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Article ; Online: Macroevolutionary patterns in intragenomic rDNA variability among planktonic foraminifera.

Greco, Mattia / Morard, Raphaël / Darling, Kate / Kucera, Michal

2023 Volume 11, Page(s) e15255

Abstract: Ribosomal intragenomic variability in prokaryotes and eukaryotes is a genomic feature commonly studied for its inflationary impact on molecular diversity assessments. However, the evolutionary mechanisms and distribution of this phenomenon within a ... ...

Abstract	Ribosomal intragenomic variability in prokaryotes and eukaryotes is a genomic feature commonly studied for its inflationary impact on molecular diversity assessments. However, the evolutionary mechanisms and distribution of this phenomenon within a microbial group are rarely explored. Here, we investigate the intragenomic variability in 33 species of planktonic foraminifera, calcifying marine protists, by inspecting 2,403 partial SSU sequences obtained from single-cell clone libraries. Our analyses show that polymorphisms are common among planktonic foraminifera species, but the number of polymorphic sites significantly differs among clades. With our molecular simulations, we could assess that most of these mutations are located in paired regions that do not affect the secondary structure of the SSU fragment. Finally, by mapping the number of polymorphic sites on the phylogeny of the clades, we were able to discuss the evolution and potential sources of intragenomic variability in planktonic foraminifera, linking this trait to the distinctive nuclear and genomic dynamics of this microbial group.
MeSH term(s)	Foraminifera/genetics ; DNA, Ribosomal/chemistry ; Plankton/genetics ; Phylogeny ; Eukaryota/genetics
Chemical Substances	DNA, Ribosomal
Language	English
Publishing date	2023-04-25
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2703241-3
ISSN	2167-8359 ; 2167-8359
ISSN (online)	2167-8359
ISSN	2167-8359
DOI	10.7717/peerj.15255
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Article ; Online: The global genetic diversity of planktonic foraminifera reveals the structure of cryptic speciation in plankton.

Biological reviews of the Cambridge Philosophical Society

2024

Abstract: 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 ... ...

Abstract	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.
Language	English
Publishing date	2024-02-13
Publishing country	England
Document type	Journal Article
ZDB-ID	1423558-4
ISSN	1469-185X ; 0006-3231 ; 1464-7931
ISSN (online)	1469-185X
ISSN	0006-3231 ; 1464-7931
DOI	10.1111/brv.13065
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Article ; Online: Ecological partitioning and diversity in tropical planktonic foraminifera

Seears Heidi A / Darling Kate F / Wade Christopher M

BMC Evolutionary Biology, Vol 12, Iss 1, p

2012 Volume 54

Abstract: Abstract Background Ecological processes are increasingly being viewed as an important mode of diversification in the marine environment, where the high dispersal potential of pelagic organisms, and a lack of absolute barriers to gene flow may limit the ... ...

Abstract	Abstract Background Ecological processes are increasingly being viewed as an important mode of diversification in the marine environment, where the high dispersal potential of pelagic organisms, and a lack of absolute barriers to gene flow may limit the occurrence of allopatric speciation through vicariance. Here we focus on the potential role of ecological partitioning in the diversification of a widely distributed group of marine protists, the planktonic foraminifera. Sampling was conducted in the tropical Arabian Sea, during the southwest (summer) monsoon, when pronounced environmental conditions result in a strong disparity in temperature, salinity and productivity between distinct northern and southern water masses. Results We uncovered extensive genetic diversity within the Arabian Sea planktonic foraminifera, identifying 13 morphospecies, represented by 20 distinct SSU rRNA genetic types. Several morphospecies/genetic types displayed non-random biogeographical distributions, partitioning between the northern and southern water masses, giving a strong indication of independent ecological adaptations. Conclusions We propose sea-surface primary productivity as the main factor driving the geographical segregation of Arabian Sea planktonic foraminifera, during the SW monsoon, with variations in symbiotic associations possibly playing a role in the specific ecological adaptations observed. Our findings suggest that ecological partitioning could be contributing to the high levels of 'cryptic' genetic diversity observed within the planktonic foraminifera, and support the view that ecological processes may play a key role in the diversification of marine pelagic organisms.
Keywords	Biology (General) ; QH301-705.5 ; Science ; Q ; DOAJ:Biology ; DOAJ:Biology and Life Sciences ; Evolution ; QH359-425
Subject code	333
Language	English
Publishing date	2012-04-01T00:00:00Z
Publisher	BioMed Central
Document type	Article ; Online
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Article ; Online: Ecological partitioning and diversity in tropical planktonic foraminifera.

Seears, Heidi A / Darling, Kate F / Wade, Christopher M

BMC evolutionary biology

2012 Volume 12, Page(s) 54

Abstract: Background: Ecological processes are increasingly being viewed as an important mode of diversification in the marine environment, where the high dispersal potential of pelagic organisms, and a lack of absolute barriers to gene flow may limit the ... ...

Abstract	Background: Ecological processes are increasingly being viewed as an important mode of diversification in the marine environment, where the high dispersal potential of pelagic organisms, and a lack of absolute barriers to gene flow may limit the occurrence of allopatric speciation through vicariance. Here we focus on the potential role of ecological partitioning in the diversification of a widely distributed group of marine protists, the planktonic foraminifera. Sampling was conducted in the tropical Arabian Sea, during the southwest (summer) monsoon, when pronounced environmental conditions result in a strong disparity in temperature, salinity and productivity between distinct northern and southern water masses. Results: We uncovered extensive genetic diversity within the Arabian Sea planktonic foraminifera, identifying 13 morphospecies, represented by 20 distinct SSU rRNA genetic types. Several morphospecies/genetic types displayed non-random biogeographical distributions, partitioning between the northern and southern water masses, giving a strong indication of independent ecological adaptations. Conclusions: We propose sea-surface primary productivity as the main factor driving the geographical segregation of Arabian Sea planktonic foraminifera, during the SW monsoon, with variations in symbiotic associations possibly playing a role in the specific ecological adaptations observed. Our findings suggest that ecological partitioning could be contributing to the high levels of 'cryptic' genetic diversity observed within the planktonic foraminifera, and support the view that ecological processes may play a key role in the diversification of marine pelagic organisms.
MeSH term(s)	Adaptation, Physiological ; Bayes Theorem ; Environment ; Foraminifera/genetics ; Genetic Variation ; Genotype ; Geography ; Oceans and Seas ; Phylogeny ; Plankton/genetics ; RNA, Ribosomal/genetics ; Seasons ; Sequence Analysis, DNA
Chemical Substances	RNA, Ribosomal
Language	English
Publishing date	2012-04-16
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2041493-6
ISSN	1471-2148 ; 1471-2148
ISSN (online)	1471-2148
ISSN	1471-2148
DOI	10.1186/1471-2148-12-54
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Article ; Online: A New Integrated Approach to Taxonomy: The Fusion of Molecular and Morphological Systematics with Type Material in Benthic Foraminifera.

Roberts, Angela / Austin, William / Evans, Katharine / Bird, Clare / Schweizer, Magali / Darling, Kate

PloS one

2016 Volume 11, Issue 7, Page(s) e0158754

Abstract: A robust and consistent taxonomy underpins the use of fossil material in palaeoenvironmental research and long-term assessment of biodiversity. This study presents a new integrated taxonomic protocol for benthic foraminifera by unequivocally reconciling ... ...

Abstract	A robust and consistent taxonomy underpins the use of fossil material in palaeoenvironmental research and long-term assessment of biodiversity. This study presents a new integrated taxonomic protocol for benthic foraminifera by unequivocally reconciling the traditional taxonomic name to a specific genetic type. To implement this protocol, a fragment of the small subunit ribosomal RNA (SSU rRNA) gene is used in combination with 16 quantitative morphometric variables to fully characterise the benthic foraminiferal species concept of Elphidium williamsoni Haynes, 1973. A combination of live contemporary topotypic specimens, original type specimens and specimens of genetic outliers were utilised in this study. Through a series of multivariate statistical tests we illustrate that genetically characterised topotype specimens are morphologically congruent with both the holotype and paratype specimens of E. williamsoni Haynes, 1973. We present the first clear link between morphologically characterised type material and the unique SSU rRNA genetic type of E. williamsoni. This example provides a standard framework for the benthic foraminifera which bridges the current discontinuity between molecular and morphological lines of evidence, allowing integration with the traditional Linnaean roots of nomenclature to offer a new prospect for taxonomic stability.
MeSH term(s)	Atlantic Ocean ; Biodiversity ; Classification ; DNA, Protozoan/genetics ; DNA, Ribosomal/genetics ; Foraminifera/classification ; Fossils ; Geography ; Microscopy, Electron, Scanning ; Multivariate Analysis ; Paleontology/methods ; Phylogeny ; Principal Component Analysis ; RNA, Ribosomal/analysis ; Ribosome Subunits, Small
Chemical Substances	DNA, Protozoan ; DNA, Ribosomal ; RNA, Ribosomal
Language	English
Publishing date	2016-07-07
Publishing country	United States
Document type	Journal Article
ZDB-ID	2267670-3
ISSN	1932-6203 ; 1932-6203
ISSN (online)	1932-6203
ISSN	1932-6203
DOI	10.1371/journal.pone.0158754
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Article ; Online: 16S rRNA gene metabarcoding and TEM reveals different ecological strategies within the genus Neogloboquadrina (planktonic foraminifer).

Bird, Clare / Darling, Kate F / Russell, Ann D / Fehrenbacher, Jennifer S / Davis, Catherine V / Free, Andrew / Ngwenya, Bryne T

PloS one

2018 Volume 13, Issue 1, Page(s) e0191653

Abstract: Uncovering the complexities of trophic and metabolic interactions among microorganisms is essential for the understanding of marine biogeochemical cycling and modelling climate-driven ecosystem shifts. High-throughput DNA sequencing methods provide ... ...

Abstract	Uncovering the complexities of trophic and metabolic interactions among microorganisms is essential for the understanding of marine biogeochemical cycling and modelling climate-driven ecosystem shifts. High-throughput DNA sequencing methods provide valuable tools for examining these complex interactions, although this remains challenging, as many microorganisms are difficult to isolate, identify and culture. We use two species of planktonic foraminifera from the climatically susceptible, palaeoceanographically important genus Neogloboquadrina, as ideal test microorganisms for the application of 16S rRNA gene metabarcoding. Neogloboquadrina dutertrei and Neogloboquadrina incompta were collected from the California Current and subjected to either 16S rRNA gene metabarcoding, fluorescence microscopy, or transmission electron microscopy (TEM) to investigate their species-specific trophic interactions and potential symbiotic associations. 53-99% of 16S rRNA gene sequences recovered from two specimens of N. dutertrei were assigned to a single operational taxonomic unit (OTU) from a chloroplast of the phylum Stramenopile. TEM observations confirmed the presence of numerous intact coccoid algae within the host cell, consistent with algal symbionts. Based on sequence data and observed ultrastructure, we taxonomically assign the putative algal symbionts to Pelagophyceae and not Chrysophyceae, as previously reported in this species. In addition, our data shows that N. dutertrei feeds on protists within particulate organic matter (POM), but not on bacteria as a major food source. In total contrast, of OTUs recovered from three N. incompta specimens, 83-95% were assigned to bacterial classes Alteromonadales and Vibrionales of the order Gammaproteobacteria. TEM demonstrates that these bacteria are a food source, not putative symbionts. Contrary to the current view that non-spinose foraminifera are predominantly herbivorous, neither N. dutertrei nor N. incompta contained significant numbers of phytoplankton OTUs. We present an alternative view of their trophic interactions and discuss these results within the context of modelling global planktonic foraminiferal abundances in response to high-latitude climate change.
MeSH term(s)	DNA Barcoding, Taxonomic ; Microscopy, Electron, Transmission ; RNA, Ribosomal, 16S/genetics ; Rhizaria/genetics
Chemical Substances	RNA, Ribosomal, 16S
Language	English
Publishing date	2018
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ISSN	1932-6203
ISSN (online)	1932-6203
DOI	10.1371/journal.pone.0191653
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Book ; Online: Assessing proxy signatures of temperature, salinity, and hypoxia in the Baltic Sea through foraminifera-based geochemistry and faunal assemblages

Groeneveld, Jeroen / Filipsson, Helena L. / Austin, William E. N. / Darling, Kate / McCarthy, David / Quintana Krupinski, Nadine B. / Bird, Clare / Schweizer, Magali

eISSN: 2041-4978

2019

Abstract: Current climate and environmental changes strongly affect shallow marine and coastal areas like the Baltic Sea. This has created a need for a context to understand the severity and potential outcomes of such changes. The context can be derived from ... ...

Abstract	Current climate and environmental changes strongly affect shallow marine and coastal areas like the Baltic Sea. This has created a need for a context to understand the severity and potential outcomes of such changes. The context can be derived from paleoenvironmental records during periods when comparable events happened in the past. In this study, we explore how varying bottom water conditions across a large hydrographic gradient in the Baltic Sea affect benthic foraminiferal faunal assemblages and the geochemical composition of their calcite tests. We have conducted both morphological and molecular analyses of the faunas and we evaluate how the chemical signatures of the bottom waters are recorded in the tests of several species of benthic foraminifera. We focus on two locations, one in the Kattegat (western Baltic Sea) and one in Hanö Bay (southern Baltic Sea). We show that seawater Mn∕Ca , Mg∕Ca , and Ba∕Ca ( Mn∕Ca sw , Mg∕Ca sw , and Ba∕Ca sw ) variations are mainly controlled by dissolved oxygen concentration and salinity. Their respective imprints on the foraminiferal calcite demonstrate the potential of Mn∕Ca as a proxy for hypoxic conditions, and Ba∕Ca as a proxy for salinity in enclosed basins such as the Baltic Sea. The traditional use of Mg∕Ca as a proxy to reconstruct past seawater temperatures is not recommended in the region, as it may be overprinted by the large variations in salinity (specifically on Bulimina marginata ), Mg∕Ca sw , and possibly also the carbonate system. Salinity is the main factor controlling the faunal assemblages: a much more diverse fauna occurs in the higher-salinity ( ∼32 ) Kattegat than in the low-salinity ( ∼15 ) Hanö Bay. Molecular identification shows that only Elphidium clavatum occurs at both locations, but other genetic types of both genera Elphidium and Ammonia are restricted to either low- or high-salinity locations. The combination of foraminiferal geochemistry and environmental parameters demonstrates that in a highly variable setting like the Baltic Sea, it is possible to separate different environmental impacts on the foraminiferal assemblages and therefore use Mn∕Ca , Mg∕Ca , and Ba∕Ca to reconstruct how specific conditions may have varied in the past.
Subject code	333 ; 511
Language	English
Publishing date	2019-02-04
Publishing country	de
Document type	Book ; Online
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Book ; Online ; Thesis: Genetic diversity, biogeography and the morpho-genetic relationship in extant planktonic foraminifera

Weiner, Agnes Katharina Maria [Verfasser] / Kucera, Michal [Akademischer Betreuer] / Darling, Kate [Akademischer Betreuer]

2014

Author's details	Agnes Katharina Maria Weiner. Gutachter: Michal Kucera ; Kate Darling. Betreuer: Michal Kucera
Keywords	Geowissenschaften ; Earth Sciences
Subject code	sg550
Language	English
Publisher	Staats- und Universitätsbibliothek Bremen
Publishing place	Bremen
Document type	Book ; Online ; Thesis
Database	Digital theses on the web

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Article: Global molecular phylogeography reveals persistent Arctic circumpolar isolation in a marine planktonic protist

Darling, Kate F / Kucera, Michal / Wade, Christopher M

Proceedings of the National Academy of Sciences of the United States of America. 2007 Mar. 20, v. 104, no. 12

2007

Abstract: The high-latitude planktonic foraminifera have proved to be particularly useful model organisms for the study of global patterns of vicariance and gene flow in the oceans. Such studies demonstrate that gene flow can occur over enormous distances in the ... ...

Abstract	The high-latitude planktonic foraminifera have proved to be particularly useful model organisms for the study of global patterns of vicariance and gene flow in the oceans. Such studies demonstrate that gene flow can occur over enormous distances in the pelagic marine environment leading to cosmopolitanism but also that there are ecological and geographical barriers to gene flow producing biogeographic structure. Here, we have undertaken a comprehensive global study of genetic diversity within a marine protist species, the high-latitude planktonic foraminiferan Neogloboquadrina pachyderma. We present extensive new data sets from the North Pacific and Arctic Oceans that, in combination with our earlier data from the North Atlantic and Southern Oceans, allow us to determine the global phylogeography of this species. The new genetic data reveal a pattern of Arctic circumpolar isolation and bipolar asymmetry between the Atlantic and Pacific Oceans. We show that the ancestry of North Pacific N. pachyderma is relatively recent. It lies within the upwelling systems and subpolar waters of the Southern Hemisphere and remarkably not within the neighboring Arctic Ocean. Instead, the Arctic Ocean population forms a genetic continuum with the North Atlantic population, which became isolated from the southern populations much earlier, after the onset of Northern hemisphere glaciation. Data from the planktonic foraminiferal morphospecies Globigerina bulloides is also introduced to highlight the isolation and endemism found within the subpolar North Pacific gyre. These data provide perspective for interpretation and discussion of global gene flow and speciation patterns in the plankton.
Language	English
Dates of publication	2007-0320
Size	p. 5002-5007.
Publishing place	National Academy of Sciences
Document type	Article
ZDB-ID	209104-5
ISSN	1091-6490 ; 0027-8424
ISSN (online)	1091-6490
ISSN	0027-8424
Database	NAL-Catalogue (AGRICOLA)

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Article: Cryptic species of planktonic foraminifera: their effect on palaeoceanographic reconstructions.

Kucera, Michal / Darling, Kate F

Philosophical transactions. Series A, Mathematical, physical, and engineering sciences

2002 Volume 360, Issue 1793, Page(s) 695–718

Abstract: Shells of planktonic foraminifera recovered from marine sediments provide a multitude of important palaeoproxies. Most of these proxies are based on the assumption that each morphospecies of planktonic foraminifera represents a genetically continuous ... ...

Abstract	Shells of planktonic foraminifera recovered from marine sediments provide a multitude of important palaeoproxies. Most of these proxies are based on the assumption that each morphospecies of planktonic foraminifera represents a genetically continuous species with a unique habitat. Recent discovery of hitherto hidden genetic diversity among modern planktonic foraminifera has significant repercussions on palaeoproxies derived from their fossil shells. We have compiled all available data on this genetic diversity. To date, 33 cryptic genetic types were found in 9 out of the 22 sequenced morphospecies of modern planktonic foraminifera. An examination of this database suggests that cryptic genetic diversity may be a prevalent pattern among modern planktonic foraminifera, but that the total number of cryptic genetic types per morphospecies is not large and that most genetic types show a non-random pattern of distribution in the oceans. Using modern distribution data from the Atlantic Ocean as constraints, the relationship between abundances of three genetic types of Globigerina bulloides and sea-surface temperature has been modelled and this model has been applied to a database of species counts in Atlantic coretops (761 samples). Trials with artificial neural networks (ANNs), the modern analogue technique and Imbrie-Kipp transfer functions showed that the splitting of G. bulloides into three genetic types resulted in substantial reduction in the prediction error rate (by 5 to 34%) and that this improvement was by far greatest in ANN trials (on average more than 20%). We conclude that such a large reduction in error rate occurred because the models resonated with a real pattern in the original data. This study indicates that genetic diversity among planktonic foraminifera may become more of a gift than malaise to palaeoproxies. If it becomes possible to distinguish these genetic types in the fossil record, the accuracy of proxies based on planktonic foraminifera will indeed substantially increase.
MeSH term(s)	Animals ; Climate ; Computer Simulation ; Earth (Planet) ; Ecosystem ; Eukaryota/classification ; Eukaryota/genetics ; Eukaryota/physiology ; Evolution, Chemical ; Evolution, Molecular ; Evolution, Planetary ; Fossils ; Genetic Variation/genetics ; Geologic Sediments ; Models, Biological ; Oceans and Seas ; Phylogeny ; Plankton/classification ; Plankton/genetics ; Plankton/physiology ; Reproducibility of Results ; Sensitivity and Specificity ; Species Specificity ; Temperature
Language	English
Publishing date	2002-04-15
Publishing country	England
Document type	Evaluation Studies ; Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	208381-4
ISSN	1471-2962 ; 1364-503X ; 0080-4614 ; 0264-3820 ; 0264-3952
ISSN (online)	1471-2962
ISSN	1364-503X ; 0080-4614 ; 0264-3820 ; 0264-3952
DOI	10.1098/rsta.2001.0962
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