Vertical niche partitioning between cryptic sibling species of a cosmopolitan marine planktonic protist.

A large portion of the surface-ocean biomass is represented by microscopic unicellular plankton. These organisms are functionally and morphologically diverse, but it remains unclear how their diversity is generated. Species of marine microplankton are widely distributed because of passive transport and lack of barriers in the ocean. How does speciation occur in a system with a seemingly unlimited dispersal potential? Recent studies using planktonic foraminifera as a model showed that even among the cryptic genetic diversity within morphological species, many genetic types are cosmopolitan, lending limited support for speciation by geographical isolation. Here we show that the current two-dimensional view on the biogeography and potential speciation mechanisms in the microplankton may be misleading. By depth-stratified sampling, we present evidence that sibling genetic types in a cosmopolitan species of marine microplankton, the planktonic foraminifer Hastigerina pelagica, are consistently separated by depth throughout their global range. Such strong separation between genetically closely related and morphologically inseparable genetic types indicates that niche partitioning in marine heterotrophic microplankton can be maintained in the vertical dimension on a global scale. These observations indicate that speciation along depth (depth-parapatric speciation) can occur in vertically structured microplankton populations, facilitating diversification without the need for spatial isolation.

Geographical distribution of cryptic genetic types in the planktonic foraminifer Globigerinoides ruber.

We present SSU rDNA data resolving the seasonal and geographical distribution of 'cryptic' genetic types of the planktonic foraminifer morphospecies Globigerinoides ruber in the eastern Atlantic Ocean and the Mediterranean Sea. Analysis of 262 sequences revealed the presence of five genetic types belonging to two distinct lineages. Although the morphospecies G. ruber occurs throughout the investigated region, its constituent 'cryptic' genetic types show a pattern of widespread exclusion, which is difficult to reconcile with the concept of ubiquitous dispersal. One of the newly discovered genetic types was exclusively found at stations in the Mediterranean Sea, possibly representing the smallest-scale example of endemism known in planktonic foraminifera. In general, our results suggest that the geographical scale of mutual exclusion between the genotypes is negatively correlated with their phylogenetic relatedness: the most similar and most recently diverged pair of siblings showed the strongest evidence for small-scale competitive exclusion. This pattern is consistent with the concept of niche partitioning, implying decreasing level of competition between genetic types with increasing degree of genetic divergence.

A Clustering Optimization Strategy for Molecular Taxonomy Applied to Planktonic Foraminifera SSU rDNA.

Identifying species is challenging in the case of organisms for which primarily molecular data are available. Even if morphological features are available, molecular taxonomy is often necessary to revise taxonomic concepts and to analyze environmental DNA sequences. However, clustering approaches to delineate molecular operational taxonomic units often rely on arbitrary parameter choices. Also, distance calculation is difficult for highly alignment-ambiguous sequences. Here, we applied a recently described clustering optimization method to highly divergent planktonic foraminifera SSU rDNA sequences. We determined the distance function and the clustering setting that result in the highest agreement with morphological reference data. Alignment-free distance calculation, when adapted to the use with partly non-homologous sequences caused by distinct primer pairs, outperformed multiple sequence alignment. Clustering optimization offers new perspectives for the barcoding of species diversity and for environmental sequencing. It bridges the gap between traditional and modern taxonomic disciplines by specifically addressing the issue of how to optimally account for both genetic divergence and given species concepts.

Using the Multiple Analysis Approach to Reconstruct Phylogenetic Relationships among Planktonic Foraminifera from Highly Divergent and Length-polymorphic SSU rDNA Sequences.

The high sequence divergence within the small subunit ribosomal RNA gene (SSU rDNA) of foraminifera makes it difficult to establish the homology of individual nucleotides across taxa. Alignment-based approaches so far relied on time-consuming manual alignments and discarded up to 50% of the sequenced nucleotides prior to phylogenetic inference. Here, we investigate the potential of the multiple analysis approach to infer a molecular phylogeny of all modern planktonic foraminiferal taxa by using a matrix of 146 new and 153 previously published SSU rDNA sequences. Our multiple analysis approach is based on eleven different automated alignments, analysed separately under the maximum likelihood criterion. The high degree of congruence between the phylogenies derived from our novel approach, traditional manually homologized culled alignments and the fossil record indicates that poorly resolved nucleotide homology does not represent the most significant obstacle when exploring the phylogenetic structure of the SSU rDNA in planktonic foraminifera. We show that approaches designed to extract phylogenetically valuable signals from complete sequences show more promise to resolve the backbone of the planktonic foraminifer tree than attempts to establish strictly homologous base calls in a manual alignment.