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

PLoS One. 2014 Mar 24;9(3):e92148. doi: 10.1371/journal.pone.0092148. eCollection 2014.

Abstract

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.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Ecological and Environmental Phenomena
  • Evolution, Molecular
  • Foraminifera / genetics*
  • Foraminifera / physiology*
  • Genetic Variation
  • Oceans and Seas*
  • Phylogeography*
  • RNA, Ribosomal / genetics
  • Tropical Climate*

Substances

  • RNA, Ribosomal

Grants and funding

Deutsche Forschungsgemeinschaft (grant KU 2259/19), the Natural Environment Research Council of the UK (grants NER/J/S/2000/00860 and NE/D009707/1) and the Swedish Research Council (project no. 2008-3726). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.