Reframing the 'Everything is everywhere' debate: evidence for high gene flow and diversity in ciliate morphospecies

Current debate on microbial diversity contrasts the 'cosmopolitan' hypothesis, which argues for high gene flow and low diversity, with the 'endemism' hypothesis, which argues for high diversity and geographically restricted gene flow. Our analyses of genetic variation in ciliate morphospecies isolated from ephemeral environments (freshwater ponds and tide pools) redefine this debate. In 2 different clades of oligotrich ciliates (in the genera Halteria/Meseres and Strombidium), we found both high levels of diversity and evidence of high gene flow as indicated by the presence of identical haplotypes across broad geographic ranges. Five recognizable morphospecies of Halteria/Meseres were found to be composed of 7 different clades, differing by as much as 7.6% sequence divergence at the ITS locus (ITS 1, ITS2 and 5.8S rDNA). Two recognizable morphospecies of Strombidium (S. oculatum and S. stylifer) resolved into 10 distinct clades, differing by as much as 15.7% at the same locus. For both groups of ciliates, the genetic divergence underlying these morphospecies may be related to cycles of isolation in their ephemeral habitats (freshwater lakes and ponds for Halteria/Meseres and tide pools for Strombidium). By comparison, there is both low diversity and high gene flow in published data on ciliates from open coastal water (Laboea strobila and several species of tintinnids), a more stable environment over evolutionary time-scales. Our analyses indicate that models of microbial diversity must test for ecologically driven patterns in the interactions of gene flow and species richness to account for observed patterns of high dispersal and high gene flow.