Consolidated data on the phylogeny and evolution of the family Tritoniidae (Gastropoda: Nudibranchia) contribute to genera reassessment and clarify the taxonomic status of the neuroscience models Tritonia and Tochuina

Abstract

Nudibranch molluscs of the family Tritoniidae are widely used neuroscience model systems for understand the behavioural and genetic bases of learning and memory. However species identity and genus-level taxonomic assignment of the tritoniids remain contested. Herein we present a taxonomic review of the family Tritoniidae using integration of molecular phylogenetic analysis, morphological and biogeographical data. For the first time the identity of the model species Tritonia tetraquetra (Pallas, 1788) and Tritonia exsulans Bergh, 1894 is confirmed. T. tetraquetra distributes across the large geographic and bathymetric distances in the North-Eastern (NE) and North-Western (NW) Pacific. In turn, at NE Pacific coasts the separate species T. exsulans is commonly occured. Thus, it reveals a misidentification of T. tetraquetra and T. exsulans species in neuroscience applications. Presence of more hidden lineages within NW Pacific T. tetraquetra is suggested. The long lasting confusion over identity of the species from the genera Tritonia and Tochuina is resolved using molecular and morphological data. We also disprove a common indication about “edible T. tetraquetra” at the Kuril Islands. It is shown that Tochuina possesses specialized tritoniid features and also some characters of “arminacean nudibranchs”, such as Doridoxa and Heterodoris. Diagnoses for the families Doridoxidae and Heterodorididae are provided. Taxonomy of the genus Doridoxa is clarified and molecular data for the genus Heterodoris presented for the first time. A taxonomic synopsis for the family Tritoniidae is provided. A new genus among tritoniid taxa is proposed. Importance of the ontogeny-based taxonomy is highlighted. The cases when apomorphic characters considerably modified in a crown group due to the paedomorphosis are revealed. Tracing of the character evolution is presented for secondary gills–a key external feature of the family Tritoniidae and traditional dendronotacean nudibranchs.

Transcriptomics provides a robust framework for the relationships of the major clades of cladobranch sea slugs (Mollusca, Gastropoda, Heterobranchia), but fails to resolve the position of the enigmatic genus Embletonia

“…Out of the seven accepted superfamilies of Cladobranchia, we were able to include members of six superfamilies, whereas a representative of the rare Doridoxoidea, recently confirmed as sister to the Arminoidea [ 26 ], was not available to us. We inferred Aeolidida, Aeolidioidea (sensu WoRMS), Proctonotoidea, and Dendronotoidea, with representatives of various families and genera, as being monophyletic.…”

“…Arminoidea and Tritonioidea are only represented by one genus each. Thus, former results on monophyly [ 26 ] still need to be tested in future genomic analyses.…”

“…Dendronotoidea and Tritonoidea were united in former times under the name Dendronotacea [ 24 ], and Proctonotoidea and Arminoidea under the name Arminacea [ 25 ]. However, many morphological and molecular studies have contested the hypotheses of Dendronotacea and Arminacea (see review in [ 21 ]), but this is not completely disregarded according to ancestral state reconstruction [ 26 ]. The enigmatic Doridoxoidea were considered for some time as the sister taxon of all other Cladobranchia, representing the Dexiarchia concept in the sense of [ 27 ].…”

“…The authors provided much evidence for the paraphyly of the former Flabellinidae, which they then split into five different families. More recently, Korshunova and Martynov [ 26 ] were able to resurrect old genus names (e.g., Duvaucelia ) and proposed a new genus Tritonicula after a careful analysis of the Tritoniidae. They also confirmed the inclusion of Doridoxa within the Cladobranchia.…”

Species delimitation and phylogeny of Doto (Nudibranchia: Dotidae) from the Northeast Atlantic, with a discussion on food specialization

“…The genus is therefore often viewed as the one of taxonomically most problematic groups among the nudibranchs. The family Dotidae, including four genera, is placed within the Dendronotoidea, combining presence of slender body, smooth oral veil, cone‐shaped dorsolateral appenadges and absence of the cuticular lining of stomach (Korshunova, Bakken, et al, 2020; Korshunova & Martynov, 2020; Wägele & Willan, 2000).…”