Phylogeography of the Tropical Planktonic Foraminifera Lineage Globigerinella Reveals Isolation Inconsistent with Passive Dispersal by Ocean Currents

Weiner, Agnes; Weinkauf, Manuel F. G.; Kurasawa, Atsushi; Darling, Kate; Kučera, Michal; Grimm, Guido W.

doi:10.1371/journal.pone.0092148

Cited by 42 publications

(49 citation statements)

References 57 publications

(88 reference statements)

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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%

“…This is carried out using one of three methods: (1) DOC DNA extraction buffer containing sodiumdeoxycholate (Holzmann and Pawlowski, 1996;Pawlowski, 2000), which does not allow preservation of the calcite shells, (2) GITC * buffer containing guanidinium isothiocyanate (e.g., Morard, 2010) or (3) urea buffer with high concentrations of urea (Seears and Wade, 2014;Weiner et al, 2014). Both of the latter methods are non-destructive for the calcite shells (Figure 3), which can thus be used for morphometric and geochemical analyses.…”

Section: Dna Extractionmentioning

confidence: 99%

“…These single-cell molecular studies have further revealed a detailed picture of the distribution patterns of the cryptic species of planktonic foraminifera, enabling comparison of the largely globally distributed morphospecies with the more restricted and ecologically specialized biogeography of their cryptic counterparts (e.g., de Vargas et al, 1999;Darling et al, 2007;Aurahs et al, 2009a;Morard et al, 2011;Seears et al, 2012;Weiner et al, 2012Weiner et al, , 2014. This approach provides a high resolution perspective for the construction of hypotheses on species dispersal, gene flow between populations and potential speciation mechanisms in the open ocean (de Vargas et al, 1999;Darling et al, 2000;Weiner et al, 2012Weiner et al, , 2014.…”

Section: Introductionmentioning

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%

“…This approach provides a high resolution perspective for the construction of hypotheses on species dispersal, gene flow between populations and potential speciation mechanisms in the open ocean (de Vargas et al, 1999;Darling et al, 2000;Weiner et al, 2012Weiner et al, , 2014.…”

Section: Introductionmentioning

confidence: 99%

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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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Section: Preservation Of Specimensmentioning

confidence: 99%

Section: Dna Extractionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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

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High dispersal capacity and biogeographic breaks shape the genetic diversity of a globally distributed reef‐dwelling calcifier

Prazeres

Morard

Roberts

et al. 2020

Ecology and Evolution

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Understanding the role of dispersal and adaptation in the evolutionary history of marine species is essential for predicting their response to changing conditions. We analyzed patterns of genetic differentiation in the key tropical calcifying species of large benthic foraminifera Amphistegina lobifera to reveal the evolutionary processes responsible for its biogeographic distribution. We collected specimens from 16 sites encompassing the entire range of the species and analyzed hypervariable fragments of the 18S SSU rDNA marker. We identified six hierarchically organized genotypes with mutually exclusive distribution organized along a longitudinal gradient. The distribution is consistent with diversification occurring in the Indo‐West Pacific (IWP) followed by dispersal toward the periphery. This pattern can be explained by: (a) high dispersal capacity of the species, (b) habitat heterogeneity driving more recent differentiation in the IWP, and (c) ecological‐scale processes such as niche incumbency reinforcing patterns of genotype mutual exclusion. The dispersal potential of this species drives the ongoing range expansion into the Mediterranean Sea, indicating that A. lobifera is able to expand its distribution by tracking increases in temperature. The genetic structure reveals recent diversification and high rate of extinction in the evolutionary history of the clade suggesting a high turnover rate of the diversity at the cryptic level. This diversification dynamic combined with high dispersal potential, allowed the species to maintain a widespread distribution over periods of geological and climatic upheaval. These characteristics are likely to allow the species to modify its geographic range in response to ongoing global warming without requiring genetic differentiation.

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Intraspecific size variation in planktonic foraminifera cannot be consistently predicted by the environment

Rillo

Miller

Kučera

et al. 2020

Ecology and Evolution

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The size structure of plankton communities is an important determinant of their functions in marine ecosystems. However, few studies have quantified how organism size varies within species across biogeographical scales. Here, we investigate how planktonic foraminifera, a ubiquitous zooplankton group, vary in size across the tropical and subtropical oceans of the world. Using a recently digitized museum collection, we measured shell area of 3,799 individuals of nine extant species in 53 seafloor sediments. We first analyzed potential size biases in the collection. Then, for each site, we obtained corresponding local values of mean annual sea‐surface temperature (SST), net primary productivity (NPP), and relative abundance of each species. Given former studies, we expected species to reach largest shell sizes under optimal environmental conditions. In contrast, we observe that species differ in how much their size variation is explained by SST, NPP, and/or relative abundance. While some species have predictable size variation given these variables ( Trilobatus sacculifer, Globigerinoides conglobatus, Globigerinella siphonifera, Pulleniatina obliquiloculata, Globorotalia truncatulinoides ), other species show no relationships between size and the studied covariates ( Globigerinoides ruber , Neogloboquadrina dutertrei , Globorotalia menardii, Globoconella inflata ). By incorporating intraspecific variation and sampling broader geographical ranges compared to previous studies, we conclude that shell size variation in planktonic foraminifera species cannot be consistently predicted by the environment. Our results caution against the general use of size as a proxy for planktonic foraminifera environmental optima. More generally, our work highlights the utility of natural history collections and the importance of studying intraspecific variation when interpreting macroecological patterns.

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Phylogeography of the Tropical Planktonic Foraminifera Lineage Globigerinella Reveals Isolation Inconsistent with Passive Dispersal by Ocean Currents

Cited by 42 publications

References 57 publications

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

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

High dispersal capacity and biogeographic breaks shape the genetic diversity of a globally distributed reef‐dwelling calcifier

Intraspecific size variation in planktonic foraminifera cannot be consistently predicted by the environment

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