Morphology, Morphometrics, and Molecular Characterization of Bryophrya gemmea n. sp. (Ciliophora, Colpodea): Implications for the Phylogeny and Evolutionary Scenario for the Formation of Oral Ciliature in the Order Colpodida

Abstract

We studied the morphology, morphometry, resting, and reproductive cysts, as well as the molecular phylogeny of Bryophrya gemmea n. sp., a colpodid ciliate that was discovered in ephemeral puddles in Idaho, northwest United States. This new species is distinguished from congeners by the irregularly pentagonal adoral organelles, four to five vestibular kineties, the single micronucleus, and one to three rows of brightly refractive protuberant interkinetal cortical granules to the right of the preoral suture. Resting cysts have two distinct membranes and an outer mucous coat. As typical for most colpodids, reproduction occurs in division cysts but details of ontogenesis are unknown. The 18S rRNA gene sequence shows only weak support for the phylogenetic relationship between Bryophrya and the bryophryid genus Notoxoma previously inferred from morphologic characters. Further, our molecular phylogenies classify bryophryids rather basal within the order Colpodida, not supporting ordinal status suggested by morphologists. Based on molecular data and morphologic characters, the colpodid genus Ilsiella is removed from the family Marynidae and placed in a new family, Ilsiellidae. Considering the molecular data, an evolutionary scenario for the formation of colpodid oral structures from a cyrtolophosidid ancestor through a bryophryid intermediate is proposed.

Congruence and indifference between two molecular markers for understanding oral evolution in the Marynidae sensu lato (Ciliophora, Colpodea)

“…In congruence with Bourland et al (2011), Foissner et al (2011) found the Marynidae s.l. to be non-monophyletic.…”

“…Recently, Bourland et al (2011) sequenced Maryna ovata , and showed that it did not form a monophyletic clade with the previously sampled Marynidae, Ilsiella palustris . However, only one of two intervening nodes between these two species was moderately supported, with 76% bootstrap by Maximum Likelihood (ML) and a posterior probability of 100% by Bayesian Inference (BI).…”

“…However, only one of two intervening nodes between these two species was moderately supported, with 76% bootstrap by Maximum Likelihood (ML) and a posterior probability of 100% by Bayesian Inference (BI). As monophyly was rejected by an S–H test ( p  < 0.05), Bourland et al (2011) concluded that the Marynidae sensu lato (s.l. ), as circumscribed in Foissner (1993), had been united based on convergent oral character states.…”

“…They moved Ilsiella into a new taxon, Ilsiellidae, and kept Maryna and other close relatives in the Marynidae sensu stricto (s.str.). Given their topology, Bourland et al (2011) also presented a hypothesis of oral evolution within the Colpodida in which the Colpoda / Maryna oral ciliary pattern originates from a cyrtolophosidid ancestor via a bardeliellid and bryophryid stage.…”

“…Both Bourland et al (2011) and Foissner et al (2011) used sequences only from the nuclear small subunit rDNA (nSSU-rDNA). The nSSU-rDNA gene trees might not be tracking accurately the species phylogeny; this would prevent accurate assessment of the evolution of oral features within the Colpodida.…”