Knowledge of the population biology is critical for interpreting the evolutionary history of species, including the role of selection and drift in shaping the features that define lineages. The current ‘popular’ view for microorganisms is that everything is everywhere (Baas-Becking 1934; Finlay 2002). Under this scenario, large population sizes coupled with the ability of some microorganisms to form environmentally resistant ‘cysts’ underlie the cosmopolitan distributions and subsequently low species diversity of microbial lineages. Data on Tetrahymena thermophila contradict this view in several key ways. First, despite the efforts of protistologists from across the globe in examining freshwater samples, T. thermophila has only been found in freshwater sites in Eastern North America. As T. thermophila does not make cysts, it is possible that this feature explains the noncosmopolitan distribution of this model ciliate. But the ability to make cysts is not correlated with a cosmopolitan distribution in the genus Tetrahymena as two cyst-forming species, T. vorax and T. corlissi, also are only found in sites in North America (Simon et al. 2008).
In this issue of Molecular Ecology, Zufall et al. (2013) provide compelling evidence that T. thermophila populations do not fit the prevailing view of cosmopolitan distributions of microorganisms (Fig. 11). Analysis of patterns of sequence variation at the mitochondrial Cox1 locus reveals a pattern of isolation by distance that is the hallmark of limited gene flow. Moreover, comparisons of substitutions in Cox1 and the nuclear-encoded actin gene are consistent with a relatively small effective population size for this microbial lineage. Hence, in contrast with the prevailing views, populations of T. thermophila are isolated from one another and evolutionary changes within this species may well have occurred in a scenario where the pressures of genetic drift, which is stronger in populations with lower effective population sizes, counteracted directional changes driven by natural selection. This scenario now provides a context for thinking about the evolution of specific cell biological features in this lineage.
Why study ciliates? To fully understand principles in biology, studies must be conducted from lineages across the tree of life. For eukaryotes, most ‘model organisms’ are closely related (i.e. fungi and animals both belong to the Opisthokont lineage, just one of 5–6 major lineages of eukaryotes). In contrast, T. thermophila is a member of the Alveolata, which is currently placed in an extremely diverse major clade known as SAR (reviewed in Katz 2012): Stramenopiles (e.g. diatoms, kelps, water moulds); Alveolates (e.g. ciliates, apicomplexans, dinoflagellates); and Rhizaria (e.g. Foraminifiera, Radiolaria, Cercozoa). Hence, T. thermophila has the virtue of being phylogenetically informative. It is also experimentally tractable, and as a result, its baroquely complex (and beautiful!) set of cellular features has been mined to yield remarkable scientific gold for more than three decades. The overarching principle of ciliate organization appears to be excess. For example, all ciliates are marked by the presence of two distinct genomes within each cell – a single germline micronucleus and a somatic macronucleus (Turkewitz et al. 2002). The micronucleus is a conventional diploid nucleus, while the macronucleus is polyploid and contains chromosomes that are dramatically modified during macronuclear development by site-specific breakage, DNA elimination of selected sequences and amplification of the remaining fragmented chromosomes. The difference between these two nuclei has been exploited to yield discoveries in molecular biology including striking insights on the basics of epigenetic processing (e.g. the role of specific histone variants and histone modifications such as histone acetylation; Brownell & Allis 1996). A second line of work focused on the ends of chromosomes, the telomeres, as during the development of the macronucleus, T. thermophila goes from having 10 chromosome ends (as in the diploid micronucleus) to thousands (in the polyploid macronucleus). This effort led to the first sequencing of telomeres, and to the discovery of the remarkable enzyme that makes them, telomerase (Blackburn & Gall 1978; Blackburn 2000). More recently, studies of the editing process that occurs during nuclear transformation elucidated a link between RNAi and heterochromatin formation (Cheng et al. 2010).
Nuclear dimorphism is not the only place where ciliate cellular complexity has been a bonanza for cell biologists. Cilia, the eponymous structures on the cell surface, are composed of microtubules, but so are a large number of other structures in Tetrahymena. The ability to distinguish different populations of microtubules that form distinctly different structures was the starting point for a set of studies on post-translational modifications to the microtubule subunit, tubulin, including identification of the key modifying enzymes (Gaertig 2000; Janke & Bulinski 2011). Those enzymes have turned out to be of wide importance throughout eukaryotes. Other researchers have focused on understanding features that may be ciliate specific, focusing on gene families that have undergone large expansions in Tetrahymena (e.g. Bright et al. 2010, Sugita et al. 2011). In these studies, the complexity of ciliate organization is being exploited to investigate how novel mechanisms and pathways can arise, and the work by Zufall et al. (2013) provides needed context to guide future work.
By estimating population parameters of the ciliate T. thermophila, Zufall et al. (2013) allow us to take a critical first step in understanding the natural history of this model ciliate. This type of study is essential for interpreting the origin and diversification of microbial lineages and for assessing to what extent the patterns match inferences made from analyses of larger organisms.