The cryptic and the apparent reversed: lack of genetic differentiation within the morphologically diverse plexus of the planktonic foraminifer <i>Globigerinoides sacculifer</i>

André, Aurore; Weiner, Agnes; Quillévéré, Frédéric; Aurahs, Ralf; Morard, Raphaël; Douady, Christophe J.; Garidel‐Thoron, Thibault de; Escarguel, Gilles; Vargas, Colomban de; Kučera, Michal

doi:10.1666/0094-8373-39.1.21

Cited by 90 publications

(84 citation statements)

References 64 publications

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“…Our results are in stark contrast to the numerous recent studies on protists showing cases of cryptic genetic diversity, where genetic divergence is not reflected in morphological differentiation (for example, Coleman, 2001). We have only found one other similar study in which four marine foraminifera morphospecies were shown to be virtually identical by SSU rDNA and ITS-1 DNA markers (André et al, 2013).…”

Section: Discussioncontrasting

confidence: 99%

Recent radiation in a marine and freshwater dinoflagellate species flock

et al. 2015

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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.

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Section: Discussioncontrasting

confidence: 99%

Recent radiation in a marine and freshwater dinoflagellate species flock

et al. 2015

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“…Each morphospecies is distinguishable by its chamber arrangement, growth ratio of chambers, and shape of the last chamber. Surprisingly, however, G. sacculifer has only one genotype, and there is no relationship between the morphologic divergence and genetics (André et al 2013). From the viewpoint of molecular phylogeny, this suggests a delimitation of classification based on tradi-tional morphology.…”

Section: Reassessment Of Shell Morphologymentioning

confidence: 97%

“…Globigerinoides sacculifer, a tropical species, has various morphologic types in the world ocean. André et al (2013) carried out a world survey of two ribosomal DNA regions (SSU and ITS-1) in different morphotypes of G. sacculifer, including G. trilobus, G. immaturus, G. quadrilobatus, and typical G. sacculifer itself.…”

Section: Reassessment Of Shell Morphologymentioning

confidence: 99%

Planktic Foraminifera

Kimoto

2015

Marine Protists

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Planktic foraminifera are single-celled marine eukaryotes characterized by having calcareous shells. They are holoplankton with 40-50 identified species in the world ocean. Their biology, diversity, and shell chemistry are sensitive to changes in the oceanic environment, and therefore their carbonate shells are useful climatic tracers of temperature, water mass, and other chemical indicators of global change. Production of carbonate shells plays an important role in marine biogeochemical cycles involving carbon and is closely related to the Earth's climate systems. Geochemical studies combined with culture experiments using planktic foraminifera provide much useful information about future biological and climatic responses on Earth. Molecular biology based on DNA has become a major tool for all ecological, biological, and evolutional studies of foraminifera. Molecular phylogenic analyses have revealed that morphologic classification of the planktic foraminifera resulted in underestimation of their biodiversity.

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“…Preservation in ethanol, a hypothetical third option commonly used for metazoans, is not recommended for foraminifera as it inhibits the amplification of DNA by PCR (Holzmann and Pawlowski, 1996;Lecroq, 2014). Drying and freezing has been used preferably in the last years, since it allows faster handling of foraminiferal specimens (André et al, 2013;Weiner et al, 2014Weiner et al, , 2015. A considerably larger number of specimens can be preserved using this method, as it does not involve individual selection and placement in microtubes immediately after sampling.…”

Section: Preservation Of Specimensmentioning

confidence: 99%

“…Using the small subunit ribosomal RNA gene (SSU rDNA) as a marker, hidden genetic diversity was discovered within established morphospecies (Huber et al, 1997;de Vargas et al, 1999). This triggered a series of subsequent studies that screened morphospecies for their cryptic diversity (e.g., Darling et al, 1999;de Vargas et al, 1999;Aurahs et al, 2009a;Morard et al, 2009Morard et al, , 2011Weiner et al, 2012Weiner et al, , 2014André et al, 2013).…”

Section: Introductionmentioning

confidence: 99%

Methodology for Single-Cell Genetic Analysis of Planktonic Foraminifera for Studies of Protist Diversity and Evolution

et al. 2016

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Single-cell genetic analysis is an essential method to investigate the biodiversity and evolutionary ecology of marine protists. In protist groups that do not reproduce under laboratory conditions, this approach provides the only means to directly associate molecular sequences with cell morphology. The resulting unambiguous taxonomic identification of the DNA sequences is a prerequisite for barcoding and analyses of environmental metagenomic data. Extensive single-cell genetic studies have been carried out on planktonic foraminifera over the past 20 years to elucidate their phylogeny, cryptic diversity, biogeography, and the relationship between genetic and morphological variability. In the course of these investigations, it has become evident that genetic analysis at the individual specimen level is confronted by innumerable challenges ranging from the negligible amount of DNA present in the single cell to the substantial amount of DNA contamination introduced by endosymbionts or food particles. Consequently, a range of methods has been developed and applied throughout the years for the genetic analysis of planktonic foraminifera in order to enhance DNA amplification success rates. Yet, the description of these methods in the literature rarely occurred with equivalent levels of detail and the different approaches have never been compared in terms of their efficiency and reproducibility. Here, aiming at a standardization of methods, we provide a comprehensive review of all methods that have been employed for the single-cell genetic analysis of planktonic foraminifera. We compile data on success rates of DNA amplification and use these to evaluate the effects of key parameters associated with the methods of sample collection, storage and extraction of single-cell DNA. We show that the chosen methods influence the success rates of single-cell genetic studies, but the differences between them are not sufficient to hinder comparisons Weiner et al.Single-Cell Genetic Analysis of Foraminifera between studies carried out by different methods. The review thus not only provides a comprehensive reference with guidelines for future genetic studies on foraminifera, but it also establishes an important benchmark for investigations using existing single-cell datasets. The methods are widely applicable and the review may help to establish similar standard principles for their utilization in other protist groups.

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The cryptic and the apparent reversed: lack of genetic differentiation within the morphologically diverse plexus of the planktonic foraminifer Globigerinoides sacculifer

Cited by 90 publications

References 64 publications

Recent radiation in a marine and freshwater dinoflagellate species flock

Recent radiation in a marine and freshwater dinoflagellate species flock

Planktic Foraminifera

Methodology for Single-Cell Genetic Analysis of Planktonic Foraminifera for Studies of Protist Diversity and Evolution

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