Skip to main content Accessibility help
×
Home

The cryptic and the apparent reversed: lack of genetic differentiation within the morphologically diverse plexus of the planktonic foraminifer Globigerinoides sacculifer

  • Aurore André (a1), Agnes Weiner (a2), Frédéric Quillévéré (a1), Ralf Aurahs (a2), Raphaël Morard (a3), Christophe J. Douady (a4), Thibault de Garidel-Thoron (a5), Gilles Escarguel (a1), Colomban de Vargas (a3) and Michal Kucera (a2)...

Abstract

Previous genetic studies of extant planktonic foraminifera have provided evidence that the traditional, strictly morphological definition of species in these organisms underestimates their biodiversity. Here, we report the first case where this pattern is reversed. The modern (sub)tropical species plexus Globigerinoides sacculifer is characterized by large morphological variability, which has led to the proliferation of taxonomic names attributed to morphological end-members within the plexus. In order to clarify the taxonomic status of its morphotypes and to investigate the genetic connectivity among its currently partly disjunct (sub)tropical populations, we carried out a global survey of two ribosomal RNA regions (SSU and ITS-1) in all recent morphotypes of the plexus collected throughout (sub)tropical surface waters of the global ocean. Unexpectedly, we find an extremely reduced genetic variation within the plexus and no correlation between genetic and morphological divergence, suggesting taxonomical overinterpretation. The genetic homogeneity within the morphospecies is unexpected, considering its partly disjunct range in the (sub)tropical Atlantic and Indo-Pacific and its old age (early Miocene). A sequence variant in the rapidly evolving ITS-1 region indicates the existence of an exclusively Atlantic haplotype, which suggests an episode of relatively recent (last glacial) isolation, followed by subsequent resumption of unidirectional gene flow from the Indo-Pacific into the Atlantic. This is the first example in planktonic foraminifera where the morphological variability in a morphospecies exceeds its rDNA genetic variability. Such evidence for inconsistent scaling of morphological and genetic diversity in planktonic foraminifera could complicate the interpretation of evolutionary patterns in their fossil record.

Copyright

Corresponding author

Corresponding author. E-mail: frederic.quillevere@univ-lyon1.fr

References

Hide All
Akaike, H. 1974. A new look at the statistical model identification IEEE. Transactions on Automatic Control 19:716722.
Aurahs, R., Grimm, G. W., Hemleben, V., Hemleben, C., and Kucera, M. 2009a. Geographical distribution of cryptic genetic types in the planktonic foraminifer Globigerinoides ruber. Molecular Ecology 18:16921706.
Aurahs, R., Göker, M., Grimm, G. W., Hemleben, V., Hemleben, C., Schiebel, R., and Kucera, M. 2009b. Using the multiple analysis approach to reconstruct phylogenetic relationships among planktonic foraminifera from highly divergent and length polymorphic SSU rDNA sequences. Bioinformatics and Biology Insights 3:155177.
Aurahs, R., Treis, Y., Darling, K., and Kucera, M. 2011. A revised taxonomic and phylogenetic concept for the planktonic foraminifer species Globigerinoides ruber based on molecular and morphometric evidence. Marine Micropaleontology 79:114.
Aze, T., Ezard, T. H. G., Purvis, A., Coxall, H. K., Stewart, D. R. M., Wade, B. S., and Pearson, P. N. 2011. A phylogeny of Cenozoic macroperforate planktonic foraminifera from fossil data. Biological Reviews 86:900927.
Bandelt, H. J., Forster, P., and Röhl, A. 1999. Median Joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution 16:3748
Banner, F. T., and Blow, W. H. 1960. Some primary types of species belonging to the superfamily Globigerinaceae. Contributions from the Cushman Foundation for Foraminiferal Research 11:145.
Barrows, T. T., and Juggins, S. 2005. Sea-surface temperatures around the Australian margin and Indian Ocean during the Last Glacial Maximum. Quaternary Science Review 24:10171047.
Bard, E., and Rickaby, R. E. M. 2009. Migration of the subtropical front as a modulator of glacial climate. Nature 560:380384.
, A. W. 1980. Gametogenetic calcification in a spinose planktonic foraminifer, Globigerinoides sacculifer (Brady). Marine Micropaleontology 5:283310.
, A. W., Anderson, O. R., Faber, W. W., and Caron, D. A. 1983. Sequence of morphological and cytoplasmic changes during gametogenesis in the planktonic foraminifer Globigerinoides sacculifer (Brady). Micropaleontology 29:319325.
Beal, L. M., de Ruijter, W. P. M., Biastoch, A., Zahn, R., and SCOR/WCRP/IAPSO Working Group 136. 2011. On the role of the Agulhas system in ocean circulation and climate. Nature 472:429436.
Berggren, W. A., Kent, D. V., Swisher, C. C., and Aubry, M. P. 1995. A revised Cenozoic geochronology and chronostratigraphy. Geochronology, time scales and global stratigraphic correlation. SEPM, Tulsa, Okla.
Bickford, D., Lohman, D. J., Sodhi, N. S., Ng, P. K. L., Meier, R., Winker, K., Ingram, K. K., and Das, I. 2007. Cryptic species as a window on diversity and conservation. Trends in Ecology and Evolution 22:148155.
Bijma, J., Erez, J., and Hemleben, C. 1990. Lunar and semi-lunar reproductive cycles in some spinose planktonic foraminifers. Journal of Foraminiferal Research 20:117127.
Bijma, J., Hemleben, C., Oberhänsli, H., and Spindler, M. 1992. The effects of increased water fertility on tropical spinose planktonic foraminifers in laboratory cultures. Journal of Foraminiferal Research 22:242256.
Brady, H. B. 1877. Supplementary note on the foraminifera of the chalk (?) of the New Britain group. Geological Magazine London 4:534536.
Budillon, F., Lirer, F., Iorio, M., Macri, P., Sagnotti, L., Vallefuoco, M., Ferraro, L., Garziglia, S., Innangi, S., Sahabi, M., and Tonielli, R. 2009. Integrated stratigraphic reconstruction for the last 80 kyr in deep sector of the Sardinia Channel (Western Mediterranean). Deep Sea Research Part II, Topical Studies in Oceanography 56:725737.
Clarke, K. R. 1993. Non-parametric multivariate analysis of changes in community structure. Australian Journal of Ecology 18:117143.
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., Kroon, D., Wade, C. M., and Leigh Brown, A. J. . 1996. Molecular phylogeny of the planktic foraminifera. Journal of Foraminiferal Research 26:324330.
Darling, K. F., Wade, C. M., Kroon, D., and Leigh Brown, A. J. . 1997. Planktic foraminiferal molecular evolution and their polyphyletic origins from benthic taxa. Marine Micropaleontology 30:251266.
Darling, K. F., Wade, C. M., Kroon, D., Leigh Brown, A. J., and Bijma, J. 1999. The diversity and distribution of modern planktic foraminiferal SSU rRNA genotypes and their potential as tracers of present and past ocean circulations. Paleoceanography 14:312.
Darling, K. F., Kucera, M., Kroon, D., and Wade, C. M. 2006. A resolution for the coiling direction paradox in Neogloboquadrina pachyderma. Paleoceanography 2:PA2011.
de Vargas, C., and Pawlowski, J. 1998. Molecular versus taxonomic rates of evolution in planktonic foraminifera. Molecular Phylogenetics and Evolution 9:463469.
de Vargas, C., Zaninetti, L., Heinz, 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 45:85294.
de Vargas, C., Norris, R. D., Zaninetti, L., Stuart, W. G., 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 96:28642868.
de Vargas, C., Renaud, S., Heinz, H. and Pawlowski, J. 2001. Pleistocene adaptive radiation in Globorotalia truncatulinoides: genetic, morphologic, and environmental evidence. Paleobiology 27:104125.
de Vargas, C., Bonzon, M., Rees, N. W., Pawlowski, J., and Zaninetti, L. 2002. A molecular approach to biodiversity and biogeography in the planktonic foraminifer Globigerinella siphonifera (d'Orbigny). Marine Micropaleontology 45:101116.
Edgar, R. C. 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 32:17921797.
Flores, J.-A., Gersonde, R., and Sierro, F. 1999. Pleistocene fluctuations in the Agulhas Current Retroflection based on the calcareous plankton record. Marine Micropaleontology 37:122.
Göker, M., Grimm, G. W., Auch, A. F., Aurahs, R., and Kucera, M. 2010. A clustering optimization strategy for molecular taxonomy applied to planktonic foraminifera SSU rDNA. Evolutionary Bioinformatics 6:97112.
Groeneveld, J., Steph, S., Tiedemann, R., Garbe-Schonberg, D., Nurnberg, D., and Sturm, A. 2006. Pliocene mixed layer oceanography for site 1241 using combined Mg/Ca and δ18O analyses of Globigerinoides sacculifer. Proceedings of the Ocean Drilling Program, Scientific Results 202:127.
Guindon, S., and Gascuel, O. 2003. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology 52:696704.
Hecht, A. 1974. Intraspecific variation in recent populations of Globigerinoides ruber and Globigerinoides trilobus and their application to paleoenvironmental analysis. Journal of Paleontology 48:12171234.
Hemleben, C., Spindler, M., Breitinger, I., and Ott, R. 1987. Morphological and physiological responses of Globigerinoides sacculifer (Brady) under varying laboratory conditions. Marine Micropaleontology 12:305324.
Hofker, J. 1959. On the splitting of Globigerina. Contributions from the Cushman Foundation for Foraminiferal Research 10:19.
Huber, B. T., Bijma, J., and Darling, K. F. 1997. Cryptic speciation in the living planktonic foraminifer Globigerinella siphonifera (d'Orbigny). Paleobiology 23:3362.
Huson, D. H., and Bryant, D. 2006. Application of phylogenetic networks in evolutionary studies. Molecular Biology and Evolution 23:254267.
Kennett, J. P. 1976. Phenotypic variation in some recent and late Cenozoic planktonic foraminifera. Pp. 111170inHedley, R. H. and Adams, C. G., eds. Foraminifera 2. Academic Press, New York.
Kennett, J. P., and Srinivasan, M. S. 1983. An atlas of Neogene planktonic foraminifera: phylogenetic approach. Hutchinson and Ross, Stroudsburg, Penn.
Kooistra, W., Sarno, D., Balzano, S., Gu, H., Andersen, R. A., and Zingone, A. 2008. Global diversity and biogeography of Skeletonema species (Bacillariophyta). Protist 159:177193.
Kučera, M., and Schönfeld, J. 2007. The origin of modern oceanic foraminiferal faunas and Neogene climate change. InWilliams, M., Haywood, A. M., Gregory, F. J., and Schmidt, D. N., eds. Deep-time perspectives on climate change: marrying the signal from computer models and biological proxies. Micropalaeontological Society Special Publication 2:409426. Geological Society: London.
Kucera, M., Weinelt, M., Kiefer, T., Pflaumann, U., Hayes, A., Weinelt, M., Chen, M., Mix, A. C., Barrows, T. T., Cortijo, E., Duprat, J., Juggins, S., and Waelbroeck, C. 2005. Reconstruction of sea-surface temperatures from assemblages of planktonic foraminifera: multi-technique approach based on geographically constrained calibration data sets and its application to glacial Atlantic and Pacific Oceans. Quaternary Science Reviews 24:951998.
Larkin, M. A., Blackshields, G., Chenna, N. P., McGettigan, P. A., McWilliam, H., Valentin, F., Wallace, I. M., Wilm, A., Lopez, R., Thompson, J. D., Gibson, T. J., and Higgins, D. G. 2007. Clustal, W and Clustal, X, Version 2.0. Bioinformatics 23:29472948.
Leroy, L. W. 1939. Some small Foraminifera, Ostracoda and otoliths from the Neogene (“Miocene”) of the Rokan-Tapanoeli area, central Sumatra. Natuurkundig Tijdschrift Voor Nederlandsch Indië 251.
Lim, D. I., Kang, S., Yoo, H. S., Jung, H. S., Choi, J. Y., Kim, H. N., and Shin, I. H. 2006. Late Quaternary sediments on the outer shelf of the Korea Strait and their paleoceanographic implications. Geo-Marine Letters 26:287296.
Logares, R., Rengefors, K., Kremp, A., Shalchian-Tabrizi, K., Boltovskoy, A., Tengs, T., Shurtleff, A., and Klaveness, D. 2007. Phenotypically different microalgal morphospecies with identical ribosomal DNA: a case of rapid adaptive evolution? Microbial Ecology 53:549561.
Majewski, W., and Pawlowski, J. 2010. Morphologic and molecular diversity of the foraminiferal genus Globocassidulina in Admiralty Bay, King George Island. Antarctic Science 22:271281.
MARGO Project Members. 2009. Constraints on the magnitude and patterns of ocean cooling at the Last Glacial Maximum. Nature Geoscience 2:127132.
Morard, R., Quillévéré, F., Escarguel, G., Ujiié, Y., de Garidel-Thoron, T., Norris, R. D., and de Vargas, C. 2009. Morphological recognition of cryptic species in the planktonic foraminifer Orbulina universa. Marine Micropaleontology 71:148165.
Morard, R., Quillévéré, F., Douady, C. J., Escarguel, G., de Garidel-Thoron, T., and de Vargas, C. 2011. Worldwide genotyping in the planktonic foraminifer Globoconella inflata: implications for life history and paleoceanography. PLoS One 6 (10):e26665.
d'Orbigny, A. 1846. Foraminifères fossiles du bassin tertiaire de Vienne (Autriche). Gide et Comp, Paris.
Paradis, E., Claude, J., and Strimmer, K. 2004. APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20:289290.
Pawlowski, J. 2000. Introduction to the molecular systematics of foraminifera. Micropaleontology 46:112.
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 11:929–232.
Peeters, F., Acheson, R., Brummer, G. J., de Ruijter, W., Schneider, R., Ganssen, G., Ufkes, E., and Kroon, D. 2004. Vigorous exchange between the Indian and Atlantic oceans at the end of the past five glacial periods. Nature 430:661665.
Posada, D., and Crandall, K. A. 1998. Modeltest: testing the model of DNA substitution. Bioinformatics 14:817818.
Quillévéré, F., Morard, R., de Vargas, C., Douady, C., Ujiié, Y., de Garidel-Thoron, T., and Escarguel, G. 2013. Global scale same-specimen morpho-genetic analysis of Truncorotalia truncatulinoides: a perspective on the morphological species concept in planktonic foraminifera. Palaeogeography, Palaeoclimatology, Palaeoecology (in press). doi: 101.1016/j.paleo.2011.03.013.
R Development Core Team. 2008. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna.
Reuss, A. E. 1850. Neue Foraminiferen aus den Schichten des österreichischen Tertiarbeckens. Denkschriften der Kaiserlichen Akademie der Wissenschaften, Mathematisch-Naturwissenschaftliche Classe 1:365390.
Saez, A. G., Probert, I., Geisen, M., Quinn, P., Young, J. R., and Medlin, L. K. 2003. Pseudocryptic speciation in coccolithophores. Proceedings of the National Academy of Sciences USA 100:71637168.
Saito, T., Thomson, P. R., and Berger, D. 1981. Systematic index of Recent and Pleistocene planktonic foraminifera. University of Tokyo Press, Tokyo.
Siani, G., Paterne, M., and Colin, C. 2010. Late glacial to Holocene planktic foraminifera bioevents and climatic record in the South Adriatic Sea. Journal of Quaternary Science 25:808821.
Siccha, M., Trommer, G., Schulz, H., Hemleben, C., and Kucera, M. 2009. Factors controlling the distribution of planktonic foraminifera in the Red Sea and implications for the development of transfer functions. Marine Micropaleontology 72:146156.
Spooner, M. I., Barrows, T. T., De Deckker, P., and Paterne, M. 2005. Palaeoceanography of the Banda Sea, and Late Pleistocene initiation of the Northwest Monsoon. Global and Planetary Change 49:2846.
Tolderlund, D. S., and Be, A. W. H. 1971. Seasonal distribution of planktonic foraminifera in the western North Atlantic. Micropaleontology 17:297329.
Tsuchiya, M., Grimm, G. W., Heinz, P., Stögerer, K., Topoc Ertan, K., Collen, J., Brüchert, V., Hemleben, C., Hemleben, V., and Kitazato, H. 2009. Ribosomal DNA shows extremely low genetic divergence in a worldwide distributed, but disjunct and highly adapted marine protozoan (Virgulinella fragilis, Foraminiferida). Marine Micropaleontology 70:819.
Ujiié, Y., and Lipps, J. H. 2009. Cryptic diversity in planktic foraminifera in the northwest Pacific Ocean. Journal of Foraminiferal Research 39:145154.
Ujiié, Y., de Garidel-Thoron, T., Watanabe, S., Wiebe, P., and de Vargas, C. 2010. Coiling dimorphism within a genetic type of the planktonic foraminifer Globorotalia truncatulinoides. Marine Micropaleontology 77:145153.
Wade, C., Darling, K., Kroon, D., and Brown, A. 1996. Early evolutionary origin of the planktonic foraminifera inferred from SSU rDNA sequences comparison. Journal of Molecular Evolution 43:672677.
Williams, M., Schmidt, D. N., Wilkinson, I. P., Miller, C. G., and Taylor, P. D. 2006. The type material of the Miocene to Recent species Globigerinoides sacculifer (Brady) revisited. Journal of Micropaleontology 25:153156.
Wilson, B. 2012. Biogeography and ecostratigraphy of Late Quaternary planktonic foraminiferal taphocoenoses in the Leeward Islands, Lesser Antilles, NE Caribbean Sea. Marine Micropaleontology 86–87:110.

The cryptic and the apparent reversed: lack of genetic differentiation within the morphologically diverse plexus of the planktonic foraminifer Globigerinoides sacculifer

  • Aurore André (a1), Agnes Weiner (a2), Frédéric Quillévéré (a1), Ralf Aurahs (a2), Raphaël Morard (a3), Christophe J. Douady (a4), Thibault de Garidel-Thoron (a5), Gilles Escarguel (a1), Colomban de Vargas (a3) and Michal Kucera (a2)...

Metrics

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed