Comparative morphology and evolution of the cnidosac in Cladobranchia (Gastropoda: Heterobranchia: Nudibranchia)

Abstract

BackgroundA number of shelled and shell-less gastropods are known to use multiple defensive mechanisms, including internally generated or externally obtained biochemically active compounds and structures. Within Nudipleura, nudibranchs within Cladobranchia possess such a special defense: the ability to sequester cnidarian nematocysts – small capsules that can inject venom into the tissues of other organisms. This ability is distributed across roughly 600 species within Cladobranchia, and many questions still remain in regard to the comparative morphology and evolution of the cnidosac – the structure that houses sequestered nematocysts (called kleptocnides). In this paper, we describe cnidosac morphology across the main groups of Cladobranchia in which it occurs, and place variation in its structure in a phylogenetic context to better understand the evolution of nematocyst sequestration.ResultsOverall, we find that the length, size and structure of the entrance to the cnidosac varies more than expected based on previous work, as does the structure of the exit, the musculature surrounding the cnidosac, and the position and orientation of the kleptocnides. The sequestration of nematocysts has originated at least twice within Cladobranchia based on the phylogeny presented here using 94 taxa and 409 genes.ConclusionsThe cnidosac is not homologous to cnidosac-like structures found in Hancockiidae. Additionally, the presence of a sac at the distal end of the digestive gland may have originated prior to the sequestration of nematocysts. This study provides a more complete picture of variation in, and evolution of, morphological characters associated with nematocyst sequestration in Cladobranchia.Electronic supplementary materialThe online version of this article (10.1186/s12983-018-0289-2) contains supplementary material, which is available to authorized users.

Multiple paedomorphic lineages of soft-substrate burrowing invertebrates: parallels in the origin of Xenocratena and Xenoturbella

“…Nudibranchs are a fascinating group of shell-less molluscs that demonstrate astonishing diversity and peculiar evolutionary traits [13,14] and are commonly used as model organisms in neurophysiology and other fields [15,16]. A subgroup of nudibranchs, treated here as suborder Aeolidacea, has evolved a defensive system for the secondary usage of cnidocysts from cnidarian prey [17,18]. While the phylogeny of Aeolidacea is currently actively studied [18][19][20][21], a majority of these nudibranchs as defined within the previously established broad-scope aeolidacean nudibranch phylogenetic framework [19], are complex animals with numerous dorsal papillae (cerata) (Figs 1-3).…”

“…A subgroup of nudibranchs, treated here as suborder Aeolidacea, has evolved a defensive system for the secondary usage of cnidocysts from cnidarian prey [17,18]. While the phylogeny of Aeolidacea is currently actively studied [18][19][20][21], a majority of these nudibranchs as defined within the previously established broad-scope aeolidacean nudibranch phylogenetic framework [19], are complex animals with numerous dorsal papillae (cerata) (Figs 1-3). However, there is a single exclusively infaunal family, Pseudovermidae, with evident paedomorphic features such as vermiform shape and reduced dorsal papillae, which strongly matches early ontogenetic stages of complex aeolidaceans [22].…”

Description of a new Moridilla species from North Sulawesi, Indonesia (Mollusca: Nudibranchia: Aeolidioidea)—based on MicroCT, histological and molecular analyses

“…Mitochondrial cytochrome c oxidase subunit I (COI) and 16S rRNA were sequenced for 12 Moridilla specimens and seven specimens belonging to Facelinidae (Table 1). Based on the results of Korshunova et al (2017) and Goodheart et al (2018) with regard to paraphyly of Facelinidae and outgroup results, we retrieved all available sequences of Facelinidae and Aeolidiidae from GenBank. According to the published phylogenetic analyses we chose available sequences of Unidentia and some Flabellinoidea as outgroup.…”

“…Additionally, the relationship of these three genera within the Facelinidae was not thoroughly analysed by any morphological or molecular phylogenetic studies. Latest molecular studies render Facelinidae paraphyletic (Carmona et al 2013;Mahguib & Valdés 2015;Goodheart et al 2015;Goodheart 2017;Goodheart et al 2018;Martynov et al 2019) and even contradict a close relationship of these genera. Palisa groups with some facelinid taxa, whereas Noumeaella groups with other facelinids as sister taxon to Aeolidiidae.…”

“…Moridilla brockii (included only in one study on Aeolidiidae) clusters with facelinid species but not with Noumeaella (Carmona et al 2013). In the available genomic studies (Goodheart 2017;Goodheart et al 2017Goodheart et al , 2018Martynov et al 2019) Moridilla was not included; however, Palisa groups with genera that also show a closer relationship to Moridilla (see Carmona et al 2013) than to Noumeaella. The description of the monotypic genus Moridilla with Moridilla brockii was based on a single individual from Pulau Dapur, Java, Indonesia (Bergh 1888).…”