Ecological partitioning and diversity in tropical planktonic foraminifera

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

Seasonal distribution of genetic types of planktonic foraminifer morphospecies in the Santa Barbara Channel and its paleoceanographic implications

We present data on the temporal distribution of planktonic foraminifer genotypes (small subunit (SSU) ribosomal (r) RNA gene) and morphospecies (sediment traps) collected during 1999 in the Santa Barbara Channel. The sampling was undertaken with special emphasis on paleoceanographically important morphospecies, predominantly Globigerina bulloides. We found the same genotype of G. bulloides (type IId) in all the changing hydrographic regimes associated with this region throughout the annual cycle with the exception of January, when we recorded the additional presence of the high-latitude G. bulloides type IIa. We identified three new genotypes: Neogloboquadrina dutertrei type Ic, N. pachyderma dextral type II, and Turborotalita quinqueloba type IId. Our data suggest that G. bulloides type IId and possibly even the new genotypes listed above may be associated specifically with the complex hydrography or other environmental features characteristic of this area. Since G. bulloides type IId occurs throughout the year and its peak fluxes are related to different hydrographic regimes, we argue that the physical properties of the water column are not the major factor influencing the distribution and growth of this genotype. In sediment trap samples we found a skewed coiling ratio for G. bulloides (most likely representing type IId), which is related neither to sea surface temperature nor to genotypic difference. This study illustrates the necessity to map both the spatial and temporal distribution of the genetic types, especially in areas of paleoceanographic interest, where geochemical and paleontological proxies are being calibrated

Cyanobacterial endobionts within a major marine, planktonic, calcifier (Globigerina bulloides, Foraminifera) revealed by 16S rRNA metabarcoding

We investigated the possibility of bacterial symbiosis in Globigerina bulloides, a palaeoceanographically important, planktonic foraminifer. This marine protist is commonly used in micropalaeontological investigations of climatically sensitive subpolar and temperate water masses as well as wind-driven upwelling regions of the world's oceans. G. bulloides is unusual because it lacks the protist algal symbionts that are often found in other spinose species. In addition, it has a large offset in its stable carbon and oxygen isotopic compositions compared to other planktonic foraminifer species, and also that predicted from seawater equilibrium. This is suggestive of novel differences in ecology and life history of G. bulloides, making it a good candidate for investigating the potential for bacterial symbiosis as a contributory factor influencing shell calcification. Such information is essential to evaluate fully the potential response of G. bulloides to ocean acidification and climate change. To investigate possible ecological interactions between G. bulloides and marine bacteria, 18S rRNA gene sequencing, fluorescence microscopy, 16SrRNA gene metabarcoding and transmission electron microscopy (TEM) were performed on individual specimens ofG. bulloides(type IId) collected from two locations in the California Current. Intracellular DNA extracted from fiveG. bulloidesspecimens was subjected to 16S rRNA gene metabarcoding and, remarkably, 37–87 % of all 16S rRNA gene sequences recovered were assigned to operational taxonomic units (OTUs) from the picocyanobacterium Synechococcus. This finding was supported by TEM observations of intact Synechococcus cells in both the cytoplasm and vacuoles of G. bulloides. Their concentrations were up to 4 orders of magnitude greater inside the foraminifera than those reported for the California Current water column and approximately 5 % of the intracellular Synechococcus cells observed were undergoing cell division. This suggests that Synechococcus is an endobiont of G. bulloides type IId, which is the first report of a bacterial endobiont in the planktonic foraminifera. We consider the potential roles of Synechococcus and G. bulloides within the relationship and the need to determine how widespread the association is within the widely distributed G. bulloides morphospecies. The possible influence of Synechococcus respiration on G. bulloides shell geochemistry is also explored

A resolution for the coiling direction paradox in Neogloboquadrina pachyderma.

We present new data on genotypic differences and biogeographic distribution of coiling types in the living planktonic foraminiferal morphospecies Neogloboquadrina pachyderma. The genetic evidence demonstrates that coiling direction in N. pachyderma is a genetic trait, heritable through time, and is not a morphological feature reflecting ecophenotypic variation. The two opposite coiling morphotypes appear to have diverged during the late Miocene, and they have distinctly different ecologies. In combination with fossil evidence, biogeography, and ecology the degree of genetic distinction between the two coiling types of N. pachyderma strongly implies that they should be considered different species. We propose the adoption of the widely recognized name N. incompta for the right coiling morphospecies. The genetic evidence also demonstrates a low level (<3%) of aberrant coiling associated with both morphotypes. The abundance of these aberrant specimens has no relationship with the environment. These findings have important consequences for the use of N. pachyderma and N. incompta as paleoceanographic signal carriers in polar and subpolar waters. Copyright 2006 by the American Geophysical Union

Geochemical imprints of genotypic variants of <i>Globigerina bulloides</i> in the Arabian Sea

Planktonic foraminifera record oceanic conditions in their shell geochemistry. Many palaeoenvironmental studies have used fossil planktonic foraminifera to constrain past seawater properties by defining species based on their shell morphology. Recent genetic studies, however, have identified ecologically distinct genotypes within traditionally recognized morphospecies, signaling potential repercussions for palaeoclimate reconstructions. Here we demonstrate how the presence of Globigerina bulloides cryptic genotypes in the Arabian Sea may influence geochemical signals of living and fossil assemblages of these morphospecies. We have identified two distinct genotypes of G. bulloides with either cool water (type-II) or warm water (type-I) temperature preferences in the Western Arabian Sea. We accompany these genetic studies with analyses of Mg/Ca and stable oxygen isotope (δ18O) compositions of individual G. bulloides shells. Both Mg/Ca and δ18O values display bimodal distribution patterns. The distribution of Mg/Ca values cannot be simply explained by seawater parameters, and we attribute it to genotype-specific biological controls on the shell geochemistry. The wide range of δ18O values in the fossil assemblage also suggests that similar controls likely influence this proxy in addition to environmental parameters. However, the magnitude of this effect on the δ18O signals is not clear from our data set, and further work is needed to clarify this. We also discuss current evidence of potential genotype-specific geochemical signals in published data on G. bulloides geochemistry and other planktonic foraminiferal species. We conclude that significant caution should be taken when utilizing G. bulloides geochemistry for paleoclimate reconstruction in the regions with upwelling activity or oceanographic fronts

Genetic diversity and ecology of the planktonic foraminifers Globigerina bulloides , Turborotalita quinqueloba and Neogloboquadrina pachyderma off the Oman margin during the late SW Monsoon

The molecular work was funded by an Advanced Fellowship award to K. Darling (UK Natural Environment Research Council (NERC); NER/J/S/2000/00860 and NE/D009707/1). SA received support from a DAAD fellowship (A0998101) and HS was supported by a DFG grant (SCHU 1605/2-1).The tropical waters of the Arabian Sea are among the richest biological areas of the world. The highly complex monsoonal system is particularly challenging for palaeoenvironmental study, which relies heavily upon understanding the modern-day ecology of planktonic foraminiferal assemblages and their geochemical signatures throughout the monsoonal cycle. Major upwelling responders such as G. bulloides, T. quinqueloba and N. pachyderma, typically associated with cooler mid to higher latitude ecosystems, are also found in number in the tropical Arabian Sea. Due to the more usual cooler water affinity of these morphospecies, the oceanographically isolated tropical upwelling ecosystem of the Arabian Sea potentially harbours new ecologically distinct genotypes (ecotypes). Samples were collected off the Oman margin at 15 stations towards the end of the summer monsoon to determine the genetic profiles of these morphospecies in both upwelling and open ocean regimes. Phylogenetic analysis of their small subunit (SSU) rDNA sequences revealed several new genetically distinct ecotypes. Two genetically divergent ecotypes of G. bulloides (Types Ia and IIf) were identified along the cruise track. Type Ia, a member of the G. bulloides warm water lineage, was found in both the upwelling and open ocean regions. The second genotype (IIf), a member of the G. bulloides cool water lineage, was found only in more marginal late upwelling cooler waters. Initial visual assessment of G. bulloides images suggests that it may be morphologically cryptic. Two highly divergent genotypes of T. quinqueloba (Types Ib and IIe) were also identified, which were largely confined to the eastern and northern Arabian Sea. Type IIe is a new member of the T. quinqueloba cool water lineage which points to its potential cool water affinity, but genotyping numbers are too low to confirm a specific association with upwelling. A new highly divergent genotype of N. pachyderma (Type VIII) was also identified at the western and southern stations. Comparison of global upwelling system genotype assemblages currently indicate little regional commonality. This complicates regional palaeoproxy understanding, since geochemical calibrations are known to be species and genotype specific. Detailed studies of the ecology and diversity of genotypes within each system should therefore be carried out to ensure the accuracy of palaeorecord interpretation.Publisher PDFPeer reviewe

Genetic and morphometric evidence for parallel evolution of the Globigerinella calida morphotype

Molecular genetic investigations of the highly abundant extant planktonic foraminifera plexus Globigerinella siphonifera/Globigerinella calida have recently shown this group to be the genetically most diverse one within planktonic foraminifera, separating it into 12 distinct genetic types belonging to three main genetic lineages. Independently, several morphological or physiological variants have been described within the group, but the correlation between the high genetic diversity and the phenotypic variability remains unclear. In this study, we combine genetic data with morphometric analyses of shell shape and porosity of genotyped individuals of the different genetic lineages. Our morphometric measurements suggest a differentiation of three morphotypes within the plexus, two of which possess the elongated chambers described as a typical trait of G. calida. These two morphotypes with elongated chambers are associated with two distinct genetic lineages. The G. calida morphology therefore appears to have evolved twice in parallel. Unexpectedly, we show that the two morphotypes with elongated chambers can be separated from each other by characters seen in the lateral view of their shells. This implies that the taxonomy of the extant members of the genus Globigerinella should be revised. A comparison with the original descriptions and type specimens of members of the genus shows that two genetic types of one major lineage correspond to G. calida. The second group with elongated chambers is associated with a recently diverged genetic type and we propose to reinstate the name Globigerinella radians for this distinct form. The remaining nine of the 12 genetic types correspond to the G. siphonifera morphology, and in the absence of evidence for morphological differentiation, they form a paraphyletic morpho-taxon. Our results highlight the prevalence of parallelism in the evolution of shell morphology in planktonic foraminifera even at the lowest level of relatedness represented by genetic types

Rapid switches in subpolar North Atlantic hydrography and climate during the Last Interglacial (MIS 5e)

Author Posting. © American Geophysical Union, 2012. This article is posted here by permission of American Geophysical Union for personal use, not for redistribution. The definitive version was published in Paleoceanography 27 (2012): PA2207, doi:10.1029/2011PA002244.At the peak of the previous interglacial period, North Atlantic and subpolar climate shared many features in common with projections of our future climate, including warmer-than-present conditions and a diminished Greenland Ice Sheet (GIS). Here we portray changes in North Atlantic hydrography linked with Greenland climate during Marine Isotope Stage (MIS) 5e using (sub)centennially sampled records of planktonic foraminiferal isotopes and assemblage counts and ice-rafted debris counts, as well as modern analog technique and Mg/Ca-based paleothermometry. We use the core MD03-2664 recovered from a high accumulation rate site (∼34 cm/kyr) on the Eirik sediment drift (57°26.34′N, 48°36.35′W). The results indicate that surface waters off southern Greenland were ∼3–5°C warmer than today during early MIS 5e. These anomalously warm sea surface temperatures (SSTs) prevailed until the isotopic peak of MIS 5e when they were interrupted by a cooling event beginning at ∼126 kyr BP. This interglacial cooling event is followed by a gradual warming with SSTs subsequently plateauing just below early MIS 5e values. A planktonic δ18O minimum during the cooling event indicates that marked freshening of the surface waters accompanied the cooling. We suggest that switches in the subpolar gyre hydrography occurred during a warmer climate, involving regional changes in freshwater fluxes/balance and East Greenland Current influence in the study area. The nature of these hydrographic transitions suggests that they are most likely related to large-scale circulation dynamics, potentially amplified by GIS meltwater influences.This work is a contribution of the European Science Foundation EuroMARC program, through the AMOCINT project, funded through grants from the Research Council of Norway (RCN) and contributes to EU-FP7 IP Past4Future. N. Irvalı was additionally funded by an ESF EUROCORES Short-term Visit grant and a RCN Leiv Eiriksson mobility grant to support research stays at the University of Edinburgh, UK, and Woods Hole Oceanographic Institution, USA, respectively, during which parts of the data for this paper were acquired. U. Ninnemann was funded by a University of Bergen Meltzer research grant.2012-11-1

Phylogeography of the tropical planktonic foraminifera lineage Globigerinella reveals isolation inconsistent with passive dispersal by ocean currents

Morphologically defined species of marine plankton often harbor a considerable level of cryptic diversity. Since many morphospecies show cosmopolitan distribution, an understanding of biogeographic and evolutionary processes at the level of genetic diversity requires global sampling. We use a database of 387 single-specimen sequences of the SSU rDNA of the planktonic foraminifera Globigerinella as a model to assess the biogeographic and phylogenetic distributions of cryptic diversity in marine microplankton on a global scale. Our data confirm the existence of multiple, well isolated genetic lineages. An analysis of their abundance and distribution indicates that our sampling is likely to approximate the actual total diversity. Unexpectedly, we observe an uneven allocation of cryptic diversity among the phylogenetic lineages. We show that this pattern is neither an artifact of sampling intensity nor a function of lineage age. Instead, we argue that it reflects an ongoing speciation process in one of the three major lineages. Surprisingly, four of the six genetic types in the hyperdiverse lineage are biogeographically restricted to the Indopacific. Their mutual co-occurrence and their hierarchical phylogenetic structure provide no evidence for an origin through sudden habitat fragmentation and their limitation to the Indopacific challenges the view of a global gene flow within the warm-water provinces. This phenomenon shows that passive dispersal is not sufficient to describe the distribution of plankton diversity. Rather, these organisms show differentiated distribution patterns shaped by species interactions and reflecting phylogenetic contingency with unique histories of diversification rates

Brecciation at the grain scale within the lithologies of the Winchcombe Mighei‐like carbonaceous chondrite

The Mighei‐like carbonaceous (CM) chondrites have been altered to various extents by water–rock reactions on their parent asteroid(s). This aqueous processing has destroyed much of the primary mineralogy of these meteorites, and the degree of alteration is highly heterogeneous at both the macroscale and nanoscale. Many CM meteorites are also heavily brecciated juxtaposing clasts with different alteration histories. Here we present results from the fine‐grained team consortium study of the Winchcombe meteorite, a recent CM chondrite fall that is a breccia and contains eight discrete lithologies that span a range of petrologic subtypes (CM2.0–2.6) that are suspended in a cataclastic matrix. Coordinated multitechnique, multiscale analyses of this breccia reveal substantial heterogeneity in the extent of alteration, even in highly aqueously processed lithologies. Some lithologies exhibit the full range and can comprise nearly unaltered coarse‐grained primary components that are found directly alongside other coarse‐grained components that have experienced complete pseudomorphic replacement by secondary minerals. The preservation of the complete alteration sequence and pseudomorph textures showing tochilinite–cronstedtite intergrowths are replacing carbonates suggest that CMs may be initially more carbonate rich than previously thought. This heterogeneity in aqueous alteration extent is likely due to a combination of microscale variability in permeability and water/rock ratio generating local microenvironments as has been established previously. Nevertheless, some of the disequilibrium mineral assemblages observed, such as hydrous minerals juxtaposed with surviving phases that are typically more fluid susceptible, can only be reconciled by multiple generations of alteration, disruption, and reaccretion of the CM parent body at the grain scale