Kate F. Darling

Molecular evidence for genetic mixing of Arctic and Antarctic subpolar populations of planktonic foraminifers

Bipolarity, the presence of a species in the high latitudes separated by a gap in distribution across the tropics, is a well-known pattern of global species distribution. But the question of whether bipolar species have evolved independently at the poles since the establishment of the cold-water provinces 16–8 million years ago, or if genes have been transferred across the tropics since that time, has not been addressed. Here we examine genetic variation in the small subunit ribosomal RNA gene of three bipolar planktonic foraminiferal morphospecies. We identify at least one identical genotype in all three morphospecies in both the Arctic and Antarctic subpolar provinces, indicating that trans-tropical gene flow must have occurred. Our genetic analysis also reveals that foraminiferal morphospecies can consist of a complex of genetic types. Such occurrences of genetically distinct populations within one morphospecies may affect the use of planktonic foraminifers as a palaeoceanographic proxy for climate change and necessitate a reassessment of the species concept for the group.

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.

Cryptic species of planktonic foraminifera: their effect on palaeoceanographic reconstructions

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.

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

Molecular phylogenetic analysis of the small subunit ribosomal RNA gene of planktic spinose foraminifers shows that morphospecies may represent clusters of different and often highly divergent genotypes. In some cases the level of divergence may justify separate taxonomic status as distinct “cryptic” species. Molecular evolution rate estimates, based on fossil record evidence, suggest that the cryptic divergences may have occurred many millions of years ago. An investigation of their distribution in the Caribbean (tropical zone), Coral Sea and Mediterranean Sea (subtropical zone), and Southern California Bight (transitional zone) indicates that genotypes are transported across water mass boundaries, and it is proposed that the direction of gene flow follows the prevailing global ocean surface circulation pattern. At the present time the prevailing currents transport tropical/subtropical genotypes from the Pacific to Atlantic around the South African Cape. Cooler water transitional genotypes may transit from Pacific to Atlantic in gene corridors opened during glacial periods.

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

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.

Planktic foraminiferal molecular evolution and their polyphyletic origins from benthic taxa

Phylogenetic analyses based on partial sequences of the small subunit (SSU) ribosomal (r) RNA gene have shown that the planktic and benthic foraminifera form a distinct monophyletic group within the eukaryotes. In order to determine the evolutionary relationships between benthic and planktic foraminifers, representatives of spinose and non-spinose planktic genera have been placed within a molecular SSU rDNA phylogeny containing sequences of the benthic suborders available to date. Our phylogenetic analysis shows that the planktic foraminifers are polyphyletic in origin, not evolving solely from a single ‘globigerinid-like’ lineage in the Mid-Jurassic, but derived from at least two ancestral benthic lines. The benthic ancestor of Neogloboquadrina dutertrei may have entered the plankton later than the Mid-Jurassic, and further investigation of related extant species should provide an indication of the timing of this event. The evolutionary origin of the non-spinose species Globorotalia menardii remains unclear. The divergences of the planktic spinose species generally support recent phylogenies based on the fossil record, which infer a radiation from a globigerinid common ancestor in the Mid- to Late Oligocene. The branching pattern indicates that there are possibly four distinct groups within the main spinose clade, with large evolutionary distances being observed between them. Globigerinoides conglobatus clusters strongly with Globigerinoides ruber and are divergent from Globigerinella siphonifera, Orbulina universa and Globigerinoides sacculifer. Conserved regions of the SSU rRNA gene show sufficient variation to discriminate foraminifers at the species level. Large genetic differences have been observed between the pink and white forms of Gs. ruber and between Ge. siphonifera Type I and II. The two types of Ge. siphonifera cannot be discriminated by traditional palaeontological methods, which has considerable implications for tracing fossil lineages and for the estimation of molecular evolutionary rates based upon the fossil record. The conserved regions show a high degree of sequence identity within a species, providing signature sequences for species identification. The variable regions of the gene may prove informative for population level studies in some species although complete sequence identity was observed in G. sacculifer and O. universa between specimens collected from the Caribbean and Western Pacific.

Palaeoceanographic implications of genetic variation in living North Atlantic Neogloboquadrina pachyderma.

The shells of the planktonic foraminifer Neogloboquadrina pachyderma have become a classical tool for reconstructing glacial–interglacial climate conditions in the North Atlantic Ocean. Palaeoceanographers utilize its left- and right-coiling variants, which exhibit a distinctive reciprocal temperature and water mass related shift in faunal abundance both at present and in late Quaternary sediments. Recently discovered cryptic genetic diversity in planktonic foraminifers now poses significant questions for these studies. Here we report genetic evidence demonstrating that the apparent ‘single species’ shell-based records of right-coiling N. pachyderma used in palaeoceanographic reconstructions contain an alternation in species as environmental factors change. This is reflected in a species-dependent incremental shift in right-coiling N. pachyderma shell calcite δ18O between the Last Glacial Maximum and full Holocene conditions. Guided by the percentage dextral coiling ratio, our findings enhance the use of δ18O records of right-coiling N. pachyderma for future study. They also highlight the need to genetically investigate other important morphospecies to refine their accuracy and reliability as palaeoceanographic proxies.

Genotypic variability in subarctic Atlantic planktic foraminifera

Specimens of the planktic foraminiferal morphospecies, Globigerina bulloides, Turborotalita quinqueloba, Neogloboquadrina pachyderma (dextral) and Globigerinita uvula, were collected along a subarctic Atlantic transect. Partial sequences of the small subunit (SSU) ribosomal (r) RNA gene were obtained and a distance-based foraminiferal phylogeny constructed. The low latitude morphospecies, Globigerina falconensis, was included to improve within cluster resolution. G. bulloides, G. falconensis and T. quinqueloba cluster together as a distinct group within the molecular phylogeny. The diversification of these three morphospecies from their common ancestor is clearly later than the main planktic spinose radiation, consistent with current interpretations of the fossil record. G. bulloides and G. falconensis are highly divergent from one another, supporting palaeontological and biological evidence that they are separate species. N. pachyderma (dextral) clusters with Neogloboquadrina dutertrei within the benthic and non-spinose planktic region of the tree. G. uvula also clusters within the benthic and non-spinose planktic region of the tree, adjacent to Globigerinita glutinata, a member of the same genus, though resolution is too low to provide evidence of a sister–taxon relationship. The Globigerina bulloides and Turborotalita quinqueloba morphospecies comprise a complex of distinct SSU rDNA genetic types. These fall into two groups, representing high and low latitude genotypes. Along the subarctic transect, G. bulloides and T. quinqueloba were each represented by two distinct genotypes. Neogloboquadrina pachyderma (dextral) and Globigerinita uvula were each represented by a single genotype. Genotypes of a morphospecies exhibit distinctive and different distribution patterns. In the case of Globigerina bulloides, the genotype distribution is suggestive of differing adaptation. However, the Turborotalita quinqueloba genotype distribution was complicated by their co-existence in the same water column throughout the eastern sector. Further investigation will be required to determine whether they occupy a different niche within the water column. Although only T. quinqueloba Type IIa was found in the western region, sampling density was low and inconclusive. The Neogloboquadrina pachyderma (dextral) genotype was found across the entire transect. Further investigation of genotype distribution and genotype/habitat relationships could provide new high-resolution proxies for past oceanographic/climate reconstructions.

Surviving mass extinction by bridging the benthic/planktic divide

Evolution of planktic organisms from benthic ancestors is commonly thought to represent unidirectional expansion into new ecological domains, possibly only once per clade. For foraminifera, this evolutionary expansion occurred in the Early–Middle Jurassic, and all living and extinct planktic foraminifera have been placed within 1 clade, the Suborder Globigerinina. The subsequent radiation of planktic foraminifera in the Jurassic and Cretaceous resulted in highly diverse assemblages, which suffered mass extinction at the end of the Cretaceous, leaving an impoverished assemblage dominated by microperforate triserial and biserial forms. The few survivor species radiated to form diverse assemblages once again in the Cenozoic. There have, however, long been doubts regarding the monophyletic origin of planktic foraminifera. We present surprising but conclusive genetic evidence that the Recent biserial planktic Streptochilus globigerus belongs to the same biological species as the benthic Bolivina variabilis, and geochemical evidence that this ecologically flexible species actively grows within the open-ocean surface waters, thus occupying both planktic and benthic domains. Such a lifestyle (tychopelagic) had not been recognized as adapted by foraminifera. Tychopelagic are endowed with great ecological advantage, enabling rapid recolonization of the extinction-susceptible pelagic domain from the benthos. We argue that the existence of such forms must be considered in resolving foraminiferal phylogeny.

Early evolutionary origin of the planktic foraminifera inferred from small subunit rDNA sequence comparisons

Phylogenetic analysis of five partial planktic foraminiferal small subunit (SSU) ribosomal (r) DNA sequences with representatives of a diverse range of eukaryote, archaebacterial, and eubacterial taxa has revealed that the evolutionary origin of the foraminiferal lineage precedes the rapid eukaryote diversification represented by the “crown” of the eukaryotic tree and probably represents one of the earliest splits among extant free-living aerobic eukaryotes. The foraminiferal rDNA sequences could be clearly separated from known symbionts, commensals, and food organisms. All five species formed a single monophyletic group distinguished from the “crown” group by unique foraminiferal specific insertions as well as considerable nucleotide distance in aligned regions.