Microbial evolution: patterns of diversity in aquatic protists

Abstract: Little is known about how microbes diversify in nature. In contrast to the more studied multicellular organisms, microbes can have a) huge population sizes, b) high reproductive rates and c) long-distance dispersal. These characteristics can affect their tempo and mode of diversification in ways that still need to be understood. For instance, it has been proposed that the huge population sizes and the potential for long-distance dispersal in microbes would restrain their overall diversification, generating a pattern consisting of relatively few cosmopolitan species in global scales. However, recent genetic data started to reveal that a) microbial biodiversity is much higher than previously estimated, b) that there are cosmopolitan as well as endemic species and, c) that vast diversity can be hidden within identical morphologies (reviewed in Paper 1). In Paper 2, I investigated one of the first cases of two phenotypically differentiated dinoflagellate (unicellular eukaryote) morphospecies which are genetically very similar. These two species were found to be part of a lineage which has diversified recently in evolutionary terms (Paper 3). I proposed that this diversification can be associated to transitions between environments, since the dinoflagellate lineage in question encompasses marine, brackish and freshwater strains/species from the Arctic, Antarctic and Europe. In Paper 4, several dinoflagellate species were investigated in marine-derived coastal Antarctic lakes. These lakes have evolved in 6,000 years from originally marine conditions into salinities ranging from freshwater to hypersaline. It was found that most dinoflagellate species present in these lakes have a marine origin, and that the new environmental conditions in the lakes have likely promoted the extinction of most colonizing dinoflagellates, leaving behind a few species. In Paper 5, I explored the genetic diversity within Antarctic and European lakes. The results indicated that there is normally a high genetic diversity within lakes, instead of one or a few dominating strains. Besides, I found evidence indicating that different genetic populations could coexist within a single lake. Moreover, I found that the marine and lacustrine populations of one of the studied polar species (Polarella glacialis) were genetically differentiated. In Paper 6 and 7, the effects of the marine-freshwater divide on the historical diversification of dinoflagellates and cryptomonads (unicellular eukaryotes) were explored. The most important results were that a) marine and freshwater species are usually not closely related, b) several freshwater species cluster into monophyletic groups, c) most marine-freshwater transitions do not seem to have occurred recently, d) only a small fraction of the marine lineages appear to have colonized fresh waters and e), only a small number of freshwater species seem to have re-colonized marine environments. Thus, it became apparent that the marine-freshwater boundary has acted as a major barrier during the evolutionary diversification of dinoflagellates and cryptomonads. Overall, the results of this thesis indicate that a) microbial diversification is not an uncommon process in nature, that b) microbial lake-population can harbor high genetic diversity, that c) marine-freshwater transitions are not common phenomena in microbes and that c) phenotypically different microbial morphospecies can be evolutionary very closely related.