Global isolation by distance despite strong regional phylogeography in a small metazoan

Scott Mills,Africa Gómez,David H Lunt

doi:10.1186/1471-2148-7-225

Scott Mills, Africa Gómez + Show 1 more

Open Access

https://doi.org/10.1186/1471-2148-7-225

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Abstract

BackgroundSmall vagile eukaryotic organisms, which comprise a large proportion of the Earth's biodiversity, have traditionally been thought to lack the extent of population structuring and geographic speciation observed in larger taxa. Here we investigate the patterns of genetic diversity, amongst populations of the salt lake microscopic metazoan Brachionus plicatilis s. s. (sensu stricto) (Rotifera: Monogononta) on a global scale. We examine the phylogenetic relationships of geographic isolates from four continents using a 603 bp fragment of the mitochondrial COI gene to investigate patterns of phylogeographic subdivision in this species. In addition we investigate the relationship between genetic and geographic distances on a global scale to try and reconcile the paradox between the high vagility of this species and the previously reported patterns of restricted gene flow, even over local spatial scales.ResultsAnalysis of global sequence diversity of B. plicatilis s. s. reveals the presence of four allopatric genetic lineages: North American-Far East Asian, Western Mediterranean, Australian, and an Eastern Mediterranean lineage represented by a single isolate. Geographically orientated substructure is also apparent within the three best sampled lineages. Surprisingly, given this strong phylogeographic structure, B. plicatilis s. s. shows a significant correlation between geographic and genetic distance on a global scale ('isolation by distance' – IBD).ConclusionDespite its cosmopolitan distribution and potential for high gene flow, B. plicatilis s. s. is strongly structured at a global scale. IBD patterns have traditionally been interpreted to indicate migration-drift equilibrium, although in this system equilibrium conditions are incompatible with the observed genetic structure. Instead, we suggest the pattern may have arisen through persistent founder effects, acting in a similar fashion to geographic barriers for larger organisms. Our data indicates that geographic speciation, contrary to historical views, is likely to be very important in microorganisms. By presenting compelling evidence for geographic speciation in a small eukaryote we add to the growing body of evidence that is forcing us to rethink our views of global biodiversity.

Highlights

Small vagile eukaryotic organisms, which comprise a large proportion of the Earth's biodiversity, have traditionally been thought to lack the extent of population structuring and geographic speciation observed in larger taxa
Microscopic organisms have long been thought to occur globally wherever suitable ecological conditions exist [1]. Such cosmopolitan distributions are considered to be the consequence of large population sizes and high vagility leading to increased rates of colonization and decreased
We investigate the patterns of genetic diversity found amongst populations of the euryhaline microscopic metazoan Brachionus plicatilis s. s. (Rotifera: Monogononta) on a global scale using a fragment of the cytochrome c oxidase subunit I gene (COI or cox1) gene

Summary

Introduction

Small vagile eukaryotic organisms, which comprise a large proportion of the Earth's biodiversity, have traditionally been thought to lack the extent of population structuring and geographic speciation observed in larger taxa. Microscopic organisms have long been thought to occur globally wherever suitable ecological conditions exist [1] Such cosmopolitan distributions are considered to be the consequence of large population sizes and high vagility leading to increased rates of colonization and decreased (page number not for citation purposes). Continental zooplanktonic species, including copepods, cladocerans and rotifers, are small, microscopic organisms that disperse passively through diapausing propagules and are often found in large densities in ponds and lakes In consequence, they were thought to follow microbial rules of biogeography often summarized in the phrase "Everything is everywhere, but, the environment selects[9]." Despite being a life-long proponent of the dominance of allopatric speciation Ernst Mayr, one of the architects of the evolutionary synthesis, wrote:

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