Origin and significance of two pairs of head tentacles in the radiation of euthyneuran sea slugs and land snails

Abstract

The gastropod infraclass Euthyneura comprises at least 30,000 species of snails and slugs, including nudibranch sea slugs, sea hares and garden snails, that flourish in various environments on earth. A unique morphological feature of Euthyneura is the presence of two pairs of sensory head tentacles with different shapes and functions: the anterior labial tentacles and the posterior rhinophores or eyestalks. Here we combine molecular phylogenetic and microanatomical evidence that suggests the two pairs of head tentacles have originated by splitting of the original single tentacle pair (with two parallel nerve cords in each tentacle) as seen in many other gastropods. Minute deep-sea snails of Tjaernoeia and Parvaplustrum, which in our phylogeny belonged to the euthyneurans’ sister group (new infraclass Mesoneura), have tentacles that are split along much of their lengths but associated nerves and epidermal sense organs are not as specialized as in Euthyneura. We suggest that further elaboration of cephalic sense organs in Euthyneura closely coincided with their ecological radiation and drastic modification of body plans. The monotypic family Parvaplustridae nov., superfamily Tjaernoeioidea nov. (Tjaernoeiidae + Parvaplustridae), and new major clade Tetratentaculata nov. (Mesoneura nov. + Euthyneura) are also proposed based on their phylogenetic relationships and shared morphological traits.

A chromosome-level genome for the nudibranch gastropod Berghia stephanieae helps parse clade-specific gene expression in novel and conserved phenotypes

“…This may be due to the fact that nematocyst sequestration relies on a largely conserved process, namely phagocytosis [ 36 , 41 , 98 ]. Our results also did not show a higher proportion clade-specific genes upregulated in the sensory rhinophores or oral tentacles compared to other tissues, which are functionally similar and homologous to tentacles in other heterobranch gastropods and caenogastropods [ 34 , 99 , 100 ]. However, the clade-specific genes that are upregulated in some of these tissues do appear to be functionally important, as our HCR results indicate that some genes (as shown in Fig.…”

How many single-copy orthologous genes from whole genomes reveal deep gastropod relationships?

“…The basis of all the above issues relies on resolving the gastropod evolutionary history, and there is great progress in subgroups, e.g ., in Vetigastropoda ( Cunha et al, 2019 ) or within Heterobranchia ( Brenzinger, Schrödl & Kano, 2021 ; Kano et al, 2016 ). However, the early gastropod phylogeny, i.e ., the relationship between major gastropod groups, is still controversial.…”

A chromosome-level genome for the nudibranch gastropodBerghia stephanieaehelps parse clade-specific gene expression in novel and conserved phenotypes

“…This may be due to the fact that nematocyst sequestration relies on a largely conserved process, namely phagocytosis [36, 41, 67]. Our results also did not show a higher proportion clade-specific genes upregulated in the sensory rhinophores or oral tentacles compared to other tissues, which are functionally similar and homologous to tentacles in other heterobranch gastropods and caenogastropods [34, 68, 69]. However, the clade-specific genes that are upregulated in some of these tissues do appear to be functionally important, as our HCR results indicate that some genes (as shown in Fig.…”