Patterns of population structure and complex haplotype sharing at continental and local scales in field isolates of the green alga Chlamydomonas reinhardtii

There has been longstanding debate concerning biogeography and speciation in microbial eukaryotes. Competing models have argued that microbial species are either ubiquitous, with effectively unlimited dispersal and subsequently low rates of speciation, or alternatively that for many species gene flow between populations will be limited, resulting in evolutionary histories more similar to those of higher animals and plants. However, microbial eukaryotes remain severely understudied, and population genomics approaches have seldom been applied to this question. We have here analysed whole-genome re-sequencing data for all 42 field isolates of Chlamydomonas reinhardtii, a green alga used extensively as a model organism. We report evidence for allopatric divergence between N. American and Japanese isolates, and possible allopatric divergence between two highly differentiated lineages within N. America. We find signatures of substantial gene flow between the N. American lineages, and describe one isolate that appears to be an ancestor of a recent migration and admixture event. Within the most densely sampled lineage (located in Quebec and Massachusetts), we find little evidence for genetic structure between sampling sites and time points, and report that genetic diversity present at single sites is of a similar magnitude to the diversity of the entire lineage. However, we find complex patterns of relatedness between isolates at local scales, and on average a random pair of isolates sampled from Quebec/Massachusetts share 9.1% of their genomes identical by descent. This result is several orders of magnitude greater than the expectation under a Wright-Fisher model, raising many further questions regarding the population genetics of C. reinhardtii and species with similar life cycles.