Macroevolutionary analyses of ciliates associated with hosts support high diversification rates

Ciliophora is a phylum that is comprised of extremely diverse microorganisms with regard to their morphology and ecology. They may be found in various environments, as free-living organisms or associated with metazoans. Such associations range from relationships with low metabolic dependence such as epibiosis, to more intimate relationships such as mutualism and parasitism. We know that symbiotic relationships occur along the whole phylogeny of the group, however, little is known about their evolution. Theoretical studies show that there are two routes for the development of parasitism, yet few authors have investigated the evolution of these characteristics using molecular tools. In the present study, we inferred a wide dated molecular phylogeny, based on the 18S rDNA gene, for the entire Ciliophora phylum, mapped life habits throughout the evolutionary time, and evaluated whether symbiotic relationships were linked to the variation in diversification rates and to the mode of evolution of ciliates. Our results showed that the last common ancestor for Ciliophora was likely a free-living organism, and that parasitism is a recent adaptation in ciliates, emerging more than once and independently via two distinct routes: (i) a free-living ciliate evolved into a mutualistic organism and, later, into a parasitic organism, and (ii) a free-living ciliate evolved directly into a parasitic organism. Furthermore, we have found a significant increase in the diversification rate of parasitic and mutualistic ciliates compared with their free-living conspecifics. The evolutionary success in different lineages of symbiont ciliates may be associated with many factors including type and colonization placement on their host, as well as physical and physiological conditions made available by the hosts.