Phylogenomic analysis of pelagic Phylliroidae

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.