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Phylogenomic analysis and morphological data suggest left-right swimming behavior evolved prior to the origin of the pelagic Phylliroidae (Gastropoda: Nudibranchia)

Citation

Goodheart, Jessica; Wägele, Heike (2020), Phylogenomic analysis and morphological data suggest left-right swimming behavior evolved prior to the origin of the pelagic Phylliroidae (Gastropoda: Nudibranchia), Dryad, Dataset, https://doi.org/10.6075/J04J0CHG

Abstract

Evolutionary transitions from benthic to pelagic habitats are major adaptive shifts. Investigations into such shifts are critical for understanding the complex interaction between co-opting existing traits for new functions and novel traits that originate during or post-transition. Gastropod mollusks are of particular interest in regard to benthic-pelagic evolutionary transitions, as shifts from benthic to pelagic habitats are uncommon. Phylliroe is one such pelagic lineage in Phylliroidae, a family of holoplanktonic nudibranchs with a highly aberrant morphology that appears to be adapted for life in the pelagic zone. However, the phylogenetic placement of this enigmatic group of pelagic nudibranchs has never been investigated. Here we present phylogenomic analyses which place Phylliroe within a group of nudibranchs called Dendronotida sensu stricto. We also discuss a subset of the morphological and behavioral features that Phylliroe shares with other closely related lineages (Dendronotidae, Tethyidae, and Scyllaeidae) and some that are unique to Phylliroe. Based on these data, and a literature review, we find a number of unique features found in Phylliroe that are adaptations to a pelagic environment, such as a fish-like body plan, highly reduced connective and muscular tissue in the notum, and elongated rhinophores. However, we were able to identify only a single commonality among Phylliroe and its closely related lineages, which is the presence of left-right swimming behavior. We further hypothesize that swimming behavior in this group likely represents an important trait that facilitated the transition from benthic to pelagic environments, and thus may provide evidence that major pelagic lifestyle transitions can rely on behavioral exaptations. These new insights into the origins of Phylliroe now provide a phylogenetic framework for testing for adaptations necessary for the benthic-pelagic transition in this group.

Methods

For morphology data: The specimens were previously embedded in hydroxyethyl methacrylate for serial sectioning (2.5 μm) (Kulzer ®7100). Sections were stained with toluidine blue and investigated under a ZEISS AXIO, Imager.Z2M with ZEISS AxioCam HRc and the software AxioVision, Release 4.8.1 (11-2009).

For molecular analyses: Illumina datasets assembled with Trinity were analyzed for orthology using HaMStR. Orthologous groups nucleotide sequences were then aligned and pruned of paralogs using phylopypruner. The remaining alignments were concatenated for phylogenetic analysis, performed using RAxML-NG with the matrix partitioned by codon position.

Custom HaMStR database (gastropoda_50_aplysia_californica) and the custom blast matrices (GASTRO50 and GASTRO50mod) originally generated using the methods outlined in Goodheart et al. 2015: Relationships within Cladobranchia (Gastropoda: Nudibranchia) based on RNA-Seq data: an initial investigation (doi.org/10.1098/rsos.150196).

Funding

Smithsonian Institution, Award: Peter Buck Predoctoral Fellowship

German Science Foundation, Award: Wa 618/10