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Introduction

The Alveolata is a monophyletic group of primarily single-celled eukaryotes that have adopted extremely diverse modes of nutrition, such as predation, photoautotrophy and intracellular parasitism. Most alveolates fall into one of three main subgroups: ciliates (see the second cell, starting from the left, in the title image), dinoflagellates (see the third cell, starting from the left, in the title image), and apicomplexans (see the fourth cell, starting from the left, in the title image). Apicomplexans are obligate parasites; the name of the group stems from a novel apparatus at the anterior end of the parasites that facilitates host cell attachment and invasion. This “apical complex” consists of a tubulin-based (closed) “conoid” that serves as a spring-like scaffolding for extrusive organelles called “rhoptries”. Apicomplexans infect (mostly) animal cells, ranging from the epithelial cells in the intestines of insects and marine invertebrates to the red blood cells of primates, including humans (e.g. Plasmodium is the causative agent of malaria). Some dinoflagellates are also parasites, but most are either free-living predators or photoautotrophs in aquatic habitats (Taylor 1987). Many photosynthetic dinoflagellates are also consumers of bacteria and other microeukaryotes, a mode of nutrition called “mixotrophy” (Stoecker 1999). The photosynthetic and mixotrophic species are very important players in oceanic carbon cycles, and some cause harmful (toxic) algal blooms when cell densities reach exceedingly high levels (Taylor 1987). Dinoflagellates have novel cytoskeletal and nuclear features (e.g. permanently condensed chromosomes) that make them very distinctive among eukaryotes (Fensome et al. 1999). Ciliates are mainly dynamic predators that perform essential roles as consumers in microbial food webs, and like dinoflagellates and apicomplexans, this group is extremely diverse. Some ciliates, for instance, inhabit ruminant intestinal tracts, while others invade the flesh of fish. The best synapomorphies for ciliates are two heteromorphic nuclei and a cell cortex containing many cilia (i.e. short flagella) arranged in specific configurations.

Several known lineages of alveolates do not fit neatly within any of the three major subgroups discussed above, such as Colpodella (see the first and last cells in the title image), Chromera, Colponema, Ellobiopsids, Oxyrrhis, Rastrimonas, Parvilucifera, and Perkinsus (Brugerolle 2002, 2003; Dodge and Crawford 1971a,b; Fernandez et al. 1999; Mignot and Brugerolle 1975; Moore et al. 2008; Myl'nikov 1991, 2000; Noren et al. 1999; Perkins 1976, 1996; Saldarriaga et al. 2003; Siddall et al. 1997, 2001; Silberman 2004; Simpson and Patterson 1996). Most of these lineages blur the distinction between predator and parasite and possess combinations of features that provide compelling insights into the earliest stages of alveolate evolution (e.g. the mosaic of character states in distant ancestors) (Leander and Keeling 2003; Cavalier-Smith and Chao 2004; Siddall et al. 2001). Colpodellids and perkinsids, for instance, have biflagellated predatory stages in their lifecycles that are remarkably similar to one another (e.g. they possess an apical complex with an open-sided conoid) (Myl'nikov 1991, 2000; Simpson and Patterson 1996). Colpodellids form the nearest sister lineage to apicomplexans, and perkinsids form the nearest sister lineage to dinoflagellates; therefore, the features shared by colpodellids and perkinsids are inferred to have been retained from the most recent ancestor of apicomplexans and dinoflagellates through morphostasis (Kuvardina et al. 2002; Leander and Keeling, 2003, 2004; Leander et al. 2003; Saldarriaga et al. 2003; Moore et al. 2008). The clade consisting of this particular ancestor and all of its descendent is called the “Myzozoa” (Cavalier-Smith and Chao 2004).

The Alveolata forms a sister group to two major clades of photosynthetic eukaryotes, namely the (ochrophyte) stramenopiles and the clade consisting of haptophytes and cryptophytes. Alveolates contain both photosynthetic lineages, such as Chromera and many dinoflagellates, and non-photosynthetic lineages, such as ciliates, colpodellids, apicomplexans and perkinsids. Some members of the last two lineages have been shown to possess remnant (non-photosynthetic) plastids that are surrounded by four membranes, usually referred to as “apicoplasts” (Kilejian 1975; Matsuzaki et al. 2008; McFadden and Waller 1997; McFadden et al. 1996; Teles-Grilo et al. 2007; Wilson 1996). On one hand, dinoflagellates are known to have endosymbiotically gained and lost photosynthesis from different prey organisms several times independently throughout their history (Saldarriaga, J.F. et al. 2001; Shalchian-Tabrizi et al. 2006). On the other hand, there is no compelling cellular evidence that ciliates have ever had photosynthetic ancestors, despite the fact that many different lineages of ciliates are known to (temporarily) harbor photosynthetic symbionts (Johnson et al. 2007). This complex set of phylogenetic and cell biological circumstances has made inferences about the evolutionary origins of photosynthesis in alveolates a very challenging, contentious, and exciting area of biodiversity research.

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