Abstract
Processes of rapid radiation among unicellular eukaryotes are much less studied than among multicellular organisms. We have investigated a lineage of cold-water microeukaryotes (protists) that appear to have diverged recently. This lineage stands in stark contrast to known examples of phylogenetically closely related protists, in which genetic difference is typically larger than morphological differences. We found that the group not only consists of the marine-brackish dinoflagellate species Scrippsiella hangoei and the freshwater species Peridinium aciculiferum as discovered previously but also of a whole species flock. The additional species include Peridinium euryceps and Peridinium baicalense, which are restricted to a few lakes, in particular to the ancient Lake Baikal, Russia, and freshwater S. hangoei from Lake Baikal. These species are characterized by relatively large conspicuous morphological differences, which have given rise to the different species descriptions. However, our scanning electron microscopic studies indicate that they belong to a single genus according to traditional morphological characterization of dinoflagellates (thecal plate patterns). Moreover, we found that they have identical SSU (small subunit) rDNA fragments and distinct but very small differences in the DNA markers LSU (large subunit) rDNA, ITS2 (internal transcribed spacer 2) and COB (cytochrome b) gene, which are used to delineate dinoflagellates species. As some of the species co-occur, and all four have small but species–specific sequence differences, we suggest that these taxa are not a case of phenotypic plasticity but originated via recent adaptive radiation. We propose that this is the first clear example among free-living microeukaryotes of recent rapid diversification into several species followed by dispersion to environments with different ecological conditions.
Similar content being viewed by others
Log in or create a free account to read this content
Gain free access to this article, as well as selected content from this journal and more on nature.com
or
References
Alverson AJ, Jansen RK, Theriot EC . (2007). Bridging the Rubicon: phylogenetic analysis reveals repeated colonizations of marine and fresh waters by thalassiosiroid diatoms. Mol Phyl Evol 45: 193–210.
André A, Weiner A, Quillévéré F, Aurahs R, Morard R, Douady CJ et al. (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.
Anisimova M, Gascuel O . (2006). Approximate likelihood ratio test for branches: a fast, accurate and powerful alternative. Syst Biol 55: 539–552.
Annenkova NV . (2013). Phylogenetic relations of the dinoflagellate Gymnodinium baicalense from Lake Baikal. CEJB 8: 366–373.
Annenkova NV, Belikov SI . (2010). Detection of the dinoflagellates which are phylogenetically close to Pfiesteriaceae family in Baikal Lake. Water Chem Ecol 11: 40–46.
Annenkova NV, Lavrov DV, Belikov SI . (2011). Dinoflagellates associated with freshwater sponges from the ancient Lake Baikal. Protist 162: 222–236.
Bråte J, Logares R, Berney C, Ree DK, Klaveness D, Jakobsen KS et al. (2010). Freshwater Perkinsea and marine-freshwater colonizations revealed by pyrosequencing and phylogeny of environmental rDNA. ISME J 4: 1144–1153.
Calado AJ, Craveiro SC, Daugbjerg N, Moestrup Ø . (2009). Description of Tyrannodinium gen. nov., a freshwater dinoflagellate closely related to the marine Pfiesteria-like species. J Phycol 45: 1195–1205.
Coleman AW . (2001). Biogeography and speciation in the Pandorina/Volvulina (Chlorophyta) superclade. J Phycol 37: 836–851.
Coleman AW . (2009). Is there a molecular key to the level of ‘‘biological species” in eukaryotes? A DNA guide. Mol Phyl Evol 50: 197–203.
Criscuolo A . (2011). morePhyML: Improving the phylogenetic tree space exploration with PhyML 3. Mol Phyl Evol 61: 944–948.
Darriba D, Taboada GL, Doallo R, Posada D . (2012). jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9: 772.
Daugbjerg N, Hansen G, Larsen J, Moestrup Ø . (2000). Phylogeny of some of the major genera of dinoflagellates based on ultrastructure and partial LSU rDNA sequence data, including the erection of three new genera of unarmoured dinoflagellates. Phycologia 39: 302–317.
Dolph S . (2000) The Ecology of Adaptive Radiation. Oxford University Press: Oxford, UK.
Dorogostaysky V . (1923). Vertical and horizontal distribution of Lake Baikal fauna. Proc Irkutsk State Univ Irkutsk 4: 103–130.
Ekman P, Fries M . (1970). Studies of sedimental from Lake Erken, eastern central Sweden. Geol För Stockh Förh 92: 214–224.
Fensome RA, Taylor FJR, Norris G, Sarjeant WAS, Wharton DI, Williams GL . (1993). A classification of living and fossil dinoflagellates. Micropaleontology 7. Sheridan Press: Hanover, Pennsylvania, USA.
Gavrilets S, Losos JB . (2009). Adaptive rRadiation: contrasting theory with data. Science 323: 732–737.
Gelman A, Rubin DB . (1992). Inference from interative simulation using multiple sequences. Stat Sci 7: 457–511.
Gómez P, Buckling A . (2013). Real-time microbial adaptive diversification in soil. Ecol Lett 16: 650–655.
Gottschling M, Soehner S, Zinssmeister C, John U, Plötner J, Schweikert M et al. (2012). Delimitation of the Thoracosphaeraceae (Dinophyceae), including the calcareous dinoflagellates, based on large amounts of ribosomal RNA sequence data. Protist 163: 15–24.
Grant PR, Grant BR . (2011) How and Why Species Multiply: the Radiation of Darwin's Finches. Princeton University Press: Princeton, NJ, USA.
Greenwood PH . (1984). What is a species flock? In: Echelle AA, Kornfield I, (eds). Evolution of Fish Species Flocks. Univ. Maine at Orono Press: Orono, Maine, USA, pp 13–19.
Hall TA . (1999). BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp 4: 95–98.
Hansen G, Flaim G . (2007). Dinoflagellates of the Trentino Province, Italy. Limnol 66: 107–141.
Harington CR . (2008). The evolution of arctic marine mammals. Ecol Appl 18: S23–S40.
Hunt DE, David LA, Gevers D, Preheim SP, Alm EJ, Polz MF . (2008). Resource partitioning and sympatric differentiation among closely related bacterioplankton. Science 320: 1081–1085.
Jones FC, Grabherr MG, Chan YF, Russell P, Mauceli E, Johnson J et al. (2012). The genomic basis of adaptive evolution in threespine sticklebacks. Nature 484: 55–61.
Kalff J . (2002) Limnology: Inland Water Ecosystems. Prentice-Hall: Upper Saddle River, NJ, USA.
Karabanov EV, Prokopenko AA, Williams DF, Khursevich GK . (2000). A new record of Holocene climate change from the bottom sediments of Lake Baikal. Paleogeogr Paleoecol 156: 211–224.
Kasuga T, White TJ, Koenig G, Mcewen J, Restrepo A, Castañeda E et al. (2003). Phylogeography of the fungal pathogen Histoplasma capsulatum. Mol Ecol 12: 3383–3401.
Katoh K, Toh H . (2010). Parallelization of the MAFFT multiple sequence alignment program. Bioinformatics 26: 1899–1900.
Khursevich GK, Karabanov EB, Prokopenko AA, Williams D, Kuzmin M, Fedenia S et al. (2001). Detailed diatom stratigraphy of Lake Baikal sediments in the Bryunes Epoch and climatic factors of speciation. Geol Geofiz 42: 108–129.
Kisselew JA, Zwetkow WN . (1935). Zur Morphologie und Ökologie von Peridinium baicalense n. sp. Beih Bot Centralbl 53: 518–524.
Kozhova OM, Izmest'eva LR (eds).. (1998) Lake Baikal: Evolution and Biodiversity. Backhuys Publications: Leiden, The Netherlands.
LaJeunesse TC . (2005). ‘Species’ radiations of symbiotic dinoflagellates in the Atlantic and Indo-Pacific since the Miocene-Pliocene transition. Mol Biol Evol 22: 570–581.
Larsen J, Kuosa H, Ikävalko J, Kivi K, Hällfors S . (1995). A redescription of Scrippsiella hangoei (Schiller) comb. nov—a red tide dinoflagellate from the Northern Baltic. Phycologia 34: 135–144.
Lin S, Zhang H, Hou Y, Zhuang Y, Miranda L . (2009). High-level diversity of dinoflagellates in the natural environment, revealed by assessment of mitochondrial cox1 and cob genes for dinoflagellate DNA barcoding. Appl Environ Microbiol 75: 1279–1290.
Litaker RW, Vandersea MW, Kibler SR, Reece KS, Stokes NA, Lutzoni FM et al. (2007). Recognizing dinoflagellate species using its rDNA sequences. J Phycol 43: 344–355.
Logares R, Bråte J, Bertilsson S, Clasen JL, Shalchian-Tabrizi K, Rengefors K . (2009). Infrequent marine-freshwater transitions in the microbial world. Trends Microbiol 17: 414–422.
Logares R, Daugbjerg N, Boltovskoy A, Kremp A, Laybourn-Parry J, Rengefors K . (2008). Recent evolutionary diversification of a protist lineage. Environ Microbiol 10: 1231–1243.
Logares R, Rengefors K, Kremp A, Shalchian-Tabrizi K, Boltovskoy A, Tengs T et al. (2007a). Phenotypically different microalgal morphospecies with identical ribosomal DNA: a case of rapid adaptive evolution? Microb Ecol 53: 549–561.
Logares R, Shalchian-Tabrizi K, Boltovskoy A, Rengefors K . (2007b). Extensive dinoflagellate phylogenies indicate infrequent marine-freshwater transitions. Mol Phyl Evol 45: 887–903.
Lozupone C, Hamady M, Knight R . (2006). UniFrac—an online tool for comparing microbial community diversity in a phylogenetic Context. BMC Bioinformatics 7: 371.
MacLean RC . (2005). Adaptive radiation in microbial microcosms. J Evol Biol 18: 1376–1384.
Martiny JBH, Bohannan BJM, Brown JH, Colwell RK, Fuhrman JA, Green JL et al. (2006). Microbial biogeography: putting microorganisms on the map. Nat Rev Microbiol 4: 102–112.
Mats VD, Sherbakov DYu, Efimova IM . (2011). Late Cretaceous-Cenozoic history of Lake Baikal depression and formztion of the unique biodiversity. Stratigr Geol Correl 19: 404–423.
Montresor M, Sgrosso S, Procaccini G, Kooistra WHCF . (2003). Intraspecific diversity in Scrippsiella trochoidea (Dinophyceae): evidence for cryptic species. Phycologia 42: 56–70.
Pfennig DW, Wund MA, Snell-Rood EC, Cruickshank T, Schlichting CD, Moczek AP . (2010). Phenotypic plasticity's impacts on diversification and speciation. Trends Ecol Evol 25: 459–467.
Popovskaya GI . (1991). Phytoplankton of Lake Baikal and its long-term changes (1958–1990). PhD thesis. Academy of Sciences, Siberian Branch, Central Siberian Botanical Garden, Novosibirsk, Russia.
Rengefors K, Anderson DM . (1998). Environmental and endogenous regulation of cyst germination in two fresh-water dinoflagellates. J Phycol 34: 568–577.
Rengefors K, Laybourn-Parry J, Logares R, Marshall WA, Hansen G . (2008). Marine-derived dinoflagellates in Antarctic saline lakes: community composition and annual dynamics. J Phycol 44: 592–604.
Rengefors K, Meyer B . (1998). Peridinium euryceps sp. nov. (Peridiniales, Dinophyceae), a cryophilic dinoflagellate from Lake Erken, Sweden. Phycologia 37: 284–291.
Ronquist F, Huelsenbeck JP . (2003). MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572–1574.
Schluter D . (2000) The Ecology of Adaptive Radiation. Oxford University Press: Oxford, UK.
Schön I, Martens K . (2004). Adaptive, pre-adaptive and non-adaptive components of radiations in ancient lakes: a review. Org Divers Evol 4: 137–156.
Seehausen O . (2006). African cichlid fish: a model system in adaptive radiation research. Proc R Soc B 273: 1987–1998.
Sherbakov DYu . (1999). Molecular phylogenetic studies on the origin of biodiversity in Lake Baikal. Trends Ecol Evol 14: 92–94.
Steidinger KA, Tangen K . (1997). Dinofllagellates. In: Tomas C, (ed). Identifying Marine Phytoplankton. Academic Press: San Diego, CA, USA, 1387–1584.
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.
Tanichev AI, Bondarenko NA . (1995). Free-living flagellates. In Timoshkin OA, (ed). The Atlas and Index of Pelagiobionts of Baikal. Nauka: Novosibirsk, Russia.
Timoshkin OA . (1999). Biology of Lake Baikal: “White spots” and progress in research. Berliner Geowiss Abh E 30: 333–348.
Wilke T, Benke M, Brändle M, Albrecht C, Bichain J-M . (2010). The neglected side of the coin: non-adaptive radiations in spring snails (Bythinella spp.). In: Glaubrecht M, (ed). Evolution in Action. Case studies in Adaptive Radiation, Speciation and the Origin of Biodiversity. Springer: Dordrecht, The Netherlands, pp 551–578.
Wolf M, Friedrich J, Dandekar T, Müller T . (2005). CBCAnalyzer: inferring phylogenies based on compensatory base changes in RNA secondary structures. In Silico Biol 5: 291–294.
Zhang H, Bhattacharya D, Lin S . (2005). Phylogeny of dinoflagellates based on mitochondrial cytochrome b and nuclear small subunit rDNA sequence comparisons. J Phycol 41: 411–420.
Zirbel MJ, Veron F, Latz MI . (2000). The reversible effect of flow on the morphology of Ceratocorys horrida (Peridiniales, Dinophyta). J Phycol 36: 46–58.
Acknowledgements
Financial support for this work was provided by The Swedish Research Council grant 621-2009-5324 to KR, a Swedish Institute Scholarship to NA and Project no. 12-04-31802-mol_a of the Russian Foundation for Basic Research to NA. We thank the Institute for System Dynamics and Control Theory SB RAS for providing access to the mvs-1000/16 cluster. We are grateful to I Khanaev and I Tomberg for their help in sample collection. Special thanks to NV Annenkova’s family for their help during expeditions and constructive suggestions on an earlier version of the article by the Plankton Ecology Group at the Aquatic Ecology Unit, Department of Biology, Lund University, Lund, Sweden. Several anonymous reviewers are thanked for their help in improving earlier versions of the manuscript.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Competing interests
The authors declare no conflict of interest.
Additional information
Supplementary Information accompanies this paper on The ISME Journal website
Rights and permissions
About this article
Cite this article
Annenkova, N., Hansen, G., Moestrup, Ø. et al. Recent radiation in a marine and freshwater dinoflagellate species flock. ISME J 9, 1821–1834 (2015). https://doi.org/10.1038/ismej.2014.267
Received:
Revised:
Accepted:
Published:
Issue date:
DOI: https://doi.org/10.1038/ismej.2014.267
This article is cited by
-
Population genomic analyses reveal that salinity and geographic isolation drive diversification in a free-living protist
Scientific Reports (2024)
-
Bumps on the back: An unusual morphology in phylogenetically distinct Peridinium aff. cinctum (= Peridinium tuberosum; Peridiniales, Dinophyceae)
Organisms Diversity & Evolution (2024)
-
Global patterns and rates of habitat transitions across the eukaryotic tree of life
Nature Ecology & Evolution (2022)
