The Diversity and Distribution of Modern Planktic Foraminiferal Small Subunit Ribosomal RNA Genotypes and their Potential as Tracers of Present and Past Ocean Circulations

Darling, Kate; Wade, Christopher M.; Kroon, Dick; Brown, Andrew; Biȷma, Jelle

doi:10.1029/1998pa900002

Cited by 130 publications

(121 citation statements)

References 26 publications

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“…Assumption 3 implies that genetic divergence mechanisms are globally ubiquitous. This assumption is consistent with empirical observations that morphospecies of planktonic foraminifera are capable of global dispersal (20) yet comprise populations that exhibit significant levels of divergence among polar to tropical oceanic provinces (21)(22)(23)(24). Together these two observations indicate that natural selection powerfully constrains effective rates of gene flow among foraminifera populations (25) and thereby facilitates genetic divergence among populations in relation to environmental gradients at all latitudes.…”

Section: Model Developmentsupporting

confidence: 75%

“…7, by using a global compilation of SSU rDNA data for Ͼ20 ''cryptic'' taxa (23) that have been identified within seven morphospecies of planktonic foraminifera (see Appendix 2, which is published as supporting information on the PNAS web site). These cryptic taxa are ecologically distinct genotypes with different geographic distributions (21)(22)(23)(24)31) and temperature optima (23). They are therefore thought to represent incipient morphotaxa in the relatively early stages of speciation (24).…”

Section: Resultsmentioning

confidence: 99%

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Kinetic effects of temperature on rates of genetic divergence and speciation

Allen

Gillooly

Savage

et al. 2006

Proc. Natl. Acad. Sci. U.S.A.

384

447

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Latitudinal gradients of biodiversity and macroevolutionary dynamics are prominent yet poorly understood. We derive a model that quantifies the role of kinetic energy in generating biodiversity. The model predicts that rates of genetic divergence and speciation are both governed by metabolic rate and therefore show the same exponential temperature dependence (activation energy of Ϸ0.65 eV; 1 eV ‫؍‬ 1.602 ؋ 10 ؊19 J). Predictions are supported by global datasets from planktonic foraminifera for rates of DNA evolution and speciation spanning 30 million years. As predicted by the model, rates of speciation increase toward the tropics even after controlling for the greater ocean coverage at tropical latitudes. Our model and results indicate that individual metabolic rate is a primary determinant of evolutionary rates: Ϸ10 13 J of energy flux per gram of tissue generates one substitution per nucleotide in the nuclear genome, and Ϸ10 23 J of energy flux per population generates a new species of foraminifera. allopatric speciation ͉ biodiversity ͉ macroevolution ͉ metabolic theory of ecology ͉ molecular clock T he latitudinal increase in biodiversity from the poles to the equator is the most pervasive feature of biogeography. For two centuries, since the time of von Humboldt, Darwin, and Wallace, scientists have proposed hypotheses to explain this pattern. New species arise through the evolution of genetic differences among populations from a common ancestral lineage (1-4). Many hypotheses therefore attribute the latitudinal biodiversity gradient to a gradient in speciation rates caused by some independent variable, such as earth surface area or solar energy input (5-7). Some fossil data suggest that speciation rates do indeed increase toward the tropics (8-10), but these findings remain open to debate due in part to our limited understanding of the factors that control macroevolutionary dynamics.Recent advances toward a metabolic theory of ecology (11) provide new opportunities for assessing the factors that control speciation rates. This recent work indicates that two fundamental variables influencing the tempo of evolution, the generation time, and the mutation rate (3) are both direct consequences of biological metabolism (12-14). Here we combine these recent insights from metabolic theory with the theory of population genetics to derive a model that predicts how environmental temperature, through its effects on individual metabolic rates (Eqs. 1-4), influences rates of genetic divergence among populations (Eqs. 5-7) and rates of speciation in communities (Eqs. 8 and 9). We evaluate the model by using data from planktonic foraminifera, because this group has extensive DNA sequence data for evaluating population-level predictions on genetic divergence combined with an exceptionally complete fossil record for evaluating community-level predictions on speciation rates. Model DevelopmentThe two individual-level variables constraining the evolutionary rate of a population, the generation time, and the mutation rate (3) ...

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Section: Model Developmentsupporting

confidence: 75%

Section: Resultsmentioning

confidence: 99%

Kinetic effects of temperature on rates of genetic divergence and speciation

Allen

Gillooly

Savage

et al. 2006

Proc. Natl. Acad. Sci. U.S.A.

384

447

View full text Add to dashboard Cite

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“…For example, fifty-four cryptic species have been identified among nine modern planktonic foraminiferal morphospecies commonly used for paleoceanographic reconstructions (Kucera and Darling, 2002;Darling and Wade, 2008;Morard et al, 2013). Several studies suggest that cryptic species can differ in their ecological preferences (Huber et al, 1997;Darling et al, 1999;de Vargas et al, 1999de Vargas et al, , 2003Stewart et al, 2001;Kuroyanagi and Kawahata, 2004;Morard et al, 2009Morard et al, , 2013Aurahs et al, 2011) and emphasize the importance of distinguishing between genotypes for paleoceanographic reconstructions (Kucera and Darling, 2002). Based on these findings, it is likely that a morphotype/genotype "lumping" approach for geochemical, morphometric and distribution analyses introduces a significant amount of noise into paleoclimate records.…”

Section: Overviewmentioning

confidence: 99%

“…Marine Micropaleontology 120 (2015) [46][47][48][49][50][51][52][53][54][55][56][57][58][59][60][61][62][63][64] However, the significance of morphological variation was not apparent until the first genetic studies of foraminifera. These studies revealed that many morphologically defined species are complexes of cryptic genetic variants (Darling et al, 1996(Darling et al, , 1999de Vargas et al, 1997de Vargas et al, , 1999de Vargas et al, , 2003Huber et al, 1997;Kucera and Darling, 2002;Darling and Wade, 2008). For example, fifty-four cryptic species have been identified among nine modern planktonic foraminiferal morphospecies commonly used for paleoceanographic reconstructions (Kucera and Darling, 2002;Darling and Wade, 2008;Morard et al, 2013).…”

Section: Overviewmentioning

confidence: 99%

Morphometric and stable isotopic differentiation of Orbulina universa morphotypes from the Cariaco Basin, Venezuela

Marshall

Thunell

Spero

et al. 2015

Marine Micropaleontology

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Biometric characteristics of Orbulina universa (d'Orbigny) were used to differentiate two morphotypes present in sediment trap samples collected from the Cariaco Basin, Venezuela. Specifically, wall thickness and weight-area relationships were used to separate shells into thin (M thin ) and thick (M thick ) morphotypes. M thick (mean thickness = 19-41 μm) comprises 75% of the total O. universa in these samples and has morphometric characteristics similar to that of the previously described Type I Caribbean genotype, whereas M thin (mean thickness = 6-22 μm) is comparable to the Type III Mediterranean genotype. The flux of M thick increases during periods of upwelling, whereas M thin flux shows no systematic relationship with changing hydrographic regimes in the basin. The δ 18O and δ 13 C of M thick are on average 0.34‰ higher and 0.38‰ lower, respectively, than those of M thin , suggesting that they calcify their final spherical chamber at different depths in the water column and/or differ in their vital effects on shell geochemistry. Additionally, the absolute offset in the stable isotopic compositions of the two morphotypes varies as a function of surface ocean stratification. During periods of upwelling, the δ

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“…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 Diversity and Distribution of Modern Planktic Foraminiferal Small Subunit Ribosomal RNA Genotypes and their Potential as Tracers of Present and Past Ocean Circulations

Cited by 130 publications

References 26 publications

Kinetic effects of temperature on rates of genetic divergence and speciation

Kinetic effects of temperature on rates of genetic divergence and speciation

Morphometric and stable isotopic differentiation of Orbulina universa morphotypes from the Cariaco Basin, Venezuela

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

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