Mitogenomics suggests a sister relationship of Relicanthus daphneae (Cnidaria: Anthozoa: Hexacorallia: incerti ordinis) with Actiniaria

Abstract

Relicanthus daphneae (formerly Boloceroides daphneae) was first described in 2006 as a giant sea anemone based on morphology. In 2014, its classification was challenged based on molecular data: using five genes, Relicanthus was resolved sister to zoanthideans, but with mixed support. To better understand the evolutionary relationship of Relicanthus with other early-branching metazoans, we present 15 newly-sequenced sea anemone mitochondrial genomes and a mitogenome-based phylogeny including all major cnidarian groups, sponges, and placozoans. Our phylogenetic reconstruction reveals a moderately supported sister relationship between Relicanthus and the Actiniaria. Morphologically, the cnidae of Relicanthus has apical flaps, the only existing synapomorphy for sea anemones. Based on both molecular and morphological results, we propose a third suborder (Helenmonae) within the Actiniaria to accommodate Relicanthus. Although Relicanthus shares the same gene order and content with other available actiniarian mitogenomes, it is clearly distinct at the nucleotide level from anemones within the existing suborders. The phylogenetic position of Relicanthus could reflect its association with the periphery of isolated hydrothermal vents, which, although patchy and ephemeral, harbor unique chemosynthetic communities that provide a relatively stable food source to higher trophic levels over long evolutionary timescales. The ability to colonize the deep sea and the periphery of new vent systems may be facilitated by Relicanthus’ large and extremely yolky eggs.

Extreme mito-nuclear discordance within Anthozoa, with notes on unique properties of their mitochondrial genomes

“…This large dataset of mitochondrial genomes further demonstrates the utility of off-target reads generated from target-capture data for mitochondrial genome assembly and adds to the growing knowledge of anthozoan evolution. d r a f t Introduction Mitochondrial (mt) genes have a long history of use for phylogenetic reconstruction in animals [1], and the relative ease with which complete mt genomes can now be obtained has fueled an increase in their use to resolve phylogenetic relationships within many groups [2][3][4].…”

“…The most notable of these discrepancies has been a lack of support for the monophyly of the anthozoan classes, Hexacorallia and Octocorallia. Mitochondrial phylogenies have often placed Octocorallia sister to the cnidarian sub-phylum Medusozoa [4,21,29,30], despite the very strong morphological and life-history evidence for the monophyly of Anthozoa [see 31], which has also been confirmed in several phylogenomic studies [32][33].…”

Deep water Actiniaria (Cnidaria: Anthozoa) Sicyonis, Ophiodiscus and Tealidium: re-evaluation of Actinostolidae and related families

“…Schmidt (1974) considered the presence of pmastigophores B (=p-rhabdoids B), which have three-lobed apical flap, being more ancient feature, while the presence of thin-walled p-mastigophores A (=p-rhabdoids A) without such flap more advanced and basing on these features subdivided mesomyarian Actiniaria (with and without acontia) on early Mesomyaria (without p-rhabdoids A) and later Mesomyaria (with prhabdoids A), while Endomyaria, according to him, is most evolutionary advanced group. However, nematocysts with three-lobed flap do not occur in other orders of Anthozoa and are synapomorphy for Actiniaria (see Rodríguez et al, 2014;Xiao et al, 2019), while nematocysts without three-lobed flap are present in all groups of corals and are symplesiomorphy. Spirocysts (also thin-walled and without flap) occur in all Hexacorallia (see Bozhenova et al, 1988).…”

Mitochondrial Group I Introns in Hexacorals Are Regulatory Genetic Elements

“…Not all deep-water hexacorals have mtDNA rearrangements. The Relicanthus sea anemone, sampled at a depth of 2500 m, [4] harbors the primary arrangement [33]. Similarly, Bolocera specimen samples at 40 m (Atlantic Ocean) [12] and at 1100 m (Pacific Ocean) [5] contain the same primary sea anemone arrangement.…”