaliid species from the Sargasso Sea off Bermuda. Journal of Foraminiferal Research 15:254–272.CrossRefGoogle Scholar
Hemleben, C., Spindler, M., and Anderson, O. R. 1989. Modern planktonic foraminifera. Springer, New-York.CrossRefGoogle Scholar
Hills, S. J. 1988. The analysis of microfossil shape: experiments using planktonic foraminifera. Ph.D. dissertation. University of California, San Diego.Google Scholar
Hills, S. J., and Thierstein, H. R. 1989. Plio-Pleistocene calcareous plankton biochronology. Marine Micropaleontology 14:67–69.CrossRefGoogle Scholar
Holzmann, M., Piller, W., and Pawlowski, J. 1996. Sequence variations in the Large-SubUnit RNA gene of Ammonia (Foraminifera, Protozoa) and their evolutionary implications. Journal of Molecular Evolution 43:145–151.CrossRefGoogle ScholarPubMed
Hooker, S. B., Rees, N. W., and Aiken, J.In press. An objective methodology for identifying oceanic provinces. Progress in Oceanography.Google Scholar
Huber, B. T., Bijma, J., and Darling, K. 1997. Cryptic speciation in the living planktonic foraminifer Globigerinella siphonifera (d'Orbigny). Paleobiology 23:33–62.CrossRefGoogle Scholar
Kelly, D. C., Arnold, A. J., and Parker, W. C. 1999. The influence of heterochrony on the stratigraphic occurrence of Morozovella ungulata. Journal of Foraminiferal Research 29:58–68.Google Scholar
Kennett, J. P. 1968. Globorotalia truncatulinoides as a paleo-oceanographic index. Science 159:1461–1463.CrossRefGoogle ScholarPubMed
Kennett, J. P. 1970. Pleistocene paleoclimates and foraminiferal biostratigraphy in subantarctic deep-sea cores. Deep-Sea Research 17:125–140.Google Scholar
Kennett, J. P. 1976. Phenotypic variation in some Recent and Late Cenozoic planktonic foraminifera. Pp. 1–60in Hedley, R. H. and Adams, C. G., eds. Foraminifera, Vol. 2, Academic Press, London.Google Scholar
Kennett, J. P., and Srinivasan, M. S. 1983. An atlas of Neogene planktonic foraminifera: phylogenetic approach. Hutchinson and Ross, Stroudsburg, Penn.Google Scholar
Larsen, N., Olsen, G. J., Maidak, B. L., McCaughey, M. J., Overbeek, R., Macke, T. J., Marsh, T. L., and Woese, C. R. 1993. The ribosomal database project. Nucleic Acids Research 21:3021–3023.CrossRefGoogle ScholarPubMed
Lazarus, D., Hilbrecht, H., Spencer-Cervato, C., and Thierstein, H. 1995. Sympatric speciation and phyletic change in Globorotalia truncatulinoides. Paleobiology 21:26–51.CrossRefGoogle Scholar
Lohmann, G. P. 1992. Increasing seasonal upwelling in the subtropical South Atlantic over the past 700,000 yrs: evidence from deep-living planktonic foraminifera. Marine Micropaleontology 19:1–12.CrossRefGoogle Scholar
Lohmann, G. P., and Malmgren, B. A. 1983. Equatorward migration of Globorotalia truncatulinoides ecophenotypes through the Late Pleistocene: gradual evolution or ocean change? Paleobiology 9:414–421.CrossRefGoogle Scholar
Lohmann, G. P., and Schweitzer, P. N. 1990. Globorotalia truncatulinoides: growth and chemistry as probes of the past thermocline. 1. Shell size. Paleoceanography 5:55–75.CrossRefGoogle Scholar
Martinez, J. I. 1997. Decreasing influence of Subantarctic Mode Water north of the Tasman Front over the past 150 ky. Palaeogeography, Palaeoclimatology, Palaeoecology 131:355–364.CrossRefGoogle Scholar
Miya, M., and Nishida, M. 1997. Speciation in the open ocean. Nature 389:803–804.CrossRefGoogle Scholar
Moore, L. R., Rocap, G., and Chisholm, S. W. 1998. Physiology and molecular phylogeny of coexisting Prochlorococcus ecotypes. Nature 393:464–467.CrossRefGoogle ScholarPubMed
Mulitza, S., Dürkoop, A., Walter, H., Wefer, G., and Niebler, H. S. 1997. Planktonic foraminifera as recorders of past surface-water stratification. Geology 25:335–338.2.3.CO;2>CrossRefGoogle Scholar
Norris, R. D., Corfield, R. M., and Cartlidge, J. E. 1994. Evolutionary ecology of Globorotalia (Globoconella) (planktic foraminifera). Marine Micropaleontology 23:121–145.CrossRefGoogle Scholar
Olsen, G. J., Matsuda, H., Hagstrom, R., and Overbeek, R. 1994. FastDNAml: a tool for construction of phylogenetic trees of DNA sequences using maximum likelihood. Computer Applications in the Biosciences 10:41–48.Google ScholarPubMed
Palumbi, S. R. 1992. Marine speciation on a small planet. Trends in Ecology and Evolution 7:114–118.CrossRefGoogle ScholarPubMed
Pawlowski, J., Bolivar, I., Fahrni, J., de Vargas, C., Gouy, M., and Zaninetti, L. 1997. Extreme differences in rates of molecular evolution of foraminifera revealed by comparison of ribosomal DNA sequences and the fossil record. Molecular Biology and Evolution 14:498–505.CrossRefGoogle ScholarPubMed
Perrière, G., and Gouy, M. 1996. WWW-Query: an on-line retrieval system for biological sequence banks. Biochimie 78:364–369.CrossRefGoogle ScholarPubMed
Pharr, R. B. 1983. Examination of the late Quaternary paleobiology of Globorotalia truncatulinoides using Fourier shape analysis. Ph.D. dissertation. University of South Carolina, Columbia.Google Scholar
Pharr, R. B. Jr., and Williams, D. F. 1987. Shape changes in Globorotalia truncatulinoides as a function of ontogeny and paleobiogeography in the southern ocean. Marine Micropaleontology 12:343–355.CrossRefGoogle Scholar
Postuma, J. A. 1971. Manual of planktonic foraminifera. Elsevier, Amsterdam.Google Scholar
Renaud, S., and Girard, C. 1999. Strategies of survival during extreme environmental perturbations: evolution of conodonts in response to the Kellwasser crisis (Upper Devonian). Palaeogeography, Palaeoclimatology, Palaeoecology 146:19–32.CrossRefGoogle Scholar
Renaud, S., Michaux, J., Jaeger, J.-J., and Auffray, J.-C. 1996. Fourier analysis applied to Stephanomys (Rodentia, Muridae) molars: nonprogressive evolutionary pattern in a gradual lineage. Paleobiology 22:255–265.CrossRefGoogle Scholar
Renaud, S., Benammi, M., and Jaeger, J.-J. 1999a. Morphological evolution of the murine rodent Paraethomys in response to climatic variations (Mio-Pliocene of North Africa). Paleobiology 25:369–382.CrossRefGoogle Scholar
Renaud, S., Michaux, J., Mein, P., Aguilar, J.-P., and Auffray, J.-C. 1999b. Patterns of size and shape differentiation during the evolutionary radiation of the European Miocene murine rodents. Lethaia 32:61–71.CrossRefGoogle Scholar
Robins, D. B., and Aiken, J. 1996. The Atlantic Meridional Transect: an oceanographic research programme to investigate physical, chemical, biological and optical variables of the Atlantic Ocean. Underwater Technology 21:8–14.CrossRefGoogle Scholar
Rohlf, F. J., and Archie, J. W. 1984. A comparison of Fourier methods for the description of wing shape in mosquitoes (Diptera: Culicidae). Systematic Zoology 33:302–317.CrossRefGoogle Scholar
Saitou, N., and Nei, M. 1987. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Molecular Biology and Evolution 4:406–425.Google Scholar
Spencer-Cervato, C., and Thierstein, H. R. 1997. First appearance of Globorotalia truncatulinoides: cladogenesis and immigration. Marine Micropaleontology 30:267–291.CrossRefGoogle Scholar
Stanley, S. M., Wetmore, K. L., and Kennett, J. P. 1988. Macroevolutionary differences between the two major clades of Neogene planktonic foraminifera. Paleobiology 14:235–249.CrossRefGoogle Scholar
Tajima, F., and Nei, M. 1984. Estimation of evolutionary distance for reconstructing molecular phylogenetic trees. Molecular Biology and Evolution 18:278–286.Google Scholar
Takayanagi, Y., Niitsuma, N., and Sakai, T. 1968. Wall microstructure of Globorotalia truncatulinoides d'Orbigny. Science report of Tohoku University, 2d series (Geology) 40:141–170.Google Scholar
Thiede, J. 1971. Variations in coiling ratios of Holocene planktonic foraminifera. Deep-Sea Research 18:823–831.Google Scholar
Wei, K. 1994. Allometric heterochrony in the Pliocene-Pleistocene planktic foraminiferal clade Globoconella. Paleobiology 20:66–84.CrossRefGoogle Scholar
Willson, H. R., and Rees, N. W.In press. Use of in situ and satellite imagery to interpret mesoscale features in the Brazil-Falkland current confluence zone. Progress in Oceanography.Google Scholar