Abstract
Coevolution of endosymbionts with their hosts plays an important role in the processes of speciation and is among the most fascinating topics in evolutionary biology. Astome ciliates represent an interesting model for coevolutionary studies because they are so tightly associated with their host organisms that they completely lost the cell oral apparatus. In the present study, we used five nuclear markers (18S rRNA gene, ITS1–5.8S–ITS2 region, and 28S rRNA gene) and two mitochondrial genes (16S rRNA gene and cytochrome c oxidase subunit I) to explore the diversity of astomes inhabiting the digestive tract of lumbricid earthworms at temperate latitudes in Central Europe and to cast more light on their host specificity and coevolution events that shaped their diversification. The present coevolutionary and phylogenetic interaction-adjusted similarity analyses suggested that almost every host switch leads to speciation and firm association with the new host. Nevertheless, the suggested high structural host specificity of astomes needs to be tested with increased earthworm sampling, as only 52 out of 735 lumbricid earthworms (7.07%) were inhabited by ciliates. On the other hand, the diversification of astomes associated with megascolecid and glossoscolecid earthworms might have been driven by duplication events without host switching.
Highlights
Astome ciliates are obligate endosymbionts of a wide range of invertebrates and some lower tetrapods such as newts and frogs (e.g., Heidenreich, 1935; de Puytorac, 1954, 1969, 1972; McAllister et al, 1993; McAllister and Trauth, 1996; Rataj and Vd’acný, 2018)
95 new sequences were obtained during this study, including 16 new 18S rRNA gene sequences, 14 new ITS1–5.8S–ITS2 region sequences along with the D1/D2 domains of the 28S rRNA gene, 35 new 16S rRNA gene sequences, and 30 new sequences coding for c oxidase subunit I (COI)
The two mitochondrial genes provide the highest resolution among the astome species (Figures 1A–E). rDNA cistron sequences were identical within individual species (Supplementary Tables 5–7), while 16S rRNA gene sequences had 0.00%–6.60% intraspecific divergence and 10.62%–20.45% divergence between congeneric species pairs
Summary
Astome ciliates are obligate endosymbionts of a wide range of invertebrates and some lower tetrapods such as newts and frogs (e.g., Heidenreich, 1935; de Puytorac, 1954, 1969, 1972; McAllister et al, 1993; McAllister and Trauth, 1996; Rataj and Vd’acný, 2018) These eukaryotic microbes are so tightly associated with their host organisms that they completely lost the whole oral apparatus (i.e., the oral ciliary structures including a paroral membrane and adoral organelles, cytopharynx, and cytostome) during the course of their evolution (Jankowski, 2007; Lynn, 2008). The coevolution of astomes with their hosts is an exciting but almost unexplored topic that needs to be addressed with molecular phylogenetic methods
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