Maupasella mucronata (Cepede, 1910)

Obert, Tomáš & Vďačný, Peter, 2021, Multi-gene phylogeny of the subclass Astomatia (Protista: Ciliophora) refreshed with two rare astome ciliates from the digestive tube of endogeic earthworms, Organisms Diversity & Evolution (New York, N. Y.) 21 (1), pp. 59-77 : 74-75

Identification of Maupasella mucronata

Maupasella mucronata was originally described in the genus Schultzellina Cépède 1910 , which was established in memory of Max Schultze, a prominent zoologist of that time. Cépède (1910) characterized the monotypic genus Schultzellina by a conspicuous skeletal apparatus and dense somatic ciliature. However, Heidenreich (1935) considered S. mucronata to be a junior synonym of M. nova Cépède 1910 . De Puytorac (1954) accepted the transfer of S. mucronata into the genus Maupasella but not the synonymization of M. mucronata with M. nova . Schultzellina was found to be a junior synonym of Maupasella by all subsequent reviser authors ( Aescht 2001; Corliss 1979; de Puytorac 1972).

Cépède (1910) discovered M. murconata in the middle part of the digestive tract of the earthworm “ Allurus tetraedrus ” (= Eiseniella tetraedra ). Heidenreich (1935) assigned all ciliates identified as M. mucronata or M. nova ( Bhatia and Gulatti 1927; Cheissin 1930; Eksemplarskaja 1931; Pertzewa 1929; Rossolimo 1926) to the M. nova complex. However, none of these authors reported M. mucronata or M. nova from Eiseniella tetraedra , the type host of M. mucronata . As mentioned above, de Puytorac (1954) and then Lom (1961) did not follow Heidenreich’ s (1935) synonymization of M. mucronata with M. nova , and their reports of M. mucronata came exclusively from the type host Eiseniella tetraedra . In addition to Eiseniella tetraedra, Dixon (1975) detected M. mucronata along with M. cepedei de Puytorac 1954 (= M. nova according to Dixon 1975) and M. herculei de Puytorac 1954 in Eisenia fetida , Lumbricus castaneus ( Savigny 1826) , and Aporrectodea caliginosa . However, these records are not substantiated by any morphological data. Unfortunately, there is a taxonomic chaos and trustworthy morphological features for distinguishing M. mucronata , M. nova , M. cepedei , and M. herculei are not known.

Cépède (1910) stated that the body length of M. mucronata ranges from 20 to 30 μm, and there are 15 ciliary rows on each side. Heidenreich (1935) recognized two size forms in the M. nova complex: the smaller form is 22–35 μm long, free swimming in the gut content and possibly serves for infestation, while the larger form is 35–76 μm long and usually attached to the intestine epithelium by the means of the apical spine. Cépède (1910) also mentioned two size forms in M. nova (smaller form up to 82 × 39 μm, larger form 117 × 18 μm) but not in M. mucronata . De Puytorac (1954) stated that the observed specimens of M. mucronata were about 90 × 48 μm in size immediately after division and had 46 ciliary rows. Lom (1961) provided an average size of 67 × 21 μm and a variation range of 41–50 ciliary rows. The presently studied population was about 90–95 × 43–63 μm in size and had 21– 23 rows on the ventral side and approximately 19 rows on the dorsal side. Our values are thus most similar to those of de Puytorac (1954) and Lom (1961). Although they are quite different from those of Cépède (1910), we cannot exclude that he observed only en-/excysting cells or overlooked the larger form, which was reported in other possibly closely related Maupasella species (see above). Because our measurements are close to those of the revising authors ( de Puytorac 1954; Lom 1961) and the host organisms match, we assign our population to M. mucronata . To solve the taxonomic problem, detailed morphological and molecular data from populations resembling M. mucronata and M. nova isolated from various host earthworms are needed.

Evolution and phylogenetic systematics of astome ciliates

As we have already thoroughly discussed elsewhere ( Obert and Vďačný 2019, 2020), astomes show an interesting eco-evolutionary trend. Their phylogeny has very likely proceeded through specialization to various ecological/systematic groups of their host organisms. On the other hand, there is only little correlation between the traditional morphology-based classifications of astomes and their groupings in the phylogenetic trees ( Fokam et al. 2011; Obert and Vďačný 2019, 2020; Rataj and Vďačný 2018, 2019; Sauvadet et al. 2017). Thus, various morphologically dissimilar astomes belonging to the genera Njinella Ngassam 1983 , Paraclausilocola Fokam et al. 2011 , Eudrilophrya de Puytorac 1969 , and “ Metaradiophrya sp. ” sensu Fokam et al. 2011, which were isolated from the endogeic megascolecid earthworm Eupolytoreutus , group together in the 18S rRNA gene phylogenies. Likewise, highly morphologically dissimilar astomes of the genera Metaracoelophrya de Puytorac and Dragesco 1969 and Almophrya de Puytorac and Dragesco 1969 , which were isolated from the endogeic glossoscolecid earthworm Alma Grube 1855 , cluster together in the phylogenetic trees. Maupasella and Subanoplophrya Obert and Vďačný 2020 , which were isolated from the endogeic lumbricid earthworms of the genera Eiseniella Michaelsen 1900 and Octolasion Örley 1885 , are depicted as independent and not closely related lineages within the paraphyletic endogeic cluster containing astomes living in megascolecid and glossoscolecid earthworms.

Njinella , Almophrya , and Anoplophrya were traditionally classified within the family Anoplophryidae due to the lack of holdfast organelles ( de Puytorac 1994; Jankowski 2007; Lynn 2008). Haptophrya Stein 1867 , Subanoplophrya , and Paraclausilocola also do not have any attachment apparatus, but they were placed in nominotypical families or incertae sedis in the Astomatia due to their conspicuous morphological/genetic differences ( Fokam et al. 2011; Obert and Vďačný 2020; Rataj and Vďačný 2018). Eudrilophrya , Metaracoelophrya , and Metaradiophrya were traditionally assigned to the family Radiophryidae based on the Λ- shaped cytoskeletal attachment organelle. However, all three genera are phylogenetically fairly distant ( Figs. 5 , 6 , and 7). The traditional classification of astomes into families is thus not reflected in the phylogenetic trees at all, i.e., Anoplophryidae and Radiophryidae are polyphyletic and taxa without attachment organelles are scattered over the astome tree of life and mixed with taxa equipped with a holdfast apparatus. This systematic chaos was very likely caused by two evolutionary phenomena—adaptive radiation and host-driven diversification. The presence of adaptive radiation is indicated by clustering of morphologically dissimilar taxa inhabiting the same host organism, while host-driven speciation is suggested by clustering of taxa within a clade according to the ecological group of their host organisms. Adaptive radiation is evidenced by clades containing morphologically dissimilar astomes obtained exclusively from megascolecid and glossoscolecid earthworms. Host-driven diversification is evidenced by taxa clustering within the genera Anoplophrya and Metaradiophrya according to the ecological groups of their host earthworms ( Obert and Vďačný 2019, 2020; present study).

The present as well as the previous phylogenetic analyses show that the systematics of the subclass Astomatia is in a need of revision. The reconciliation of the traditional and molecular frameworks will very likely require accounting for adaptive radiation and host-driven diversification, evolutionary phenomena that might have shaped and governed the evolution of astome ciliates. However, much larger genetic sampling of the morphological and ecological diversity of astomes is required to obtain a clearer picture of the evolutionary trends in this peculiar clade of endosymbiotic ciliates.

Figures

Fig. 5 Phylogenetic tree based on the 18S rRNA gene, showing the systematic positions of Metaradiophrya speculorum sp. n. and Maupasella mucronata within the class Oligohymenophorea. The subclass Peniculia was used to a posteriori root the tree. Bootstrap values for maximum likelihood conducted in IQTrees as well as posterior probabilities for Bayesian inferences conducted in Phycas and

Fig. 6 Phylogenetic tree based on the 18S rRNA gene, showing the systematic positions of Metaradiophrya speculorum sp. n. and Maupasella mucronata isolated from endogeic lumbricid earthworms. The phylogenetic tree suggests that the evolution of endosymbiotic astome ciliates has proceeded through specialization to ecological groups of their host earthworms. Haptophrya planariarum and Dexiotricha spp. were used to a posteriori root the tree. Bootstrap