Molecular evidence links cryptic diversification in polar planktonic protists to Quaternary climate dynamics - PubMed (original) (raw)

Kate F Darling et al. Proc Natl Acad Sci U S A. 2004.

Abstract

It is unknown how pelagic marine protists undergo diversification and speciation. Superficially, the open ocean appears homogeneous, with few clear barriers to gene flow, allowing extensive, even global, dispersal. Yet, despite the apparent lack of opportunity for genetic isolation, diversity is prevalent within marine taxa. A lack of candidate isolating mechanisms would seem to favor sympatric over allopatric speciation models to explain the diversity and biogeographic patterns observed in the oceans today. However, the ocean is a dynamic system, and both current and past circulation patterns must be considered in concert to gain a true perspective of gene flow through time. We have derived a comprehensive picture of the mechanisms potentially at play in the high latitudes by combining molecular, biogeographic, fossil, and paleoceanographic data to reconstruct the evolutionary history of the polar planktonic foraminifer Neogloboquadrina pachyderma sinistral. We have discovered extensive genetic diversity within this morphospecies and that its current "extreme" polar affinity did not appear until late in its evolutionary history. The molecular data demonstrate a stepwise progression of diversification starting with the allopatric isolation of Atlantic Arctic and Antarctic populations after the onset of the Northern Hemisphere glaciation. Further diversification occurred only in the Southern Hemisphere and seems to have been linked to glacial-interglacial climate dynamics. Our findings demonstrate the role of Quaternary climate instability in shaping the modern high-latitude plankton. The divergent evolutionary history of N. pachyderma sinistral genotypes implies that paleoceanographic proxies based on this taxon should be calibrated independently.

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Figures

Fig. 1.

Fig. 1.

Sampling localities and distribution of the high-latitude and Benguela left-coiling (sin) N. pachyderma SSU genotypes (n = 566). (Inset A) Distribution pattern of N. pachyderma (sin) type I (n = 216) in the Fram Strait and Norwegian Sea. The contours denote the sediment “core-top” coiling ratio (% sin coiling), delineating the modern N. pachyderma (sin) province (11). (Inset B) Distribution pattern of N. pachyderma (sin) types II (n = 41), III (n = 117), and IV (n = 79) in the subpolar/polar Antarctic. The pink contour delineates the approximate position in austral summer of 2000 of the Sub-antarctic Front and the blue contour of the Polar Front as deduced from its average position (12) and from sea-surface temperature profiles generated during cruise JR48. The main map shows the location of the N. pachyderma (sin) type IV samples (n = 3) collected from the Bellingshausen Sea ice core and the location of the type V samples (n = 22) collected from the Benguela upwelling system.

Fig. 2.

Fig. 2.

SSU rDNA phylogenetic trees highlighting the evolutionary relationships among the Neogloboquadrinidae. Trees were constructed both including (A) (685 sites, NJ) and excluding (B) (835 sites, ML) the highly divergent right-coiling (dextral) N. pachyderma SSU genotype. G. inflata was used as an outgroup. Bootstrap values (NJ/ML; expressed as a percentage) indicate support for branches in the trees.

Fig. 3.

Fig. 3.

Sequence alignment showing the extensive variation in the first variable region of the SSU rRNA gene fragment. The variable region is shown in normal text. Conserved regions, alignable across all neogloboquadrinid and outgroup taxa and used in phylogenetic tree construction (Fig. 2), are shown in bold type (∼ indicates sequences not displayed; -indicates gaps introduced in aligning sequences). Additional differences are observed between SSU genotypes in other variable regions of the SSU rDNA fragment.

Fig. 4.

Fig. 4.

(A) PL chronogram (29) with branches proportional to time. The boxed divergence times are based on the foraminiferal fossil record (27) (FAD indicates first appearance datum). Estimates of divergence times of the cryptic divergences within N. pachyderma (sin) are indicated in italic type. (B) These estimates can be compared with a proxy record for global ice volume (30). Major intervals of ice-sheet growth in the Northern Hemisphere are indicated with dashed arrows (31).

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