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How Has Foraminiferal Genetic Diversity Developed? A Case Study of Planoglabratella opercularis and the Species Concept Inferred from Its Ecology, Distribution, Genetics, and Breeding Behavior

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Book cover Approaches to Study Living Foraminifera

Abstract

The nature of Planoglabratella opercularis has been revealed through multidisciplinary studies focusing on its ecology, life cycle, growth rate, interbreeding, morphology, natural abundance, distribution, and molecular ecology. Our research is aimed at revealing the processes and mechanisms behind foraminiferal evolution. P. opercularis is a benthic inhabitant of rocky-shore environments, where it crawls on coralline algae. Gametes are not released into the ambient seawater; rather this species forms plastogamic pairs and exchanges gametes inside the shell. Thus, the mobility and dispersal of both individuals and gametes are extremely low. In fact, genetic divergence has likely occurred within each geographic population. Interpopulational breeding experiments revealed breeding incompatibility between gamont specimens from widely separated local populations. The genetic connectivity in P. opercularis is affected by ecological characteristics such as habitat and mobility. Molecular ecological studies have revealed that P. opercularis likely diversified through reproductive isolation resulting from geographical separation following changes in land–ocean distributions.

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References

  • Aizawa M (1987) The seasonal changes in benthic foraminifera at the rocky shore. Undergraduate thesis, Institute of Geosciences, Shizuoka University, p 40 (in Japanese with English abstract)

    Google Scholar 

  • Alve E, Goldstein ST (2002) Resting stage in benthic foraminiferal propagules: a key feature for dispersal? Evidence from two shallow-water species. J Micropalaeontol 21:95–96

    Article  Google Scholar 

  • Alve E, Goldstein ST (2003) Propagule transport as a key method of dispersal in benthic foraminifera (Protista). Limnol Oceanogr 48:2163–2170

    Article  Google Scholar 

  • Asano K (1951) Illustrated catalogue of Japanese Tertiary smaller foraminifera, part 14. Hosokawa Printing Co, Tokyo, pp 1–14

    Google Scholar 

  • Chinzei K (1986) Faunal succession and geographic distribution of Neogene molluscan faunas in Japan. In: Kotaka T (ed) Japanese Cenozoic mulluscs-their origin and migration. Paleontological Society of Japan, Special papers, no. 29, pp 17–32

    Google Scholar 

  • Chinzei K (1991) Late Cenozoic zoogeography of the Sea of Japan area. Episodes 14:231–235

    Google Scholar 

  • Darling KF, Wade CM (2008) The genetic diversity of planktic foraminifera and the global distribution of ribosomal RNA genotypes. Mar Micropaleontol 67:216–238

    Article  Google Scholar 

  • Darling KF, Kucera M, Pudsey CJ, Wade CM (2004) Molecular evidence links cryptic diversification in polar planktonic protists to Quaternary climate dynamics. Proc Natl Acad Sci USA 101:7657–7662. doi:10.1073/pnas.0402401101

    Article  CAS  Google Scholar 

  • Erskian MG, Lipps JH (1987) Population dynamics of the foraminiferan Glabratella ornatissima (Cushman) in northern California. J Foramin Res 17:240–250

    Article  Google Scholar 

  • Ertan KT, Hemleben V, Hemleben C (2004) Molecular evolution of some selected benthic foraminifera as inferred from sequences of the small subunit ribosomal DNA. Mar Micropaleontol 53:367–388

    Article  Google Scholar 

  • Fujita Y, Ito S (1957) A study of the foraminiferal assemblages from the Miocene formation, Date District, Fukushima Prefecture, Japan. J Geol Soc Jpn 63:497–513 (in Japanese, with English abstract)

    Article  Google Scholar 

  • Grell KG (1954) Der Generationswechsel der polythalamen Foraminifere Rotaliella heterocaryotica. Arch Protistk 100:211–235

    Google Scholar 

  • Grell KG (1957) Untersuchungen ĂĽber die Fortpflanzung und sexualität der Foraminiferen I. Rotaliella roscoffensis. Arch Protistk 102:147–164

    Google Scholar 

  • Grell KG (1958) Untersuchungen ĂĽber die Fortpflanzung und sexualität der Foraminiferen III. Glabratella sulcata. Arch Protistk 102:449–472

    Google Scholar 

  • Grell KG (1979) Cytogenetic systems and evolution in foraminifera. J Foramin Res 9:1–13

    Article  Google Scholar 

  • Grimm GW, Stögerer K, Ertan KT, Kitazato H, KuÄŤera M, Hemleben V, Hemleben C (2007) Diversity of rDNA in Chilostomella: molecular differentiation patterns and putative hermit types. Mar Micropaleontol 62:75–90

    Article  Google Scholar 

  • Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 59:307–321

    Article  CAS  Google Scholar 

  • Hallock PM, Cottey TL, Forward LB, Halas J (1986) Population biology and sediment production of Archaias angulatus (foraminiferida) in largo sound Florida. J Foramin Res 16:1–8

    Article  Google Scholar 

  • Hasegawa S (1979) Foraminifera of the Himi group, Hokuriku Province, Central Japan. The science reports of the Tohoku university, 2nd series (Geology), vol 49, pp 89–163

    Google Scholar 

  • Higuchi Y (1954) Fossil foraminifera from the Miyata formation, Miura Peninsula, Kanagawa Prefecture. J Geol Soc Jpn 60:138–145 (in Japanese with English abstract)

    Article  Google Scholar 

  • Hirooka K (1988) Neogene paleoposition of the Japanese Islands inferred from paleomagnetic studies. In: Tsuchi R, Chiji M, Takayanagi Y (eds) IGCP project 246-Pacific Neogene events in time and space: Osaka museum of natural history, special publication. Osaka Museum of Natural History, Osaka, pp 3–16 (in Japanese, with English abstract)

    Google Scholar 

  • Holzmann M (2000) Species concept in foraminifera: Ammonia as a case study. Micropaleontology 46(Suppl 1):21–37

    Google Scholar 

  • Holzmann M, Pawlowski J (1996) Preservation of foraminifera for DNA extraction and PCR amplification. J Foramin Res 26:264–267

    Article  Google Scholar 

  • Holzmann M, Pawlowski J (2000) Taxonomic relationships in the genus Ammonia (Foraminifera) based on ribosomal DNA sequences. J Micropaleontol 19:85–95

    Article  Google Scholar 

  • Ishitani Y, Ishikawa SA, Inagaki Y, Tsuchiya M, Takahashi K, Takishita K (2011) Multigene phylogenetic analyses including diverse radiolarian species support the “Retaria” hypothesis: the sister relationship of Radiolaria and Foraminifera. Mar Micropaleontol 81:32–42

    Article  Google Scholar 

  • Ishitani Y, Kamikawa R, Yabuki A, Tsuchiya M, Inagaki Y, Takishita K (2012) Evolution of elongation factor-like (EFL) protein in rhizaria is revised by radiolarian EFL gene sequences. J Eukaryot Microbiol 59:367–373

    Article  CAS  Google Scholar 

  • Kaizuka S (1984) Landforms in and around the South Fossa Magna and their tectonic processes of growth. Quaternary Res 23:55–70 (in Japanese, with English abstract)

    Article  Google Scholar 

  • Kamikawa R, Inagaki Y, Sako Y (2008) Direct phylogenetic evidence for lateral transfer of elongation factor-like gene. Proc Natl Acad Sci USA 105:6965–6969

    Article  CAS  Google Scholar 

  • Kanesaki H (1987) Geographic distributions of rocky shore foraminifera adjacent to the Japanese Islands. Undergraduate thesis, Institute of Geosciences, Shizuoka University, P 86 (in Japanese with English abstract)

    Google Scholar 

  • Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120

    Article  CAS  Google Scholar 

  • Kitazato H (1984) Microhabitats of benthic foraminifera and their application to fossil assemblages. In: Oertli HJ (ed) Benthos ’83: 2nd international symposium on benthic foraminifera, France, pp 339–344

    Google Scholar 

  • Kitazato H (1988) Ecology of benthic foraminifera in the tidal zone of a rocky shore. Benthos ’86, pp 815–825

    Google Scholar 

  • Kitazato H (1992) Pseudopodia of benthic foraminifera and their relationships to the test morphology. In: Takayanagi Y, Saito T (eds) Studies in benthic foraminifera. Tohoku University Press, Tokyo, pp 103–108

    Google Scholar 

  • Kitazato H (1994) Foraminiferal microhabitats in four marine environments around Japan. Mar Micropaleontol 24:29–41

    Article  Google Scholar 

  • Kitazato H (1997) Paleogeographic changes in central Honshu, Japan, during the late Cenozoic in relation to the collision of the Izu-Ogasawara Arc with the Honshu Arc. Island Arc 6:144–157

    Article  Google Scholar 

  • Kitazato H, Tsuchiya M, Takahara K (2000) Recognition of breeding populations in foraminifera: an example using the genus Glabratella. Paleontol Res 4:1–15

    Google Scholar 

  • Lee JJ, Faber WW Jr, Anderson OR, Pawlowski J (1991) Life–cycles of foraminifera. In: Lee JJ, Anderson OR (eds) Biology of foraminifera. Academic, London, pp 285–334

    Google Scholar 

  • Matoba Y, Tomizawa A, Maruyama T, Shiraishi T, Aita Y, Okamoto K (1990) Neogene and quaternary sedimentary sequences in the Oga Peninsula. Benthos ’90: the 4th international symposium on benthic foraminifera, Sendai, Japan

    Google Scholar 

  • Matsushima Y (1984) Shallow marine molluscan assemblages of postglacial period in the Japanese islands: its historical and geographical changes induced by the environmental changes. Bull Kanagawa Pref Mus 15:37–109 (in Japanese, with English abstract)

    Google Scholar 

  • Miya M, Nishida M (1997) Speciation in the open ocean. Nature 389(803):804

    Google Scholar 

  • Moodley L, Hess C (1992) Tolerance of infaunal benthic foraminifera for low and high oxygen concentrations. Biol Bull 183:94–98

    Article  Google Scholar 

  • Murray JW (2006) Ecology and applications of benthic foraminifera. Cambridge University Press, Cambridge, 426 pp

    Book  Google Scholar 

  • Myers EH (1938) The present state of our knowledge concerning the life cycle of the foraminifera. Proc Natl Acad Sci USA 24:10–17

    Article  CAS  Google Scholar 

  • Myers EH (1940) Observations on the origin and fate of flagellated gametes in multiple tests of Discorbis (Foraminifera). J Mar Biol Assoc UK 24:201–226

    Article  Google Scholar 

  • Nakamura K, Shimazaki K, Yonekura N (1984) Subduction, bending and eduction: present and Quaternary tectonics of the northern border of the Philippine Sea plate. Bull Soc GĂ©ol France XXVI:221–243

    Google Scholar 

  • Nemoto N, Yoshimoto N (2001) Foraminiferal fossils from the Pleistocene Hamada formation in the Chikagawa area, Eastern Shimokita Peninsula, Northeast Japan. Fossils (Palaeontol Soc Jpn) 69:1–24 (in Japanese, with English abstract)

    Google Scholar 

  • Nomura R (1992) Miocene benthic foraminifers at sites 794, 795, and 797. Proc Ocean Drill Program Sci Results 127/128:493–540

    Google Scholar 

  • Oba T, Kato M, Kitazato H, Koizumi I, Omura A, Sakai T, Takayama T (1991) Paleoenvironmental changes in the Japan Sea during the last 85,000 years. Paleoceanography 6:499–518

    Article  Google Scholar 

  • Ogasawara K (1994) Neogene paleogeography and marine climate of the Japanese Islands based on shallow marine molluscs. Palaeogeogr Palaeoclimatol Palaeoecol 108:335–351

    Article  Google Scholar 

  • Otofuji Y, Matsuda T (1984) Timing of rotational motion of southwest Japan inferred from paleomagnetism. Earth Planet Sci Lett 70:373–382

    Article  Google Scholar 

  • Pawlowski J (2000) Introduction to the molecular systematics of foraminifera. Micropaleontology 46(suppl 1):1–12

    Google Scholar 

  • Pawlowski J, Holzmann M (2008) Diversity and geographic distribution of benthic foraminifera: a molecular perspective. Biodivers Conserv 17:317–328

    Article  Google Scholar 

  • Pawlowski J, Bolivar I, Fahrni JF, Cavalier-Smith T, Gouy M (1996) Early origin of Foraminifera suggested by SSU rRNA gene sequences. Mol Biol Evol 13:445–450

    Article  CAS  Google Scholar 

  • Pawlowski J, Fahrni J, Lecroq B, Longet D, Cornelius N, Excoffier L, Cedhagen T, Gooday AJ (2007) Bipolar gene flow in deep-sea benthic foraminifera. Mol Ecol 16:4089–4096

    Article  CAS  Google Scholar 

  • Pillet L, Fontaine D, Pawlowski J (2012) Intra-genomic ribosomal RNA polymorphism and morphological variation in Elphidium macellum suggests inter-specific hybridization in foraminifera. PLoS ONE 7:e32373. doi:10.1371/journal.pone.0032373

    Article  CAS  Google Scholar 

  • Rambaut A (1996) Se-Al version 2.0a11: sequence alignment editor. http://evolve.zoo.ox.ac.uk/

  • Ross CA (1972) Biology and ecology of Marginopora vertebralis (Foraminiferida), Great Barrier Reef. J Protozool 19:181–192

    Article  Google Scholar 

  • Röttger R (1974) Larger foraminifer: reproduction and early stages of development in Heterostegina depressa. Mar Biol 26:5–12

    Article  Google Scholar 

  • Röttger R, KrĂĽge R, de Rijk S (1990) Trimorphism in foraminifera (protozoa)-verification of an old hypothesis. Euro J Protist 25:226–228

    Article  Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    CAS  Google Scholar 

  • Sakaguchi M, Takishita K, Matsumoto T, Hashimoto T, Inagaki Y (2009) Tracing back EFL gene evolution in the cryptomonads-haptophytes assemblage: separate origins of EFL genes in haptophytes, photosynthetic cryptomonads, and goniomonads. Gene 441:126–131

    Article  CAS  Google Scholar 

  • Schweizer M, Pawlowski J, Duijnstee IAP, Kouwenhoven TJ, van der Zwaan GJ (2005) Molecular phylogeny of the foraminiferal genus Uvigerina based on ribosomal DNA sequences. Mar Micropaleontol 57:51–67

    Article  Google Scholar 

  • Spindler M (1980) The pelagic gulfweed Sargassum natans as a habitat for the benthic foraminifera Planorbulina acervalis and Rosalina globularis. Neues Jahrbuch Geol Paläont Mh 110:569–580

    Google Scholar 

  • Takahara K (1989) Morphological analysis by plastogamy experiment on the benthic foraminifera, Glabratella. Undergraduate thesis, Institute of Geosciences, Shizuoka University, p 61 (in Japanese with English abstract)

    Google Scholar 

  • Takishita K, Inagaki Y, Tsuchiya M, Sakaguchi M, Maruyama T (2005) A close relationship between Cerocozoa and foraminifera supported by phylogenetic analysis based on combined amino acid sequences of three cytoskeletal proteins (actin, α-tubulin, and β-tubulin). Gene 362:153–160

    Article  CAS  Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739

    Article  CAS  Google Scholar 

  • Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680

    Article  CAS  Google Scholar 

  • Toyofuku T, Kitazato H (2005) Micromapping of Mg/Ca values in cultured specimens of the high-magnesium benthic foraminifera. Geochem Geophys Geosyst 6:Q11P05. doi:10.1029/2005GC000961

    Article  Google Scholar 

  • Toyofuku T, Kitazato H, Kawahata H, Tsuchiya M, Nohara M (2000) Evaluation of Mg/Ca thermometry in foraminifera: comparison of experimental results and measurements in nature. Paleoceanography 15:456–464

    Article  Google Scholar 

  • Tsuchiya M, Aizawa M, Suzuki-Kanesaki H, Kitazato H (1994) Life history of Glabratella opercularis (d’Orbigny): observations and experiments. PaleoBios 16:62

    Google Scholar 

  • Tsuchiya M, Kitazato H, Pawlowski J (2000) Phylogenetic relationships among species of Glabratellidae (Foraminifera) inferred from ribosomal DNA sequences: comparison with morphological and reproductive data. Micropaleontology 46(suppl 1):13–20

    Google Scholar 

  • Tsuchiya M, Kitazato H, Pawlowski J (2003) Analysis of internal transcribed spacer of ribosomal DNA reveals cryptic speciation in Planoglabratella opercularis. J Foramin Res 33:285–293

    Article  Google Scholar 

  • Tsuchiya M, Tazume M, Kitazato H (2008) Molecular characterization of the non-costate morphotypes of buliminid foraminifers based on internal transcribed region of ribosomal DNA (ITS rDNA) sequence data. Mar Micropaleontol 69:212–224

    Article  Google Scholar 

  • Tsuchiya M, Grimm GW, Heinz P, Stögerer K, Ertan KT, Collen J, BrĂĽchert V, Hemleben C, Hemleben V, Kitazato H (2009) Ribosomal DNA shows extremely low genetic divergence in a world-wide distributed, but disjunct and highly adapted marine protozoan (Virgulinella fragilis, Foraminiferida). Mar Micropaleontol 70:8–19

    Article  Google Scholar 

  • UjiiĂ© Y, Asami T, de Garidel-Thoron T, Liu H, Ishitani Y, de Vargas C (2012) Longitudinal differentiation among pelagic populations in a planktic foraminifer. Ecol Evol. doi:10.1002/ece3.28610.1002/ece3.286

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Tsuchiya, M., Takahara, K., Aizawa, M., Suzuki-Kanesaki, H., Toyofuku, T., Kitazato, H. (2014). How Has Foraminiferal Genetic Diversity Developed? A Case Study of Planoglabratella opercularis and the Species Concept Inferred from Its Ecology, Distribution, Genetics, and Breeding Behavior. In: Kitazato, H., M. Bernhard, J. (eds) Approaches to Study Living Foraminifera. Environmental Science and Engineering(). Springer, Tokyo. https://doi.org/10.1007/978-4-431-54388-6_9

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