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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)

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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.

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Data availability

Aligned data matrices, tree files, and images for morphological data are available in the Dryad Digital Repository (https://doi.org/10.6075/J04J0CHG). Newly sequenced transcriptome data are available in the NCBI Sequence Read Archive (SRR12006001 & SRR12006002; see Tables S1, 2, 3, 4).

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Acknowledgments

The authors would like to thank Maik Scherholz (former student with HW at ZFMK) who compiled much of the morphological data for the Dendronotida s.l., Steve Haddock and Lynne Christianson of MBARI for access to a tissue sample for Phylliroe bucephala, and Karen Cheney of the University of Queensland for the sample of Pteraeolidia ianthina. Use was made of computational facilities purchased with funds from the National Science Foundation (CNS-1725797) and administered by the Center for Scientific Computing (CSC). The CSC is supported by the California NanoSystems Institute and the Materials Research Science and Engineering Center (MRSEC; NSF DMR 1720256) at UC Santa Barbara. We are also grateful to the Laboratories of Analytical Biology of the National Museum of Natural History for use of the molecular laboratory facilities. We further thank two anonymous reviewers for their constructive comments, which helped us to improve this manuscript.

Funding

JAG. was supported by the NSF (PRFB Award: 1711201). Funding for RNA sequencing was provided by a Peter Buck Predoctoral Fellowship to JAG from the Smithsonian Institution. Part of the morphological study was performed with financial support of the German Science Foundation (DFG) to HW (Wa 618/10).

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  1. Scripps Institution of Oceanography, University of California, San Diego, La Jolla, CA, 92037, USA

    Jessica A. Goodheart

  2. Zoologisches Forschungsmuseum Alexander Koenig, 53113, Bonn, Germany

    Heike Wägele

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JAG and HW conceived the study and participated in study design; HW collected morphological data; JAG collected molecular data; JAG and HW participated in morphological and molecular data analysis, helped draft the manuscript, and gave final approval for publication.

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Correspondence to Jessica A. Goodheart.

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Goodheart, J.A., Wägele, H. Phylogenomic analysis and morphological data suggest left-right swimming behavior evolved prior to the origin of the pelagic Phylliroidae (Gastropoda: Nudibranchia). Org Divers Evol 20, 657–667 (2020). https://doi.org/10.1007/s13127-020-00458-9

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