The global genetic diversity of planktonic foraminifera reveals the structure of cryptic speciation in plankton.

automated delimitation barcoding biodiversity biogeography cryptic diversity ecology metabarcoding molecular taxonomy planktonic foraminifera protists

Journal

Biological reviews of the Cambridge Philosophical Society
ISSN: 1469-185X
Titre abrégé: Biol Rev Camb Philos Soc
Pays: England
ID NLM: 0414576

Informations de publication

Date de publication:
13 Feb 2024
Historique:
revised: 04 02 2024
received: 31 08 2023
accepted: 07 02 2024
medline: 14 2 2024
pubmed: 14 2 2024
entrez: 14 2 2024
Statut: aheadofprint

Résumé

The nature and extent of diversity in the plankton has fascinated scientists for over a century. Initially, the discovery of many new species in the remarkably uniform and unstructured pelagic environment appeared to challenge the concept of ecological niches. Later, it became obvious that only a fraction of plankton diversity had been formally described, because plankton assemblages are dominated by understudied eukaryotic lineages with small size that lack clearly distinguishable morphological features. The high diversity of the plankton has been confirmed by comprehensive metabarcoding surveys, but interpretation of the underlying molecular taxonomies is hindered by insufficient integration of genetic diversity with morphological taxonomy and ecological observations. Here we use planktonic foraminifera as a study model and reveal the full extent of their genetic diversity and investigate geographical and ecological patterns in their distribution. To this end, we assembled a global data set of ~7600 ribosomal DNA sequences obtained from morphologically characterised individual foraminifera, established a robust molecular taxonomic framework for the observed diversity, and used it to query a global metabarcoding data set covering ~1700 samples with ~2.48 billion reads. This allowed us to extract and assign 1 million reads, enabling characterisation of the structure of the genetic diversity of the group across ~1100 oceanic stations worldwide. Our sampling revealed the existence of, at most, 94 distinct molecular operational taxonomic units (MOTUs) at a level of divergence indicative of biological species. The genetic diversity only doubles the number of formally described species identified by morphological features. Furthermore, we observed that the allocation of genetic diversity to morphospecies is uneven. Only 16 morphospecies disguise evolutionarily significant genetic diversity, and the proportion of morphospecies that show genetic diversity increases poleward. Finally, we observe that MOTUs have a narrower geographic distribution than morphospecies and that in some cases the MOTUs belonging to the same morphospecies (cryptic species) have different environmental preferences. Overall, our analysis reveals that even in the light of global genetic sampling, planktonic foraminifera diversity is modest and finite. However, the extent and structure of the cryptic diversity reveals that genetic diversification is decoupled from morphological diversification, hinting at different mechanisms acting at different levels of divergence.

Identifiants

pubmed: 38351434
doi: 10.1111/brv.13065
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : Deutsche Forschungsgemeinschaft
ID : 390741603
Organisme : Juan de la Cierva-formación 2021
ID : FJC2021-047494-I/MCIN/AEI/10.13039/501100011033
Organisme : Natural Environment Research Council of the United Kingdom
ID : NER/J/S/2000/00860
Organisme : Natural Environment Research Council of the United Kingdom
ID : NE/D009707/1

Informations de copyright

© 2024 The Authors. Biological Reviews published by John Wiley & Sons Ltd on behalf of Cambridge Philosophical Society.

Références

Adl, S. M., Bass, D., Lane, C. E., Lukeš, J., Schoch, C. L., Smirnov, A., Agatha, S., Berney, C., Brown, M. W., Burki, F., Cárdenas, P., Čepička, I., Chistyakova, L., del Campo, J., Dunthorn, M., et al. (2019). Revisions to the classification, nomenclature, and diversity of eukaryotes. Journal of Eukaryotic Microbiology 66, 4-119.
André, A., Quillévéré, F., Morard, R., Ujiié, Y., Escarguel, G., de Vargas, C., de Garidel-Thoron, T. & Douady, C. J. (2014). SSU rDNA divergence in planktonic foraminifera: molecular taxonomy and biogeographic implications. PLoS ONE 9, e104641.
*André, A., Quillévéré, F., Schiebel, R., Morard, R., Howa, H., Meilland, J. & Douady, C. J. (2018). Disconnection between genetic and morphological diversity in the planktonic foraminifer Neogloboquadrina pachyderma from the Indian sector of the Southern Ocean. Marine Micropaleontology 144, 14-24.
André, A., Weiner, A., Quillévéré, F., Aurahs, R., Morard, R., Douady, C. J., de Garidel-Thoron, T., Escarguel, G., de Vargas, C. & Kucera, M. (2013). The cryptic and the apparent reversed: lack of genetic differentiation within the morphologically diverse plexus of the planktonic foraminifer Globigerinoides sacculifer. Paleobiology 39, 21-39.
*Aurahs, R., Göker, M., Grimm, G. W., Hemleben, V., Hemleben, C., Schiebel, R. & Kučera, M. (2009a). 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, 155-177.
Aurahs, R., Grimm, G. W., Hemleben, V., Hemleben, C. & Kucera, M. (2009b). Geographical distribution of cryptic genetic types in the planktonic foraminifer Globigerinoides ruber. Molecular Ecology 18, 1692-1706.
Aurahs, R., Treis, Y., Darling, K. & 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, 1-14.
Aze, T., Ezard, T. H. G., Purvis, A., Coxall, H. K., Stewart, D. R. M., Wade, B. S. & Pearson, P. N. (2011). A phylogeny of Cenozoic macroperforate planktonic foraminifera from fossil data. Biological Reviews 86, 900-927.
*Barbera, P., Kozlov, A. M., Czech, L., Morel, B., Darriba, D., Flouri, T. & Stamatakis, A. (2019). EPA-ng: massively parallel evolutionary placement of genetic sequences. Systematic Biology 68, 365-369.
Barrenechea Angeles, I., Lejzerowicz, F., Cordier, T., Scheplitz, J., Kucera, M., Ariztegui, D., Pawlowski, J. & Morard, R. (2020). Planktonic foraminifera eDNA signature deposited on the seafloor remains preserved after burial in marine sediments. Scientific Reports 10, 1-12.
Bauch, D., Darling, K., Simstich, J., Bauch, H. A. & Erlenkeuser, H. (2003). Palaeoceanographic implications of genetic variation in living North Atlantic Neogloboquadrina pachyderma. Nature 424, 11-14.
*Becker, R. A., Wilks, A. R., Brownrigg, R., Minka, T. P. & Deckmyn, A. (2021). maps: draw geographical maps. https://cran.r-project.org/package=maps.
Bickford, D., Lohman, D. J., Sodhi, N. S., Ng, P. K. L., Meier, R., Winker, K., Ingram, K. K. & Das, I. (2007). Cryptic species as a window on diversity and conservation. Trends in Ecology and Evolution 22, 148-155.
*Bird, C., Darling, K. F., Russell, A. D., Davis, C. V., Fehrenbacher, J., Free, A., Wyman, M. & Ngwenya, B. T. (2017). Cyanobacterial endobionts within a major marine planktonic calcifier (Globigerina bulloides, foraminifera) revealed by 16S rRNA metabarcoding. Biogeosciences 14, 901-920.
Bird, C., Darling, K. F., Russell, A. D., Fehrenbacher, J. S., Davis, C. V., Free, A. & Ngwenya, B. T. (2018). 16S rRNA gene metabarcoding and TEM reveals different ecological strategies within the genus Neogloboquadrina (planktonic foraminifer). PLoS ONE 13, e0191653.
Blaxter, M. (2016). Imagining Sisyphus happy: DNA barcoding and the unnamed majority. Philosophical Transactions of the Royal Society B: Biological Sciences 371, 20150329.
Brummer, G. A., Hemleben, C. & Spindler, M. (1986). Planktonic foraminiferal ontogeny and new perspectives for micropalaeontology. Nature 319, 50-52.
Brummer, G. A. & Kucera, M. (2022). Taxonomic review of living planktonic foraminifera. Journal of Micropalaeontology 41, 29-74.
Bucklin, A. N. N., Lindeque, P. K., Rodriguez-ezpeleta, N., Albaina, A. & Lehtiniemi, M. (2016). Metabarcoding of marine zooplankton: prospects, progress and pitfalls. Journal of Plankton Research 38, 393-400.
Burki, F., Sandin, M. M. & Jamy, M. (2021). Diversity and ecology of protists revealed by metabarcoding. Current Biology 31, R1267-R1280.
*Callahan, B. J., McMurdie, P. J., Rosen, M. J., Han, A. W., Johnson, A. J. A. & Holmes, S. P. (2016). DADA2: high-resolution sample inference from illumina amplicon data. Nature Methods 13, 581-583.
Caron, D. A. & Hu, S. K. (2019). Are we overestimating protistan diversity in nature? Trends in Microbiology 27, 197-205.
Chaabane, S., de Garidel-Thoron, T., Giraud, X., Schiebel, R., Beaugrand, G., Brummer, G.-J., Casajus, N., Greco, M., Grigoratou, M., Howa, H., Jonkers, L., Kucera, M., Kuroyanagi, A., Meilland, J., Monteiro, F., et al. (2023). The FORCIS database: A global census of planktonic foraminifera from ocean waters. Scientific Data 10, 1-16.
Chapman, M. G. & Underwood, A. J. (1999). Ecological patterns in multivariate assemblages: information and interpretation of negative values in ANOSIM tests. Marine Ecology Progress Series 180, 257-265.
*Conway, J. & Gehlenborg, N. (2017). UpSetR: a more scalable alternative to Venn and Euler diagrams for visualizing intersecting sets. https://github.com/hms-dbmi/UpSetR.
Cordier, T., Angeles, I. B., Henry, N., Lejzerowicz, F., Berney, C., Morard, R., Brandt, A., Cambon-Bonavita, M.-A., Guidi, L., Lombard, F., Arbizu, P. M., Massana, R., Orejas, C., Poulain, J., Smith, C. R., et al. (2022). Patterns of eukaryotic diversity from the surface to the deep-ocean sediment. Science Advances 8, 1-13.
Cristescu, M. E. (2014). From barcoding single individuals to metabarcoding biological communities: towards an integrative approach to the study of global biodiversity. Trends in Ecology & Evolution 29, 566-571.
*Darling, K. F., Kroon, D., Wade, C. M. & Leigh Brown, A. J. (1996). Molecular phylogeny of the planktic foraminifera. The Journal of Foraminiferal Research 26, 324-330.
Darling, K. F., Kucera, M., Kroon, D. & Wade, C. M. (2006). A resolution for the coiling direction paradox in Neogloboquadrina pachyderma. Paleoceanography 21, PA2011.
Darling, K. F., Kucera, M., Pudsey, C. J. & Wade, C. M. (2004). Molecular evidence links cryptic diversification in polar planktonic protists to quaternary climate dynamics. Proceedings of the National Academy of Sciences of the United States of America 101, 7657-7662.
Darling, K. F., Kucera, M. & Wade, C. M. (2007). Global molecular phylogeography reveals persistent Arctic circumpolar isolation in a marine planktonic protist. Proceedings of the National Academy of Sciences of the United States of America 104, 5002-5007.
Darling, K. F., Kucera, M., Wade, C. M., von Langen, P. & Pak, D. (2003). Seasonal distribution of genetic types of planktonic foraminifer morphospecies in the Santa Barbara Channel and its paleoceanographic implications. Paleoceanography 18, 1-10.
Darling, K. F. & Wade, C. M. (2008). The genetic diversity of planktic foraminifera and the global distribution of ribosomal RNA genotypes. Marine Micropaleontology 67, 216-238.
Darling, K. F., Wade, C. M., Kroon, D. & Brown, A. J. L. (1997). Planktic foraminiferal molecular evolution and their polyphyletic origins from benthic taxa. Marine Micropaleontology 30, 251-266.
*Darling, K. F., Wade, C. M., Kroon, D., Brown, A. J. L. & 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 circulation. Paleoceanography 14, 3-12.
Darling, K. F., Wade, C. M., Siccha, M., Trommer, G., Schulz, H., Abdolalipour, S. & Kurasawa, A. (2017). Genetic diversity and ecology of the planktonic foraminifers Globigerina bulloides, Turborotalita quinqueloba and Neogloboquadrina pachyderma off the Oman margin during the late SW monsoon. Marine Micropaleontology 137, 64-77.
Darling, K. F., Wade, C. M., Stewart, I. A., Kroon, D., Dingle, R. & Brown, A. J. (2000). Molecular evidence for genetic mixing of Arctic and Antarctic subpolar populations of planktonic foraminifers. Nature 405, 43-47.
*Darriba, D., Posada, D., Kozlov, A. M., Stamatakis, A., Morel, B. & Flouri, T. (2020). ModelTest-NG: a new and scalable tool for the selection of DNA and protein evolutionary models. Molecular Biology and Evolution 37, 291-294.
Davis, C. V., Livsey, C. M., Palmer, H. M., Hull, P. M., Thomas, E., Hill, T. M. & Benitez-Nelson, C. R. (2020). Extensive morphological variability in asexually produced planktic foraminifera. Science Advances 6, 1-8.
De Queiroz, K. (2007). Species concepts and species delimitation. Systematic biology 56, 879-886.
de Vargas, C., Audic, S., Henry, N., Decelle, J., Mahé, F., Logares, R., Lara, E., Berney, C., Le Bescot, N., Probert, I., Carmichael, M., Poulain, J., Romac, S., Colin, S., Aury, J.-M., et al. (2015). Eukaryotic plankton diversity in the sunlit ocean. Science 348, 1261605.
de Vargas, C., Bonzon, M., Rees, N. W., Pawlowski, J. & Zaninetti, L. (2002). A molecular approach to biodiversity and biogeography in the planktonic foraminifer Globigerinella siphonifera (d'Orbigny). Marine Micropaleontology 45, 101-116.
*De Vargas, C., Le Bescot, N., Pollina, T., Henry, N., Romac, S., Haëntjens, N., Carmichael, M., Berger, C., Le Guen, D., Decelle, J., Poulain, J., Malpot, E., Beaumont, C., Hardy, M., Guiffant, D., et al. (2022). Plankton planet: a frugal, cooperative measure of aquatic life at the planetary scale. Frontiers in Marine Science 9, 1-17.
de Vargas, C., Norris, R., Zaninetti, L., Gibb, S. W. & Pawlowski, J. (1999). Molecular evidence of cryptic speciation in planktonic foraminifers and their relation to oceanic provinces. Proceedings of the National Academy of Sciences of the United States of America 96, 2864-2868.
de Vargas, C. & Pawlowski, J. (1998). Molecular versus taxonomic rates of evolution in planktonic foraminifera. Molecular Phylogenetics and Evolution 9, 463-469.
de Vargas, C., Renaud, S., Hilbrecht, H. & Pawlowski, J. (2001). Pleistocene adaptive radiation in Globorotalia truncatulinoides: genetic, morphologic, and environmental evidence. Paleobiology 27, 104-125.
*de Vargas, C., Zaninetti, L., Hilbrecht, H. & 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.
*Duarte, C. M. (2015). Seafaring in the 21st century: the Malaspina 2010 circumnavigation expedition. Limnology and Oceanography Bulletin 24, 11-14.
Eme, D., Zagmajster, M., Delić, T., Fišer, C., Flot, J.-F., Konecny-Dupré, L., Pálsson, S., Stoch, F., Zakšek, V., Douady, C. J. & Malard, F. (2018). Do cryptic species matter in macroecology? Sequencing European groundwater crustaceans yields smaller ranges but does not challenge biodiversity determinants. Ecography 41, 424-436.
*Ertan, K. T., Hemleben, V. & Hemleben, C. (2004). Molecular evolution of some selected benthic foraminifera as inferred from sequences of the small subunit ribosomal DNA. Marine Micropaleontology 53, 367-388.
Fenton, I. S., Aze, T., Farnsworth, A., Valdes, P. & Saupe, E. E. (2023). Origination of the modern-style diversity gradient 15 million years ago. Nature 614, 708-712.
Fenton, I. S., Woodhouse, A., Aze, T., Lazarus, D., Renaudie, J., Dunhill, A. M., Young, J. R. & Saupe, E. E. (2021). Triton, a new species-level database of Cenozoic planktonic foraminiferal occurrences. Scientific Data 8, 160.
Flegontova, O., Lukeš, J. & Horák, A. (2023). Intragenomic diversity of the V9 hypervariable domain in eukaryotes has little effect on metabarcoding. iScience 26, 107291.
Förderer, M., Rödder, D. & Langer, M. R. (2018). Patterns of species richness and the center of diversity in modern Indo-Pacific larger foraminifera. Scientific Reports 8, 8189.
Gomez, F. (2012). A quantitative review of the lifestyle, habitat and trophic diversity of dinoflagellates (Dinoflagellata, Alveolata). Systematics and Biodiversity 10, 267-275.
Greco, M., Morard, R., Darling, K. & Kucera, M. (2023). Macroevolutionary patterns in intragenomic rDNA variability among planktonic foraminifera. PeerJ 11, e15255.
Greco, M., Morard, R. & Kucera, M. (2021). Single-cell metabarcoding reveals biotic interactions of the Arctic calcifier Neogloboquadrina pachyderma with the eukaryotic pelagic community. Journal of Plankton Research 43, 113-125.
Guillou, L., Bachar, D., Audic, S., Bass, D., Berney, C., Bittner, L., Boutte, C., Burgaud, G., de Vargas, C., Decelle, J., del Campo, J., Dolan, J. R., Dunthorn, M., Edvardsen, B., Holzmann, M., et al. (2013). The protist ribosomal reference database (PR2): a catalog of unicellular eukaryote small sub-unit rRNA sequences with curated taxonomy. Nucleic Acids Research 41, D597-D604.
Hebert, P. D. N., Cywinska, A., Ball, S. L. & DeWaard, J. R. (2003). Biological identifications through DNA barcodes. Proceedings Biological Sciences/The Royal Society 270, 313-321.
Henry, N., de Vargas, C. & Audic, S. (2019). PR2_V9, a SSU V9 rDNA reference database with functional annotations. [Data set]. Zenodo. https://doi.org/10.5281/zenodo.3768951
Hillebrand, H. (2004). On the generality of the latitudinal diversity gradient. American Naturalist 163, 192-211.
Holzmann, M., Habura, A., Giles, H., Bowser, S. S. & Pawlowski, J. (2007). Freshwater foraminiferans revealed by analysis of environmental DNA samples. The Journal of Eukaryotic Microbiology 50, 135-139.
*Holzmann, M. & Pawlowski, J. (2017). An updated classification of rotaliid foraminifera based on ribosomal DNA phylogeny. Marine Micropaleontology 132, 18-34.
*Hsieh, T. C., Ma, K. H. & Chao, A. (2016). iNEXT: an R package for rarefaction and extrapolation of species diversity (Hill numbers). Methods in Ecology and Evolution 7, 1451-1456.
Huber, B. T., Bijma, J. & Darling, K. (1997). Cryptic speciation in the living planktonic foraminifer Globigerinella siphonifera. Paleobiology 23, 33-62.
*Ibarbalz, F. M., Henry, N., Brandão, M. C., Martini, S., Busseni, G., Byrne, H., Coelho, L. P., Endo, H., Gasol, J. M., Gregory, A. C., Mahé, F., Rigonato, J., Royo-Llonch, M., Salazar, G., Sanz-Sáez, I., et al. (2019). Global trends in marine plankton diversity across kingdoms of life. Cell 179, 1084-1097.
Jonkers, L. & Kučera, M. (2015). Global analysis of seasonality in the shell flux of extant planktonic foraminifera. Biogeosciences 12, 2207-2226.
Karsenti, E., Acinas, S. G., Bork, P., Bowler, C., De Vargas, C., Raes, J., Sullivan, M., Arendt, D., Benzoni, F., Claverie, J.-M., Follows, M., Gorsky, G., Hingamp, P., Iudicone, D., Jaillon, O., et al. (2011). A holistic approach to marine eco-systems biology. PLoS Biology 9, e1001177.
*Kassambara, A. (2016). Factoextra: extract and visualize the results of multivariate data analyses. R package version 1.0.7. https://cran.r-project.org/web/packages/factoextra%0A.
*Katoh, K. & Standley, D. M. (2013). MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution 30, 772-780.
Katz, M. E., Cramer, B. S., Franzese, a., Honisch, B., Miller, K. G., Rosenthal, Y. & Wright, J. D. (2010). Traditional and emerging geochemical proxies in foraminifera. The Journal of Foraminiferal Research 40, 165-192.
Keck, F., Couton, M. & Altermatt, F. (2022). Navigating the seven challenges of taxonomic reference databases in metabarcoding analyses. Molecular Ecology Resources 23, 742-755.
Kimoto, K. & Tsuchiya, M. (2006). The “unusual” reproduction of planktic foraminifera: an asexual reproductive phase of Neogloboquadrina pachyderma (Ehrenberg). Anuário do Instituto de Geociências - UFRJ 29, 461.
Kucera, M. (2007). Chapter six planktonic foraminifera as tracers of past oceanic environments. In Developments in Marine Geology (eds C. Hillaire-Marcel and A. De Vernal), pp. 213-262. GEOTOP-Université du Québec à Montréal, Montréal, Québec, Canada.
Kucera, M. & Darling, K. F. (2002). Cryptic species of planktonic foraminifera: their effect on palaeoceanographic reconstructions. Philosophical Transactions Series A, Mathematical, Physical, and Engineering Sciences 360, 695-718.
Kucera, M., Rosell-Melé, A., Schneider, R., Waelbroeck, C. & Weinelt, M. (2005). Multiproxy approach for the reconstruction of the glacial ocean surface (MARGO). Quaternary Science Reviews 24, 813-819.
*Kuroyanagi, A., Tsuchiya, M., Kawahata, H. & Kitazato, H. (2008). The occurrence of two genotypes of the planktonic foraminifer Globigerinoides ruber (white) and paleo-environmental implications. Marine Micropaleontology 68, 236-243.
Lecroq, B., Lejzerowicz, F., Bachar, D., Christen, R., Esling, P., Baerlocher, L., Osterås, M., Farinelli, L. & Pawlowski, J. (2011). Ultra-deep sequencing of foraminiferal microbarcodes unveils hidden richness of early monothalamous lineages in deep-sea sediments. Proceedings of the National Academy of Sciences of the United States of America 108, 13177-13182.
Lejzerowicz, F., Gooday, A. J., Barrenechea Angeles, I., Cordier, T., Morard, R., Apothéloz-Perret-Gentil, L., Lins, L., Menot, L., Brandt, A., Levin, L. A., Martinez Arbizu, P., Smith, C. R. & Pawlowski, J. (2021). Eukaryotic biodiversity and spatial patterns in the Clarion-Clipperton zone and other abyssal regions: insights from sediment DNA and RNA metabarcoding. Frontiers in Marine Science 8, 671033.
Lejzerowicz, F., Pawlowski, J., Fraissinet-Tachet, L. & Marmeisse, R. (2010). Molecular evidence for widespread occurrence of foraminifera in soils. Environmental Microbiology 12, 2518-2526.
*Letunic, I. & Bork, P. (2021). Interactive tree of life (iTOL) v5: an online tool for phylogenetic tree display and annotation. Nucleic Acids Research 49, 293-296.
Macher, J.-N., Coots, N. L., Poh, Y.-P., Girard, E. B., Langerak, A., Muñoz-Gómez, S. A., Sinha, S. D., Jirsová, D., Vos, R., Wissels, R., Gile, G. H., Renema, W. & Wideman, J. G. (2023). Single-cell genomics reveals the divergent mitochondrial genomes of Retaria (foraminifera and Radiolaria). mBio 14, e00302-e00323.
Mahé, F., De Vargas, C., Bass, D., Czech, L., Stamatakis, A., Lara, E., Singer, D., Mayor, J., Bunge, J., Sernaker, S., Siemensmeyer, T., Trautmann, I., Romac, S., Berney, C., Kozlov, A., et al. (2017). Parasites dominate hyperdiverse soil protist communities in neotropical rainforests. Nature Ecology and Evolution 1, 91.
Malviya, S., Scalco, E., Audic, S., Vincent, F., Veluchamy, A., Poulain, J., Wincker, P., Iudicone, D., de Vargas, C., Bittner, L., Zingone, A. & Bowler, C. (2016). Insights into global diatom distribution and diversity in the world's ocean. Proceedings of the National Academy of Sciences 113, E1516-E1525.
Meilland, J., Ezat, M. M., Westgard, A., Manno, C., Morard, R., Siccha, M. & Kucera, M. (2022). Rare but persistent asexual reproduction explains the success of planktonic foraminifera in polar oceans. Journal of Plankton Research 45, 15-32.
*Milivojević, T., Rahman, S. N., Raposo, D., Siccha, M., Kucera, M. & Morard, R. (2021). High variability in SSU rDNA gene copy number among planktonic foraminifera revealed by single-cell qPCR. ISME Communications 1, 63.
Mora, C., Tittensor, D. P., Adl, S., Simpson, A. G. B. & Worm, B. (2011). How many species are there on Earth and in the ocean? PLoS biology 9, e1001127.
*Morard, R. (2010). For a better characterization of the fossil pelagic record: molecular, biogeographical and ecological diversity of planctonic foraminifers cryptic species. Université Claude Bernard Lyon I.
Morard, R., Darling, K. F., Mahé, F., Audic, S., Ujiié, Y., Weiner, A. K. M., André, A., Seears, H. a., Wade, C. M., Quillévéré, F., Douady, C. J., Escarguel, G., de Garidel-Thoron, T., Siccha, M., Kucera, M., et al. (2015). PFR2: a curated database of planktonic foraminifera 18S ribosomal DNA as a resource for studies of plankton ecology, biogeography and evolution. Molecular Ecology Resources 15, 1472-1485.
Morard, R., Escarguel, G., Weiner, A. K. M., André, A., Douady, C. J., Wade, C. M., Darling, K. F., Ujiié, Y., Seears, H. A., Quillévéré, F., de Garidel-Thoron, T., de Vargas, C. & Kucera, M. (2016). Nomenclature for the nameless: a proposal for an integrative molecular taxonomy of cryptic diversity exemplified by planktonic foraminifera. Systematic Biology 65, 925-940.
Morard, R., Füllberg, A., Brummer, G. J. A., Greco, M., Jonkers, L., Wizemann, A., Weiner, A. K. M., Darling, K., Siccha, M., Ledevin, R., Kitazato, H., De Garidel-Thoron, T., De Vargas, C. & Kucera, M. (2019a). Genetic and morphological divergence in the warm-water planktonic foraminifera genus Globigerinoides. PLoS ONE 14, 1-30.
Morard, R., Hassenrück, C., Greco, M., Fernandez-Guerra, A., Rigaud, S., Douady, C. J. & Kucera, M. (2022). Renewal of planktonic foraminifera diversity after the Cretaceous Paleogene mass extinction by benthic colonizers. Nature Communications 13, 1-9.
Morard, R., Lejzerowicz, F., Darling, K. F., Lecroq-bennet, B., Pedersen, M. W., Orlando, L., Pawlowski, J., Mulitza, S., De Vargas, C. & Kucera, M. (2017). Planktonic foraminifera-derived environmental DNA extracted from abyssal sediments preserves patterns of plankton macroecology. Biogeosciences 14, 2741-2754.
Morard, R., Mahé, F., Romac, S., Poulain, J., Kucera, M. & De Vargas, C. (2018). Surface ocean metabarcoding confirms limited diversity in planktonic foraminifera but reveals unknown hyper-abundant lineages. Scientific Reports 8, 2539.
Morard, R., Quillévéré, F., Douady, C. J., de Vargas, C., de Garidel-Thoron, T. & Escarguel, G. (2011). Worldwide genotyping in the planktonic foraminifer Globoconella inflata: implications for life history and paleoceanography. PLoS ONE 6, e26665.
Morard, R., Quillévéré, F., Escarguel, G., de Garidel-Thoron, T., de Vargas, C. & Kucera, M. (2013). Ecological modeling of the temperature dependence of cryptic species of planktonic foraminifera in the southern hemisphere. Palaeogeography, Palaeoclimatology, Palaeoecology 391, 13-33.
*Morard, R., Quillévéré, F., Escarguel, G., Ujiie, Y., de Garidel-Thoron, T., Norris, R. D. & de Vargas, C. (2009). Morphological recognition of cryptic species in the planktonic foraminifer Orbulina universa. Marine Micropaleontology 71, 148-165.
Morard, R., Vollmar, N. M., Greco, M. & Kucera, M. (2019b). Unassigned diversity of planktonic foraminifera from environmental sequencing revealed as known but neglected species. PLoS ONE 14, e0213936.
*NASA Goddard Space Flight Center, Ocean Ecology Laboratory, Ocean Biology Processing Group. Moderate-resolution Imaging Spectroradiometer (MODIS) Aqua Sea Surface Temperature Data (2014). Reprocessing. NASA OB.DAAC, Greenbelt.
*Oksanen, J., Kindt, R., Legendre, P., O'Hara, B., Stevens, M. H. H., Oksanen, M. J. & Suggests, M. (2007). The vegan package. Community Ecology Package 10, 631-637.
Olenin, S., Gollasch, S., Jonušas, S. & Rimkutè, I. (2000). En-route investigations of plankton in ballast water on a ship's voyage from the Baltic Sea to the open Atlantic coast of Europe. International Review of Hydrobiology 85, 577-596.
*Paradis, E., Blomber, S., Bolker, B., Brown, J., Claude, J., Hoa, S., Desper, R., Didier, G., Durand, B., Dutheil, J., Ewing, R., Gascuel, O., Guillerme, T., Heibl, C., Ives, A., et al. (2019). Package ‘ape’: analyses of phylogenetics and evolution depends R (3.2.0).
Pawlowski, J. & Holzmann, M. (2014). A plea for DNA barcoding of foraminifera. The Journal of Foraminiferal Research 44, 62-67.
*Pawlowski, J., Holzmann, M. & Tyszka, J. (2013). New supraordinal classification of foraminifera: molecules meet morphology. Marine Micropaleontology 100, 1-10.
Pawlowski, J. & Lecroq, B. (2010). Short rDNA barcodes for species identification in foraminifera. The Journal of Eukaryotic Microbiology 57, 197-205.
Puillandre, N., Brouillet, S. & Achaz, G. (2021). ASAP: assemble species by automatic partitioning. Molecular Ecology Resources 21, 609-620.
Quillévéré, F., Morard, R., Escarguel, G., Douady, C. J., Ujiié, Y., de Garidel-Thoron, T. & de Vargas, C. (2013). Global scale same-specimen morpho-genetic analysis of Truncorotalia truncatulinoides: A perspective on the morphological species concept in planktonic foraminifera. Palaeogeography, Palaeoclimatology, Palaeoecology 391, 2-12.
*R Core Team (2020). R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna https://www.r-project.org/.
Rillo, M. C., Sugawara, M. T. C., Cabella, B., Jonkers, L., Baranowski, U. K., Kučera, M. & Ezard, T. H. G. (2019). On the mismatch in the strength of competition among fossil and modern species of planktonic foraminifera. Global Ecology and Biogeography 28, 1866-1878.
Rillo, M. C., Woolley, S. & Hillebrand, H. (2022). Drivers of global pre-industrial patterns of species turnover in planktonic foraminifera. Ecography 2022, 1-11.
*Rognes, T., Flouri, T., Nichols, B., Quince, C. & Mahé, F. (2016). VSEARCH: a versatile open source tool for metagenomics. PeerJ 4, e2584.
*Sadekov, A. Y., Darling, K. F., Ishimura, T., Wade, C. M., Kimoto, K., Singh, A. D., Anand, P., Kroon, D., Jung, S., Ganssen, G., Ganeshram, R., Tsunogai, U. & Elderfield, H. (2016). Geochemical imprints of genotypic variants of Globigerina bulloides in the Arabian Sea. Paleoceanography 31, 1440-1452.
Sandin, M. M., Romac, S. & Not, F. (2022). Intra-genomic rRNA gene variability of Nassellaria and Spumellaria (Rhizaria, Radiolaria) assessed by Sanger, MinION and Illumina sequencing. Environmental Microbiology 24, 2979-2993.
*Schmidtko, S., Johnson, G. C. & Lyman, J. M. (2013). MIMOC: a global monthly isopycnal upper-ocean climatology with mixed layers. Journal of Geophysical Research: Oceans 118, 1658-1672.
Schnell, I. B., Bohmann, K. & Gilbert, M. T. P. (2015). Tag jumps illuminated - reducing sequence-to-sample misidentifications in metabarcoding studies. Molecular Ecology Resources 15, 1289-1303.
*Schweizer, M., Pawlowski, J., Kouwenhoven, T. J., Guiard, J. & van der Zwaan, B. (2008). Molecular phylogeny of Rotaliida (foraminifera) based on complete small subunit rDNA sequences. Marine Micropaleontology 66, 233-246.
Seears, H. a., Darling, K. F. & Wade, C. M. (2012). Ecological partitioning and diversity in tropical planktonic foraminifera. BMC Evolutionary Biology 12, 1-15.
Siccha, M. & Kucera, M. (2017). ForCenS, a curated database of planktonic foraminifera census counts in marine surface sediment samples. Scientific Data 4, 170109.
Sierra, R., Mauffrey, F., Cruz, J., Holzmann, M., Gooday, A. J., Maurer-Alcalá, X., Thakur, R., Greco, M., Weiner, A. K. M., Katz, L. A. & Pawlowski, J. (2022). Taxon-rich transcriptomics supports higher-level phylogeny and major evolutionary trends in foraminifera. Molecular Phylogenetics and Evolution 174, 1-6.
Slatkin, M. (1987). Gene flow and the geographic structure of natural populations. Science 236, 787-792.
Spalding, M. D., Agostini, V. N., Rice, J. & Grant, S. M. (2012). Pelagic provinces of the world: a biogeographic classification of the world's surface pelagic waters. Ocean & Coastal Management 60, 19-30.
*Spezzaferri, S., Kucera, M., Pearson, P. N., Wade, B. S., Rappo, S., Poole, C. R., Morard, R. & Stalder, C. (2015). Fossil and genetic evidence for the polyphyletic nature of the planktonic foraminifera ‘Globigerinoides’, and description of the new genus Trilobatus. PLoS ONE 10, e0128108.
Stewart, I. A., Darling, K. F., Kroon, D., Wade, C. M. & Troelstra, S. R. (2001). Genotypic variability in subarctic Atlantic planktic foraminifera. Marine Micropaleontology 43, 143-153.
Strack, T., Jonkers, L., Rillo, C. M., Hillebrand, H. & Kucera, M. (2022). Plankton response to global warming is characterized by non-uniform shifts in assemblage composition since the last ice age. Nature Ecology & Evolution 6, 1871-1880.
Suzuki, N. & Not, F. (2015). Biology and ecology of Radiolaria. In Marine Protists: Diversity and Dynamics, 1st Edition, (eds S. Ohtsuka, T. Suzaki, T. Horiguchi, N. Suzuki and F. Not), pp. 179-222. Springer Japan, Tokyo.
Takagi, H., Kurasawa, A. & Kimoto, K. (2020). Observation of asexual reproduction with symbiont transmission in planktonic foraminifera. Journal of Plankton Research 42, 403-410.
*Ujiié, Y. & Asami, T. (2014). Temperature is not responsible for left-right reversal in pelagic unicellular zooplanktons. Journal of Zoology 293, 16-24.
Ujiié, Y., Asami, T., de Garidel-Thoron, T., Liu, H., Ishitani, Y. & de Vargas, C. (2012). Longitudinal differentiation among pelagic populations in a planktic foraminifer. Ecology and Evolution 2, 1725-1737.
*Ujiié, Y., de Garidel-Thoron, T., Watanabe, S., Wiebe, P. & de Vargas, C. (2010). Coiling dimorphism within a genetic type of the planktonic foraminifer Globorotalia truncatulinoides. Marine Micropaleontology 77, 145-153.
*Ujiié, Y. & Ishitani, Y. (2016). Evolution of a planktonic foraminifer during environmental changes in the tropical oceans. PLoS ONE 11, 1-16.
*Ujiié, Y., Kimoto, K. & Pawlowski, J. (2008). Molecular evidence for an independent origin of modern triserial planktonic foraminifera from benthic ancestors. Marine Micropaleontology 69, 334-340.
Ujiié, Y. & Lipps, J. H. (2009). Cryptic diversity in planktonic foraminifera in the northwest Pacific ocean. Journal of Foraminiferal Research 39, 145-154.
*Wade, C. M., Darling, K. F., Kroon, D. & Brown, A. J. L. (1996). Early evolutionary origin of the planktic foraminifera inferred from small subunit rDNA sequence comparisons. Journal of Molecular Evolution 43, 672-677.
*Wang, Q., Garrity, G. M., Tiedje, J. M. & Cole, J. R. (2007). Naïve Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Applied and Environmental Microbiology 73, 5261-5267.
Weber, A. A.-T. & Pawlowski, J. (2014). Wide occurrence of SSU rDNA intragenomic polymorphism in foraminifera and its implications for molecular species identification. Protist 165, 645-661.
Weiner, A., Aurahs, R., Kurasawa, A., Kitazato, H. & Kucera, M. (2012). Vertical niche partitioning between cryptic sibling species of a cosmopolitan marine planktonic protist. Molecular Ecology 21, 4063-4073.
Weiner, A. K. M., Morard, R., Weinkauf, M. F., Darling, K. F., André, A., Quillévéré, F., Ujiie, Y., Douady, C. J., de Vargas, C. & Kucera, M. (2016). Methodology for single-cell genetic analysis of planktonic foraminifera for studies of protist diversity and evolution. Frontiers in Marine Science 3, 1-15.
Weiner, A. K. M., Sehein, T., Cote-L'Heureux, A., Sleith, R. S., Greco, M., Malekshahi, C., Ryan-Embry, C., Ostriker, N. & Katz, L. A. (2023). Single-cell transcriptomics supports presence of cryptic species and reveals low levels of population genetic diversity in two testate amoebae morphospecies with large population sizes. Evolution 77, 2472-2483.
Weiner, A. K. M., Weinkauf, M. F. G., Kurasawa, A., Darling, K. F. & Kucera, M. (2015). Genetic and morphometric evidence for parallel evolution of the Globigerinella calida morphotype. Marine Micropaleontology 114, 19-35.
Weiner, A. K. M., Weinkauf, M. F. G., Kurasawa, A., Darling, K. F., Kucera, M. & Grimm, G. W. (2014). Phylogeography of the tropical planktonic foraminifera lineage Globigerinella reveals isolation inconsistent with passive dispersal by ocean currents. PLoS ONE 9, e92148.
Weinkauf, M. F. G., Siccha, M. & Weiner, A. K. M. (2022). Reproduction dynamics of planktonic microbial eukaryotes in the open ocean. Journal of the Royal Society Interface 19, 1-11.
*Wickham, H. (2009). ggplot2: Elegant Graphics for Data Analysis. Springer-Verlag, New York.
*Wickham, H., Averick, M., Bryan, J., Chang, W., McGowan, L., François, R., Grolemund, G., Hayes, A., Henry, L., Hester, J., Kuhn, M., Pedersen, T., Miller, E., Bache, S., Müller, K., et al. (2019). Welcome to the Tidyverse. Journal of Open Source Software 4, 1686.
*Wuyts, J., Van de Peer, Y. & De Wachter, R. (2001). Distribution of substitution rates and location of insertion sites in the tertiary structure of ribosomal RNA. Nucleic Acids Research 29, 5017-5028.
Yasuhara, M., Wei, C. L., Kucera, M., Costello, M. J., Tittensor, D. P., Kiessling, W., Bonebrake, T. C., Tabor, C. R., Feng, R., Baselga, A., Kretschmer, K., Kusumoto, B. & Kubota, Y. (2020). Past and future decline of tropical pelagic biodiversity. Proceedings of the National Academy of Sciences of the United States of America 117, 12891-12896.
Zhang, J., Kapli, P., Pavlidis, P. & Stamatakis, A. (2013). A general species delimitation method with applications to phylogenetic placements. Bioinformatics 29, 2869-2876.

Auteurs

Raphaël Morard (R)

MARUM Center for Marine Environmental Sciences, University of Bremen, Leobener Strasse, Bremen, 28359, Germany.

Kate F Darling (KF)

School of GeoSciences, University of Edinburgh, Edinburgh, EH9 3JW, UK.
Biological and Environmental Sciences, University of Stirling, Stirling, FK9 4LA, UK.

Agnes K M Weiner (AKM)

NORCE Climate and Environment, NORCE Norwegian Research Centre AS, Bjerknes Centre for Climate Research, Jahnebakken 5, Bergen, 5007, Norway.

Christiane Hassenrück (C)

Biological Oceanography, Leibniz Institute for Baltic Sea Research Warnemünde (IOW), Seestrasse 15, Warnemünde, 18119, Germany.

Chiara Vanni (C)

MARUM Center for Marine Environmental Sciences, University of Bremen, Leobener Strasse, Bremen, 28359, Germany.

Tristan Cordier (T)

NORCE Climate and Environment, NORCE Norwegian Research Centre AS, Bjerknes Centre for Climate Research, Jahnebakken 5, Bergen, 5007, Norway.

Nicolas Henry (N)

CNRS, Sorbonne Université, FR2424, ABiMS, Station Biologique de Roscoff, Roscoff, 29680, France.
Research Federation for the Study of Global Ocean Systems Ecology and Evolution, FR2022/Tara Oceans GOSEE, 3 rue Michel-Ange, Paris, 75016, France.

Mattia Greco (M)

Institut de Ciències del Mar, Passeig Marítim de la Barceloneta, Barcelona, 37-49, Spain.

Nele M Vollmar (NM)

MARUM Center for Marine Environmental Sciences, University of Bremen, Leobener Strasse, Bremen, 28359, Germany.
NORCE Climate and Environment, NORCE Norwegian Research Centre AS, Bjerknes Centre for Climate Research, Jahnebakken 5, Bergen, 5007, Norway.

Tamara Milivojevic (T)

MARUM Center for Marine Environmental Sciences, University of Bremen, Leobener Strasse, Bremen, 28359, Germany.
Max Planck Institute for Marine Microbiology, Bremen, Germany.

Shirin Nurshan Rahman (SN)

MARUM Center for Marine Environmental Sciences, University of Bremen, Leobener Strasse, Bremen, 28359, Germany.

Michael Siccha (M)

MARUM Center for Marine Environmental Sciences, University of Bremen, Leobener Strasse, Bremen, 28359, Germany.

Julie Meilland (J)

MARUM Center for Marine Environmental Sciences, University of Bremen, Leobener Strasse, Bremen, 28359, Germany.

Lukas Jonkers (L)

MARUM Center for Marine Environmental Sciences, University of Bremen, Leobener Strasse, Bremen, 28359, Germany.

Frédéric Quillévéré (F)

Univ Lyon, Université Claude Bernard Lyon 1, ENS de Lyon, CNRS, UMR CNRS 5276 LGL-TPE, Villeurbanne, F-69622, France.

Gilles Escarguel (G)

Univ Lyon, Université Claude Bernard Lyon 1, CNRS, ENTPE, UMR 5023 LEHNA, Villeurbanne, F-69622, France.

Christophe J Douady (CJ)

Univ Lyon, Université Claude Bernard Lyon 1, CNRS, ENTPE, UMR 5023 LEHNA, Villeurbanne, F-69622, France.
Institut Universitaire de France, Paris, France.

Thibault de Garidel-Thoron (T)

Aix Marseille Univ, CNRS, IRD, INRAE, CEREGE, Aix-en-Provence, France.

Colomban de Vargas (C)

CNRS, Sorbonne Université, FR2424, ABiMS, Station Biologique de Roscoff, Roscoff, 29680, France.
Sorbonne Université, CNRS, Station Biologique de Roscoff, AD2M, UMR7144, Place Georges Teissier, Roscoff, 29680, France.

Michal Kucera (M)

MARUM Center for Marine Environmental Sciences, University of Bremen, Leobener Strasse, Bremen, 28359, Germany.

Classifications MeSH