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

• Published in: Biological Reviews
• Main Authors: Morard, Raphaël, Darling, Kate, Weiner, Agnes, Hassenrück, Christiane, Vanni, Chiara, Cordier, Tristan, Henry, Nicolas, Greco, Mattia, Vollmar, Nele, Milivojevic, Tamara, Rahman, Shirin Nurshan, Siccha, Michael, Meilland, Julie, Jonkers, Lukas, Quillévéré, Frédéric, Escarguel, Gilles, Douady, Christophe, de Garidel-Thoron, Thibault, de Vargas, Colomban, Kucera, Michal
• Other Authors: Center for Marine Environmental Sciences Bremen (MARUM), Universität Bremen, School of Geosciences Edinburgh, University of Edinburgh (Edin.), Biological and Environmental Sciences Stirling, University of Stirling, Norwegian Research Center (NORCE), Biological Oceanography, Leibniz Institute for Baltic Sea Research Warnemünde (IOW), Fédération de recherche de Roscoff (FR2424), Station biologique de Roscoff = Roscoff Marine Station (SBR), Sorbonne Université (SU)-Centre National de la Recherche Scientifique (CNRS)-Sorbonne Université (SU)-Centre National de la Recherche Scientifique (CNRS), Global Oceans Systems Ecology & Evolution - Tara Oceans (GOSEE), Université de Perpignan Via Domitia (UPVD)-École Pratique des Hautes Études (EPHE), Université Paris Sciences et Lettres (PSL)-Université Paris Sciences et Lettres (PSL)-Aix Marseille Université (AMU)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université d'Évry-Val-d'Essonne (UEVE)-Université de Toulon (UTLN)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Sorbonne Université (SU)-Université Paris-Saclay-Centre National de la Recherche Scientifique (CNRS)-Université Grenoble Alpes 2016-2019 (UGA 2016-2019 )-Institut de Recherche pour le Développement (IRD France-Nord )-Ecole Normale Supérieure Paris-Saclay (ENS Paris Saclay)-European Molecular Biology Laboratory (EMBL)-NANTES UNIVERSITÉ - École Centrale de Nantes (Nantes Univ - ECN), Nantes Université (Nantes Univ)-Nantes Université (Nantes Univ)-Université australe du Chili, Institute of Marine Sciences / Institut de Ciències del Mar Barcelona (ICM), Consejo Superior de Investigaciones Cientificas España = Spanish National Research Council Spain (CSIC), Max Planck Institute for Marine Microbiology, Max-Planck-Gesellschaft, Laboratoire de Géologie de Lyon - Terre, Planètes, Environnement (LGL-TPE), École normale supérieure de Lyon (ENS de Lyon)-Université Claude Bernard Lyon 1 (UCBL), Université de Lyon-Université de Lyon-Institut national des sciences de l'Univers (INSU - CNRS)-Université Jean Monnet - Saint-Étienne (UJM)-Centre National de la Recherche Scientifique (CNRS), Équipe 6 - Paléontologie, Paléoécologie, Paléobiogéographie, Évolution (P3E), Laboratoire d'Ecologie des Hydrosystèmes Naturels et Anthropisés (LEHNA), Université Claude Bernard Lyon 1 (UCBL), Université de Lyon-Université de Lyon-École Nationale des Travaux Publics de l'État (ENTPE)-Centre National de la Recherche Scientifique (CNRS)-Université Claude Bernard Lyon 1 (UCBL), Université de Lyon-Université de Lyon-École Nationale des Travaux Publics de l'État (ENTPE)-Centre National de la Recherche Scientifique (CNRS), Équipe 3 - Écologie, Évolution, Écosystemes Souterrains (E3S), Institut universitaire de France (IUF), Ministère de l'Education nationale, de l’Enseignement supérieur et de la Recherche (M.E.N.E.S.R.), Centre Européen de Recherche et d'Enseignement des Géosciences de l'Environnement (CEREGE), Institut de Recherche pour le Développement (IRD)-Aix Marseille Université (AMU)-Collège de France (CdF (institution))-Institut national des sciences de l'Univers (INSU - CNRS)-Centre National de la Recherche Scientifique (CNRS)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), Adaptation et diversité en milieu marin (AD2M), Station biologique de Roscoff Roscoff (SBR), Université Pierre et Marie Curie - Paris 6 (UPMC)-Centre National de la Recherche Scientifique (CNRS)-Université Pierre et Marie Curie - Paris 6 (UPMC)-Centre National de la Recherche Scientifique (CNRS)-Centre National de la Recherche Scientifique (CNRS)
• Format: Article in Journal/Newspaper
• Language: English
• Published: HAL CCSD 2024
• Subjects: protists; planktonic foraminifera; cryptic diversity; molecular taxonomy; automated delimitation; barcoding; metabarcoding; ecology; biogeography; biodiversity; [SDE]Environmental Sciences; Planktonic foraminifera
• Online Access: https://univ-lyon1.hal.science/hal-04552961; https://doi.org/10.1111/brv.13065

International audience 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 ...