Citation: | Marcelle K. BouDagher-Fadel. Evolution, Extinction, Homology and Homoplasy of the Larger Benthic Foraminifera from the Carboniferous to the Present Day, as Exemplified by Planispiral-Fusiform and Discoidal Forms. Journal of Earth Science, 2022, 33(6): 1348-1361. doi: 10.1007/s12583-021-1596-7 |
Examples of evolution, extinction and homoplasy of the larger benthic foraminifera (LBF) occur throughout their history. Since the Carboniferous, LBF have thrived in carbonate-rich tropical and subtropical shallow-marine shelf environments. Their high abundance and diversity are due primarily to their extraordinary ability to inhabit a range of ecological niches and by hosting a variety of symbionts. Attaining relatively large, centimetre-scale sizes, made some forms very specialized and vulnerable to rapid ecological changes. For this reason, some LBF have shown a tendency to suffer periodically during major extinctions, especially when environmental conditions have changed rapidly and/or substantially. This, however, makes them valuable biostratigraphic microfossils and, in addition, gives invaluable insight into the spatial and temporal process of biological evolution, such as convergent/homoplasy and homology/iterative evolution. Here the evolutionary behavior of two important morphological types that occurred throughout the history of the LBF are discussed, namely the planispiral-fusiform test as typified by the fusulinids in the Late Paleozoic and the alveolinids in the Mid-Cretaceous and Neogene, and the three-layered discoid lenticular test as characterized by the orbitoids in the Mid- to Late Cretaceous, the orthophragminids in the Paleogene, and lepidocyclinids in the Oligocene to Quaternary. Understanding the propensity of these forms to convergent and iterative evolution, with the repeated re-occurrence of certain morphological features, is essential in understanding and constructing their phylogenetic relationships more generally within the main groups of the LBF. The insights gained from the history of these LBF have wider implications, and provide a more general understanding of the impacts of climate and ecological changes as driving forces for biological evolution.
Ali, N., Özcan, E., Yücel, A. O., et al., 2018. Bartonian Orthophragminids with New Endemic Species from the Pirkoh and Drazinda Formations in the Sulaiman Range, Indus Basin, Pakistan. Geodinamica Acta, 30(1): 31–62. https://doi.org/10.1080/09853111.2017.1419676 |
Beavington-Penney, S. J., Racey, A., 2004. Ecology of Extant Nummulitids and other Larger Benthic Foraminifera: Applications in Palaeoenviron-Mental Analysis. Earth-Science Reviews, 67(3/4): 219–265. https://doi.org/10.1016/j.earscirev.2004.02.005 |
Benedetti, A., Briguglio, A., 2012. Risananeiza crassaparies n. sp. from the Upper Chattian of Porto Badisco (Southern Apulia, Italy). Bollettino Della Societa Paleontologica Italiana, 51(3): 167–176. https://doi.org/10.4435/bspi.2012.19 |
Benedetti, A., Di Carlo, M., Pignatti J., 2010. Embryo Size Variation in Larger Foraminiferal Lineages: Stratigraphy versus Paleoecology in Nephrolepidina Praemarginata (R. Douvillé, 1908) from the Majella Mt. (Central Appennines). Journal of Mediterranean Earth Sciences, 2: 19–29. https://doi.org/10.3304/jmes.2010.003 |
Boersma, A., 1978. Foraminifera. In: Haq, B. U., Boersma, A., eds., Introduction to Marine Micropaleontology in Foraminifera. Elsevier, New York. 19–78 |
Bosellini, F. R., Papazzoni, C. A., 2003. Palaeoecological Significance of Coral-Encrusting Foraminiferan Associations: A Case-Study from the Upper Eocene of Northern Italy. Acta Palaeontologica Polonica, 48(2): 279–292 |
BouDagher-Fadel, M. K., 2008. The Cenozoic Larger Benthic Foraminifera: The Palaeogene. In: BouDagher-Fadel, M. K., ed., Developments in Palaeontology and Stratigraphy. Elsevier. 297–545. https://doi.org/10.1016/s0920-5446(08)00006-x |
BouDagher-Fadel, M. K., 2015. Biostratigraphic and Geological Significance of Planktonic Foraminifera (Updated 2nd Edition). UCL Press, London. 306 |
BouDagher-Fadel, M. K., 2018a. Evolution and Geological Significance of Larger Benthic Foraminifera. UCL Press, London. 704 |
BouDagher-Fadel, M. K., 2018b. Revised Diagnostic First and Last Occurrences of Mesozoic and Cenozoic Planktonic Foraminifera. UCL Office of the Vice-Provost Research, Professional Papers Series, London. 1–5 |
BouDagher-Fadel, M. K., Lord, A. R., 2000. The Evolution of Lepidocyclina (L.) isolepidinoides, L. (Nephrolepidina) nephrolepidinoides, L. (N.) brouweri in the Late Oligocene–Miocene of the Far East. Journal of Foraminiferal Research, 30(1): 71–76. https://doi.org/10.2113/0300071 |
BouDagher-Fadel, M. K., Price, G. D., 2021. The Geographic, Environmen-tal and Phylogenetic Evolution of the Alveolinoidea from the Cretaceous to the Present Day. UCL Open: Environment, 2: 1–34. https://doi.org/10.14324/111.444/ucloe.000015 |
BouDagher-Fadel, M. K., Price, G. D., 2017. The Paleogeographic Evolution of the Orthophragminids of the Paleogene. Journal of Foraminiferal Research, 47(4): 337–357. https://doi.org/10.2113/gsjfr.47.4.337 |
BouDagher-Fadel, M. K., Price, G. D., 2014. The Phylogenetic and Palaeogeographic Evolution of the Nummulitoid Larger Benthic Forami-nifera. Micropaleontology, 60(6): 483–508. https://doi.org/10.47894/mpal.60.6.01 |
BouDagher-Fadel, M. K., Price, G. D., 2013. The Phylogenetic and Palaeogeographic Evolution of the Miogypsinid Larger Benthic Foraminifera. Journal of the Geological Society, 170(1): 185–208. https://doi.org/10.1144/jgs2011-149 |
BouDagher-Fadel, M. K., Price, G. D., 2010a. Evolution and Paleogeographic Distribution of the Lepidocyclinids. Journal of Foraminiferal Research, 40(1): 79–108. https://doi.org/10.2113/gsjfr.40.1.79 |
BouDagher-Fadel, M. K., Price, G. D, 2010b. American Miogypsinidae: An Analysis of Their Phylogeny and Biostratigraphy. Micropaleontology, 56(6): 567–586. https://doi.org/10.47894/mpal.56.6.04 |
Brandano, M., Tomassetti, L., Bosellini, F., et al., 2010. Depositional Model and Paleodepth Reconstruction of a Coral-Rich, Mixed Siliciclastic-Carbonate System: The Burdigalian of Capo Testa (Northern Sardinia, Italy). Facies, 56(3): 433–444. https://doi.org/10.1007/s10347-009-0209-1 |
Briguglio, A., Kinoshita, S., Wolfgring, E., et al., 2016. Morphological Variations in Cycloclypeus carpenteri: Multiple Embryos and Multiple Equatorial Layers. Palaeontologia Electronica, 19(1.3A): 1–22. https://doi.org/10.26879/595 |
Chaproniere, G. C. H., 1975. Palaeoecology of Oligo–Miocene Larger Fora-miniferida, Australia. Alcheringa, 1(1): 37–58. https://doi.org/10.1080/03115517508619479 |
Coletti, G., Stainbank, S., Fabbrini, A., et al., 2018. Biostratigraphy of Large Benthic Foraminifera from Hole U1468A (Maldives): A CT-Scan Taxonomic Approach. Swiss Journal of Geosciences, 111(3): 523–536. https://doi.org/10.1007/s00015-018-0306-7 |
Conway Morris, S., 2003. Life's Solution: Inevitable Humans in a Lonely Universe. Cambridge University Press, Cambridge. 464 |
Coxall, H. K., Wilson, P. A., Pearson, P. N., et al., 2007. Iterative Evolution of Digitate Planktonic Foraminifera. Paleobiology, 33(4): 495–516. https://doi.org/10.1666/06034.1 |
Davydov, V. I., Arefifard, S., 2007. Permian Fusulinid Fauna of Peri-Gondwanan Affinity from the Kalmard Region, East-Central Iran and Its Significance for Tectonics and Paleogeography. Palaeontologia Electronica, 40(2.10A): 1–40 |
Drooger, C. W., Raju, D. S. N., 1973. Protoconch Diameter in the Miogypsinidae. Proceedings of the Koninklijke Nederlandse Akadamie Wetenschappen, Amsterdam, Ser. B, 76: 206–216 |
Eames, F. E., Banner, F. T., Blow, W. H., et al., 1962. Fundamentals of Mid-Tertiary Stratigraphical Correlation. Cambridge University Press, Cambridge. 163 |
Ferrandez-Canadell, C., Serra-Kiel, J., 1992. Morphostructure and Paleobiology of Discocyclina Guembel, 1870. Journal of Foraminiferal Research, 22(2): 147–165. https://doi.org/10.2113/gsjfr.22.2.147 |
Hall, B. K., 1999. Evolutionary Developmental Biology. Kluwer Academic Publishers. 491 |
Hallock, P., 1985. Why are Larger Foraminifera Large? Paleobiology, 11(2): 195–208. https://doi.org/10.1017/s0094837300011507 |
Hallock, P., 1987. Fluctuations in the Trophic Resource Continuum: A Factor in Global Diversity Cycles? Paleoceanography, 2(5): 457–471. https://doi.org/10.1029/pa002i005p00457 |
Hallock, P., Seddighi, M., 2022. Why did some Larger Benthic Foraminifera Become so Large and Flat? Sedimentology, 69(1): 74–87. https://doi.org/10.1111/sed.12837 |
Haynes, J. R., 1981. Foraminifera. MacMillan, London. 433 |
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., Yordanova, E., Nakano, Y., et al., 1999. Habitats of Larger Foraminifera on the Upper Reef Slope of Sesoko Island, Okinawa, Japan. Marine Micropaleontology, 36(2/3): 109–168. https://doi.org/10.1016/s0377-8398(98)00030-9 |
Hottinger, L., 2006. Illustrated Glossary of Terms Used in Foraminiferal Research. Carnets de Géologie (Notebooks on Geology), Memoir 2006/02. https://doi.org/10.4267/2042/5832 |
Hottinger, L., 1997. Shallow Benthic Foraminiferal Assemblages as Signals for Depth of Their Deposition and Their Limitations. Bulletin de la Societe Geologique de France, 168(4): 491–505 |
Hottinger, L., Drobne, K., Caus, E., 1989. Late Cretaceous, Larger, Complex Miliolids (Foraminifera) Endemic in the Pyrenean Faunal Province. Facies, 21(1): 99–133. https://doi.org/10.1007/bf02536833 |
Hottinger, L. C., 2000. Functional Morphology of Benthic Foraminiferal Shells, Envelopes of Cells beyond Measure. Micropaleontology, 46(Suppl. 1): 57–86 |
Keller, G., Abramovich, S., 2009. Lilliput Effect in Late Maastrichtian Planktic Foraminifera: Response to Environmental Stress. Palaeogeography, Palaeoclimatology, Palaeoecology, 284(1/2): 47–62. https://doi.org/10.1016/j.palaeo.2009.08.029 |
Laugié, M., Donnadieu, Y., Ladant, J. B., et al., 2020. Stripping back the Modern to Reveal the Cenomanian-Turonian Climate and Temperature Gradient underneath. Climate of the Past, 16(3): 953–971. https://doi.org/10.5194/cp-16-953-2020 |
Leppig, U., 1992. Functional Anatomy of Fusulinids (Foraminifera): Significance of the Polar Torsion Illustrated in Triticites and Schwagerina (Schwagerinidae). Palaontologische Zeitschrift, 66(1): 39–50. https://doi.org/10.1007/bf02989476 |
Less, G., Kovács, L. Ó., 1996. Age-Estimates by European Paleogene Orthophragminae Using Numerical Evolutionary Correlation. Geobios, 29(3): 261–285. https://doi.org/10.1016/s0016-6995(96)80029-5 |
Less, G., Özcan, E., Báldi-Beke, M., et al., 2007. Thanetian and Early Ypresian Orthophragmines (Foraminifera, Discocyclinidae and Orbitoclypeidae) from the Central Western Tethys (Turkey, Italy and Bulgaria) and Their Revised Taxonomy and Biostratigraphy. Rivista Italiana di Paleontogia e Stratigrafia, 113: 415–448 |
Less, G., 1998. The Zonation of the Mediterranean Upper Paleocene and Eocene by Orthopfragminae. In: Hottinger, L., Drobne, K., eds., Paleogene Shallow Benthos of the Tethys, Slovenian Academy of Sciences and Arts, Ljubljana. 2: 21–43 |
Leven, E. Y., 2003. Diversity Dynamics of Fusulinid Genera and Main Stages of Their Evolution. Stratigraphy and Geological Correlation, 11(3): 220–230 |
Lipps, J. H., Severin, K. P., 1986. Alveolinella Quoyi, a Living Fusiform Foraminifera, at Motupore Island, Papua New Guinea. Science in New Guinea, 11: 126–137 |
Lunt, P., Luan, X. W., 2022. East Tethyan Cenozoic Larger Foraminifera: Taxonomic Questions, Apparent Radiation and Abrupt Extinctions. Journal of Earth Science, 33(6): 1378–1399. https://doi.org/10.1007/s12583-022-1614-4 |
Mateu-Vicens, G., Hallock, P., Brandano, M., et al., 2009. Test-Shape Variability of Amphistegina d'Orbigny, 1826 as a Paleobathymetric Proxy: Application to Two Miocene Examples. Geologic Problem Solving with Microfossils. SEPM Special Publications, 93: 67–82. https://doi.org/10.2110/sepmsp.093.067 |
Narayan, G. R., Reymond, C. E., Stuhr, M., et al., 2021. Response of Large Benthic Foraminifera to Climate and Local Changes: Implications for Future Carbonate Production. Sedimentology, 69(1): 121–161. https://doi.org/10.1111/sed.12858 |
Özcan, E., Less, G., Báldi-Beke, M., et al., 2006. Biometric Analysis of Middle and Upper Eocene Discocyclinidae and Orbitoclypeidae (Foraminifera) from Turkey and Updated Orthophragmine Zonation in the Western Tethys: Micropaleontology, 52: 485–520 doi: 10.2113/gsmicropal.52.6.485 |
Pomar, L., Hallock, P., 2008. Carbonate Factories: A Conundrum in Sedimentary Geology. Earth-Science Reviews, 87(3/4): 134–169. https://doi.org/10.1016/j.earscirev.2007.12.002 |
Rauser-Chernousova, D. M., Bensh, F. R., Vdovenko, M. V., et al., 1996. Guidebook on the Systematics of Foraminifers of Paleozoic. Academy of Sciences of Russia. Nauka Publishing House (in Russian) |
Renema, W., 2007. Fauna Development of Larger Benthic Foraminifera in the Cenozoic of Southeast Asia. In: Renema, W., ed., Biogeography, Time, and Place: Distributions, Barriers, and Islands. Springer Netherlands, Dordrecht. 179–215. https://doi.org/10.1007/978-1-4020-6374-9_6 |
Reymond, C. E., Bode, M., Renema, W., et al., 2011. Ecological Incumbency Impedes Stochastic Community Assembly in Holocene Foraminifera from the Huon Peninsula, Papua New Guinea. Paleobiology, 37(4): 670–685. https://doi.org/10.1666/09087.1 |
Rokas, A., Carroll, S. B., 2008. Frequent and Widespread Parallel Evolution of Protein Sequences. Molecular Biology and Evolution, 25(9): 1943–1953. https://doi.org/10.1093/molbev/msn143 |
Seilacher, A., 1970. Arbeitskonzept Zur Konstruktions-Morphologie. Lethaia, 3(4): 393–396. https://doi.org/10.1111/j.1502-3931.1970.tb00830.x |
Serra-Kiel, J., Hottinger, L., Caus, E., et al., 1998. Larger Foraminiferal Biostratigraphy of the Tethyan Paleocene and Eocene. Bulletin de la Société Géologique de France, 169: 281–299 |
Song, H. J., Tong, J. N., Wignall, P. B., et al., 2016. Early Triassic Disaster and Opportunistic Foraminifers in South China. Geological Magazine, 153(2): 298–315. https://doi.org/10.1017/s0016756815000497 |
Stuhr, M., Cameron, L. P., Blank-Landeshammer, B., et al., 2021. Divergent Proteomic Responses Offer Insights into Resistant Physiological Responses of a Reef-Foraminifera to Climate Change Scenarios. Oceans, 2(2): 281–314. https://doi.org/10.3390/oceans2020017 |
Tan, S. H., 1932. On the genus Cycloclypeus, Pt. 1, and an Appendix on the Heterostegines of Tjimanggoe, S. Bantam, Java. Wetenschappelijke Mededeelingen van de Dienst van de Mijnbouw in Nederlandsch-Oost-Indië, 19: 1–194 |
Urbanek, A., 1993. Biotic Crises in the History of Upper Silurian Graptoloids: A Palaeobiological Model. Historical Biology, 7(1): 29–50. https://doi.org/10.1080/10292389309380442 |
You, Y., Huber, M., Müller, R. D., et al., 2009. Simulation of the Middle Miocene Climate Optimum. Geophysical Research Letters, 36(4): L04702. https://doi.org/10.1029/2008gl036571 |
van der Vlerk, I. M., 1922. Studiën over Nummulinidae en Alveolinidae. Haar voorkomen op Soembawa en haar Betekenis voor de Geologie van Oost-Azië en Australië. Wetenschappelijke Mededeelingen van de Dienst van de Mijnbouw in Nederlandsch-Oost-Indië, 6: 329–468 |
van der Vlerk, I. M., 1929. Groote Foraminiferen van N. O. Borneo. Wetenschappelijke Mededeelingen van de Dienst van den Mijnbouw in Nederlandsch-Oost-Indië, 9: 1–45 |
van Gorsel, J., 1975. Evolutionary Trends and Stratigraphic Significance of the Late Cretaceous Helicorbitoides-Lepidorbitoides Lineage. Utrecht Micropaleontological Bulletins, 12: 1–99 |
Vogwill, T., Kojadinovic, M., Furió, V., et al., 2014. Testing the Role of Genetic Background in Parallel Evolution Using the Comparative Experimental Evolution of Antibiotic Resistance. Molecular Biology and Evolution, 31(12): 3314–3323. https://doi.org/10.1093/molbev/msu262 |
Wignall, P. B., Benton, M. J., 1999. Discussion on Lazarus Taxa and Fossil Abundance at Times of Biotic Crisis. Journal of the Geological Society, 156(3): 453–456 |