Molecular evidence of cryptic speciation in planktonic foraminifers and their relation to oceanic provinces

Abstract

The fossil record of planktonic foraminifers is a key source of data on the biodiversity and evolution of marine plankton. One of the most distinctive foraminiferal taxa, Orbulina universa, widely used as a stratigraphic and paleoclimatic index, has always been regarded as a single species. Here we present a phylogenetic analysis of Orbulina small subunit rDNA sequences from 25 pelagic stations covering 100 degrees latitude in the Atlantic Ocean. The genetic data reveal the presence of three cryptic species, whose distribution is clearly correlated to hydrographic provinces, and particularly to sea-surface total chlorophyll a concentration. Our results, together with previous studies, suggest that a considerable part of the diversity among planktonic foraminifers has been overlooked in morphological taxonomies. Our data also support the idea that planktonic foraminifers, even if adapted to particular hydrographic conditions, are high-dispersal organisms whose speciation may be similar to that of other high-dispersal taxa in which reproductive mechanisms and behavior, rather than just geographic barriers to dispersal, play key roles in species formation and maintenance.

Figure 1

Cryptic speciation in Orbulina universa. (A) SSU rDNA-based phylogenetic relationships between 37 Orbulina from Atlantic and Pacific pelagic stations and three representatives of the genus Globigerinoides, chosen as outgroup. DNA and fossil analyses (15) have shown that G. sacculifer is an ancestor of Orbulina, both lineages splitting about 19 million years ago. Blue, green, and orange frames, respectively highlight the Caribbean, Mediterranean, and Sargasso Orbulina genotypes. Scale and branch lengths are given in substitutions per site, bootstrap proportions (1,000 replicates) are encircled next to each internal branch. (B) Scanning electron microscope pictures of the tests from the three Orbulina species; note the differences in perforation size and density. Diameters of the tests are, from top to bottom: 600, 540, and 648 m. (C) Distribution of the three Orbulina species across the Atlantic Ocean. Colors and symbols for the different genotypes are the same as in A and B. Specimens from Puerto Rico, Villefranche-sur-Mer, Bermuda, and AMT-5 (14) were collected in March 1995, December 1995, April 1996, and September–October 1997, respectively.

Figure 2

Total chlorophyll a concentration (⧫) and sea surface temperature (solid line) on the AMT-5 transect. Color frames on the graph represent the distribution of Orbulina genotypes along the geographic latitudes. Note that the chlorophyll scale (left) is logarithmic.