Evolutionary Associations of Endosymbiotic Ciliates Shed Light on the Timing of the Marsupial–Placental Split

Abstract

Trichostome ciliates are among the most conspicuous protists in the gastrointestinal tract of a large variety of vertebrates. However, little is still known about phylogeny of the trichostome/vertebrate symbiotic systems, evolutionary correlations between trichostome extrinsic traits, and character-dependent diversification of trichostomes. These issues were investigated here, using the relaxed molecular clock technique along with stochastic mapping of character evolution, and binary-state speciation and extinction models. Clock analyses revealed that trichostomes colonized the vertebrate gastrointestinal tract ∼135 Ma, that is, near the paleontological minimum for the split of therian mammals into marsupials and placentals. According to stochastic mapping, the last common ancestor of trichostomes most likely invaded the hindgut of a mammal. Although multiple shifts to fish/amphibian or avian hosts and to the foregut compartments took place during the trichostome phylogeny, only transition to the foregut was recognized as a key innovation responsible for the explosive radiation of ophryoscolecid trichostomes after the Cretaceous/Tertiary boundary, when ungulates began their diversification. Since crown radiations of main trichostome lineages follow those of their mammalian hosts and are in agreement with their historic dispersal routes, the present time-calibrated phylogeny might help to elucidate controversies in the geological and molecular timing of the split between marsupials and placental mammals.

A Proposed Timescale for the Evolution of Armophorean Ciliates: Clevelandellids Diversify More Rapidly Than Metopids

“…; Rataj and Vďačný ; Sauvadet et al. ; Vďačný ). The present time‐calibrated phylogeny indicates that evolution of metopid and clevelandellid ciliates is also coupled with that of their hosts.…”

Delimitation of five astome ciliate species isolated from the digestive tube of three ecologically different groups of lumbricid earthworms, using the internal transcribed spacer region and the hypervariable D1/D2 region of the 28S rRNA gene

“…Recent phylogenetic studies have suggested that some endosymbiotic ciliates cluster according to associations with higher taxa of their hosts. For instance, astome ciliates originating from terrestrial oligochaetes form a clade that is sister to the cluster of astomes from marine polychaetes [11][12][13][14]; clevelandellid ciliates, which live in the hindgut of panesthiine cockroaches, form a monophyletic group [4,15]; and trichostome ciliates exhibit a clustering specific for higher taxa of their vertebrate hosts and individual gastrointestinal compartments [10,[16][17][18].…”

Evolutionary Origin and Host Range of Plagiotoma lumbrici (Ciliophora, Hypotrichia), an Obligate Gut Symbiont of Lumbricid Earthworms

“…This either points to an unusual evolution or existence of a species complex. Moreover, Plagiotoma lumbrici is an obligate endosymbiont and hence may be subjected to an accelerated molecular evolution, as known for instance from trichostome ciliates (Vďačný ). To analyze the rate constancy, we performed the two‐cluster relative‐rate test on the 18S rRNA gene alignment as well as on the concatenated super‐matrix.…”

“…Nevertheless, detailed morphological and molecular data from ciliates identified as Plagiotoma lumbrici isolated from various host species are needed to confirm the determination of their gut symbionts. Interestingly, endosymbiotic ciliates are usually not restricted to a single host species, but they are generally restricted to ecologically similar, higher taxa of their hosts (for details, see Rataj and Vďačný , ; Vďačný ; Vďačný et al. , ).…”

“…Diversification and distribution of endobiotic ciliates are very likely governed by the geographic range and biology of their hosts (e.g. Rataj and Vďačný ; Vďačný ; Vďačný et al. ).…”