Limits to gene flow in a cosmopolitan marine planktonic diatom

Abstract

The role of geographic isolation in marine microbial speciation is hotly debated because of the high dispersal potential and large population sizes of planktonic microorganisms and the apparent lack of strong dispersal barriers in the open sea. Here, we show that gene flow between distant populations of the globally distributed, bloom-forming diatom species Pseudo-nitzschia pungens (clade I) is limited and follows a strong isolation by distance pattern. Furthermore, phylogenetic analysis implies that under appropriate geographic and environmental circumstances, like the pronounced climatic changes in the Pleistocene, population structuring may lead to speciation and hence may play an important role in diversification of marine planktonic microorganisms. A better understanding of the factors that control population structuring is thus essential to reveal the role of allopatric speciation in marine microorganisms.allopatric speciation | dispersal | marine cosmopolitan planktonic microorganisms | population structure | microsatellites

Biogeography of the uncultured marine picoeukaryote MAST-4: temperature-driven distribution patterns

“…This intriguing feature, perhaps indicating some dispersal restriction for clades B and C, could also be due to undersampling and deserves more attention in future surveys. If confirmed by further results, the dispersal limitation of clades B and C would be comparable with that found with the cosmopolitan marine planktonic diatom Pseudo-nitzschia pungens (Casteleyn et al, 2010).…”

Evidence for environmental and ecological selection in a microbe with no geographic limits to gene flow

“…However, it can be conservatively estimated that these water samples contained populations that were strongly differentiated from each other because F ST values for highly variable microsatellite loci tend to be smaller than for biallelic loci (39). Divergence in T. rotula was similar to other phytoplankton species sampled over large distances, such as across the Baltic Sea and the NE Atlantic (maximum F ST = 0.099) (21,22) but below the maximum F ST (0.76) observed among allopatrically separated populations of the pennate diatom P. pungens (17). Divergence in T. rotula was comparable to population divergence observed in globally distributed, highly migratory marine macrofauna (maximum F ST = 0.175) (40)(41)(42).…”

“…Global population structure has only been investigated in the diatom Pseudonitzschia pungens. In this pennate diatom, geographic distance appeared to be a strong barrier to gene flow, suggesting allopatric isolation despite high dispersal potential (17). Individuals of P. pungens collected from the same region but at different times were pooled to represent geographically defined populations, assuming that no genetic changes occurred over time in a given location in this pennate diatom.…”

“…In theory, enormous dispersal potential should reduce genetic partitioning and homogenize gene pools. Instead, phytoplankton species harbor vast diversity and show evidence for highly structured populations and communities (17,(20)(21)(22)(23). Within the phytoplankton, diatoms are among the most productive and speciose eukaryotic microbes in the ocean (4,24), and are found across the globe, making them useful organisms through which to explore the important links between dispersal, environmental selection, and the evolution of diversity.…”

“…However, despite the evolutionary significance of environmental selection, its role in structuring populations within species occupying the high dispersal environment of the global ocean remains unclear. The additional role of dispersal and geography in structuring populations throughout the global ocean has added complexity to the debate (5,17,18).…”