Abstract
The genus Operculina, a large symbiont-bearing benthic foraminifer, is characterized by high morphological variability showing thick involute to intermediate semi-involute to flat evolute tests. Different morphotypes are either considered as ecophenotypes or distinct species. In order to test the hypothesis of ecophenotypes versus different species, a single cell high throughput sequencing approach was applied to assess the interspecific diversity of Operculina. This results in two groups of ribotypes, one corresponding to Operculina ammonoides/Operculina discoidalis, the other containing Operculina complanata/Operculina elegans. These groups can also be separated morphologically. Therefore, O. complanata and O. elegans represent a single species and the latter can be regarded as a junior synonym of O. complanata. Operculina ammonoides and O. discoidalis also form a single species, which makes the latter a junior synonym of O. ammonoides. Because generic differences in Operculina species are manifested in morphology and molecular genetics, the genus Neoassilina with the designated species Neoassilina ammonoides is installed. Additional analysis of ribosomal SSU rDNA data of eight recent nummulitid genera confirms the obtained high troughput sequencing results and further shows that Palaeonummulites venosus builds a clade with O. complanata that branches at the base of other Nummulitidae containing Planostegina, Planoperculina, Cycloclypeus, Heterostegina, Operculinella and Neoassilina.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
References Cited
Banner, F. T., Hodgkinson, R. L., 1991. A Revision of the Foraminiferal Subfamily Heterostegininae. Revista Espanola de Micropaleontologica, 13(2): 101–140
Beavington-Penney, S. J., Racey, A., 2004. Ecology of Extant Nummulitids and other Larger Benthic Foraminifera: Applications in Palaeoenvironmental Analysis. Earth-Science Reviews, 67(3/4): 219–265. https://doi.org/10.1016/j.earscirev.2004.02.005
Callahan, B. J., McMurdie, P. J., Rosen, M. J., et al., 2016. DADA2: High-Resolution Sample Inference from Illumina Amplicon Data. Nature Methods, 13(7): 581–583. https://doi.org/10.1038/nmeth.3869
Cavalier-Smith, T., 2002. The Phagotrophic Origin of Eukaryotes and Phylogenetic Classification of Protozoa. International Journal of Systematic and Evolutionary Microbiology, 52(2): 297–354. https://doi.org/10.1099/00207713-52-2-297
Cushman, J. A., 1914. A Monograph of the Forminifera of the North Pacific Ocean Pt. 4: Chilostomellidae, Globigerinidae, Nummulitidae. Bulletin of the United States National Museum, 71(4): 1–46. https://doi.org/10.5479/si.03629236.71.4
d’Orbigny, A., 1839. Foraminifères, in de la Sagra R., Histoire Physique, Politique et Naturelle de l’ile de Cuba. A. Bertrand, Paris. 1–224
d’Orbigny, A., 1826. Tableau Méthodique de la Classe des Céphalopodes. 3ème ordre-Foraminifères. Annales du Muséum d’Histoire Naturelles, Paris. 7: 1–275
de Blainville, H. M. D., Prêtre, J. G., Turpin, P. J. F., 1827. Manuel de Malacologie et de Conchyliologie. F. G. Levrault, Paris. 1–644. https://doi.org/10.5962/bhl.title.11582
Defrance, J. L. M., 1822. Dictionnaire des Sciences Naturelles. F. G. Levrault, Paris, Strasssbourg. 25: 453
Dufresne, Y., Lejzerowicz, F., Perret-Gentil, L. A., et al., 2019. SLIM: A Flexible Web Application for the Reproducible Processing of Environmental DNA Metabarcoding Data. BMC Bioinformatics, 20(1): 88. https://doi.org/10.1186/s12859-019-2663-2
Esling, P., Lejzerowicz, F., Pawlowski, J., 2015. Accurate Multiplexing and Filtering for High-Throughput Amplicon-Sequencing. Nucleic Acids Research, 43(5): 2513–2524. https://doi.org/10.1093/nar/gkv107
Fornasini, C., 1903. Illustrazione di Specie Orbignyane di «Nummulitidae» Istituite nel 1826. Bollettino della Società Geologica Italiana, 22: 395–397
Gouy, M., Guindon, S., Gascuel, O., 2010. SeaView Version 4: A Multiplatform Graphical User Interface for Sequence Alignment and Phylogenetic Tree Building. Molecular Biology and Evolution, 27(2): 221–224. https://doi.org/10.1093/molbev/msp259
Gronovius, L. T., 1781. Zoophylacii Gronoviani. Haak et Cie, 3: 241–380
Guindon, S., Dufayard, J. F., Lefort, V., et al., 2010. New Algorithms and Methods to Estimate Maximum-Likelihood Phylogenies: Assessing the Performance of PhyML 3.0. Systematic Biology, 59(3): 307–321. https://doi.org/10.1093/sysbio/syq010
Hammer, Ø., 2021. PAST. Paleontological Statistics, Version 4.06. [2021-8-6]. http://priede.bf.lu.lv/ftp/pub/TIS/datu_analiize/PAST/4.xx/past-4.06-manual.pdf
Hohenegger, J., 2000. Coenoclines of Larger Foraminifera. Micropaleontology, 46(Suppl. 1): 127–151
Hohenegger, J., 2004. Depth Coenoclines and Environmental Considerations of Western Pacific Larger Foraminifera. Journal of Foraminiferal Research, 34(1): 9–33. https://doi.org/10.2113/0340009
Hohenegger, J., 2006. Morphocoenoclines, Character Combination, and Environmental Gradients: A Case Study Using Symbiont-Bearing Benthic Foraminifera. Paleobiology, 32(1): 70–99. https://doi.org/10.1666/0094-8373(2006)032[0070:mccaeg]2.0.co;2
Hohenegger, J., 2011. Growth-Invariant Meristic Characters Tools to Reveal Phylogenetic Relationships in Nummulitidae (Foraminifera). Turkish Journal of Earth Sciences, 20: 655–681
Hohenegger, J., 2018. Foraminiferal Growth and Test Development. Earth-Science Reviews, 185: 140–162. https://doi.org/10.1016/j.earscirev.2018.06.001
Hohenegger, J., Yordanova, H. A., 2000. Remarks on West Pacific Nummulitidae (Foraminifera). Journal of Foraminiferal Research, 30(1): 3–28. https://doi.org/10.2113/0300003
Holzmann, M., Pawlowski, J., 2017. An Updated Classification of Rotaliid Foraminifera Based on Ribosomal DNA Phylogeny. Marine Micropaleontology, 132: 18–34. https://doi.org/10.1016/j.marmicro.2017.04.002
Holzmann, M., Berney, C., Hohenegger, J., 2006. Molecular Identification of Diatom Endosymbionts in Nummulitid Foraminifera. Symbiosis, 42: 93–101
Holzmann, M., Hohenegger, J., Pawlowski, J., 2003. Molecular Data Reveal Parallel Evolution in Nummulitid Foraminifera. Journal of Foraminiferal Research, 33(4): 277–284. https://doi.org/10.2113/0330277
Hottinger, L., 1977. Foraminifères Operculiniformes. Mémoires du Muséum National d’Histoire Naturelle, Paris, Série C, 40: 1–159
Hottinger, L., 2006a. The Depth-Depending Ornamentation of some Lamellar-Perforate Foraminifera. Symbiosis, 42(3): 141–151
Hottinger, L., 2006b. Illustrated Glossary of Terms Used in Foraminiferal Research. Carnets de Géologie, Memoires, (2): 1–43. https://doi.org/10.4267/2042/5832
Langer, M., Hottinger, L., 2000. Biogeography of Selected “Larger” Foraminifera. Micropaleontology, 46(Suppl. 1): 105–126
Lee, J. J., McEnery, M. E., Kuile, B. T., et al., 1989. Identification and Distribution of Endosymbiotic Diatoms in Larger Foraminifera. Micropaleontology, 35(4): 353–366. https://doi.org/10.2307/1485677
Lefort, V., Longueville, J. E., Gascuel, O., 2017. SMS: Smart Model Selection in PhyML. Molecular Biology and Evolution, 34(9): 2422–2424. https://doi.org/10.1093/molbev/msx149
Loeblich, A. R. Jr., Tappan, H., 1988. Foraminiferal Genera and Their Classification. Van Nostrand Reinhold, New York
Mukhopadhyay, S. K., 2016. Neonummulites gen. nov., Representing a Phylogenetic Link between Evolute and Involute Nummulitines. Micropaleontology, 62(5): 365–383. https://doi.org/10.47894/mpal.62-5.03
Oron, S., Abramovich, S., Almogi-Labin, A., et al., 2018. Depth Related Adaptations in Symbiont Bearing Benthic Foraminifera: New Insights from a Field Experiment on Operculina Ammonoides. Scientific Reports, 8: 9560. https://doi.org/10.1038/s41598-018-27838-8
Papp, A., Küpper, K., 1954. The Genus Heterostegina in the Upper Tertiary of Europe. Contributions from the Cushman Foundation for Foraminiferal Research, 5(3): 108–127
Pawlowski, J., Holzmann, M., 2014. A Plea for DNA Barcoding of Foraminifera. Journal of Foraminiferal Research, 44(1): 62–67. https://doi.org/10.2113/gsjfr.44.1.62
Pawlowski, J., Lejzerowicz, F., Esling, P., 2014. Next-Generation Environmental Diversity Surveys of Foraminifera: Preparing the Future. Biological Bulletin, 227(2): 93–106. https://doi.org/10.1086/bblv227n2p93
Pawlowski, J., Holzmann, M., Tyszka, J., 2013. New Supraordinal Classification of Foraminifera: Molecules Meet Morphology. Marine Micropaleontology, 100: 1–10. https://doi.org/10.1016/j.marmicro.2013.04.002
Pecheux, M. J. F., 1995. Ecomorphology of a Recent Largeforaminifer, Operculina Ammonoides. Geobios, 28(5): 529–566. https://doi.org/10.1016/s0016-6995(95)80209-6
Reiss, Z., Hottinger, L., 1984. The Gulf of Aqaba. Ecological Micropaleontology. Springer Verlag, Berlin. 354
Schaub, H., 1981. Nummulites et Assilines de la Tethys Paléogène. Taxonomie, Phylogenèse et Biostratigraphie. Mémoires de la Société Paléontologique Suisse/Abhandlungen der Schweizerischen Paläontologischen Gesellschaft. 104: 1–236; 105: pl. 1–48; 106: pl. 49–97
Torres-Silva, A. I., Eder, W., Hohenegger, J., et al., 2019. Morphometric Analysis of Eocene Nummulitids in Western and Central Cuba: Taxonomy, Biostratigraphy and Evolutionary Trends. Journal of Systematic Palaeontology, 17(7): 557–595. https://doi.org/10.1080/14772019.2018.1446462
Yordanova, E. K., Hohenegger, J., 2004. Morphoclines of Living Operculinid Foraminifera Based on Quantitative Characters. Micropaleontology, 50(2): 149–177.https://doi.org/10.1661/0026-2803(2004)050[0149:molofb]2.0.co;2
Acknowledgments
The current study was supported by Israel Science Foundation (No. 1267/21) to Sigal Abramovich and the Swiss National Science Foundation (No. 31003A_179125) to Jan Pawlowski. Open Access funding provided by University of Geneva. The final publication is available at Springer via https://doi.org/10.1007/s12583-021-1595-8.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.
About this article
Cite this article
Holzmann, M., Hohenegger, J., Apothéloz-Perret-Gentil, L. et al. Operculina and Neoassilina: A Revision of Recent Nummulitid Genera Based on Molecular and Morphological Data Reveals a New Genus. J. Earth Sci. 33, 1411–1424 (2022). https://doi.org/10.1007/s12583-021-1595-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12583-021-1595-8