Pole-to-Pole Gene Flow in Protozoan Ciliates

Microorganisms represent the smallest but arguably most important component of the ocean life. They are essential to all nutrient cycles because they form the bottom of the marine food chain and outnumber all other marine species by orders of magnitude. Sampling of remote and inaccessible habitats and large-scale genomic analysis have shown how little we know about the microbial life in the oceans, and how our poor knowledge of the marine chemistry and biology is preventing us from foreseeing the detrimental effects that a too rapidly changing world has on the oceans’ ecosystems. In this context, polar microorganisms are attracting particular interest because of their role in global-scale biogeochemical cycles, in particular the carbon dioxide exchange with the atmosphere (Falkowski et al. 2008). Considering this interest, planktonic and benthic microbial communities from Arctic and Antarctic areas have become the focus of more systematic samplingand rigorous analyses for their taxonomic, prokaryotic (bacterial) and eukaryotic (protist), biodiversity. A relevant result of these analyses was the finding of microbial species that, like a diverse range of plant and animal species (Lindberg 1991; Crame 1993), warrant the definition ‘‘bipolar’’ (or ‘‘anti-tropical’’), i.e. species represented by high-latitude populations physically separated in distribution across the tropics (Darling et al. 2000; Montresor et al. 2003; Brandt et al. 2007; Pawlowski et al. 2007). This concept of species bipolarity has inherently raised the intriguing question whether co-specific Antarctic and Arctic populations evolved independently since the effective separation (approximately 10–15 million years ago) between the Arctic and Antarctic cold-water provinces, or whether a trans-tropical gene flow ensures that these polar populations maintain genetic continuity (Darling et al. 2000). Morphological studies alone are clearly insufficient to address this question, due to recurrent phenomena of parallel or convergent morphological evolution that take place under similar environmental forces. Therefore, more solid grounds supporting the concept of species bipolarity have been obtained in some species of foraminifera and dinozoans from analysis of genetic variation in sequences of the small subunit (SSU) rRNA nuclear gene (Darling et al. 2000; Montresor et al. 2003; Brandt et al. 2007; Pawlowski et al. 2007). Nevertheless, unless the calibration of a molecular clock is supported by abundance in fossil records, as is the case in foraminifera (Pawlowski et al. 1997), also this genetic approach is impaired by the fact that the same DNA regions may evolve at different rates among closely related organisms. A solution to overcoming this challenge is provided by the well-defined, monophyletic group of ciliates which are ideal organisms for the analysis of the breeding structure of natural microbial populations and, therefore, for obtaining data which satisfy the interbreeding criterion on which the biological (Darwinian) concept of species is founded. Ciliates govern their gene exchanges through a unique sexual phenomenon, known as conjugation (or mating), in which two functionally hermaphroditic individuals unite temporarily in pairs for a mutual exchange of a ‘‘migratory’’ (‘‘male’’) gametic nucleus destined to fuse into a synkaryon with a ‘‘resident’’ (‘‘female’’) gametic nucleus. In addition, ciliates more than any other group of polar microorganisms can readily provide living laboratory material in virtually unlimited amounts, since every aquatic polar habitat hosts a large variety of ciliate species that are relatively easy to collect and expand into permanent clonal cultures (i.e., descendants from single wild-type specimens). Here we review results that have been obtained from breeding analyses of Antarctic, Fuegian and Arctic populations of the ciliate Euplotes nobilii. These results have provided compelling evidence that these populations are genetically interconnected by gene flow and form a unique interbreeding biological species. The description of these results is preceded by an outline of our current knowledge of ciliate biodiversity in the polar regions, and by a rationalization of the genetic mechanism of the mating types that represents the major driving force of ciliate breeding strategies.