Homology and homoplasy of swimming behaviors and neural circuits in the Nudipleura (Mollusca, Gastropoda, Opisthobranchia) James M. Newcomba, Akira Sakuraib, Joshua L. Lillvisb, Charuni A. Gunaratneb, and Paul S. Katzb,1 aDepartment of Biology, New England College, Henniker, NH 03242; and bNeuroscience Institute, Georgia State University, Atlanta, GA 30302 Edited by John C. Avise, University of California, Irvine, CA, and approved April 23, 2012 (received for review February 29, 2012) How neural circuit evolution relates to behavioral evolution is not individually identifiable neurons, allowing the neural circuitry well understood. Here the relationship between neural circuits underlying the swimming behaviors to be determined with and behavior is explored with respect to the swimming behaviors cellular precision. of the Nudipleura (Mollusca, Gastropoda, Opithobranchia). Nudi- Here we will summarize what is known about the phylogeny of pleura is a diverse monophyletic clade of sea slugs among which Nudipleura, their swimming behaviors, and the neural circuits only a small percentage of species can swim. Swimming falls into underlying swimming. We will also provide data comparing the a limited number of categories, the most prevalent of which are roles of homologous neurons. We find that neural circuits un- rhythmic left–right body flexions (LR) and rhythmic dorsal–ventral derlying the behaviors of the same category are composed of body flexions (DV). The phylogenetic distribution of these behav- overlapping sets of neurons even if they most likely evolved in- iors suggests a high degree of homoplasy. The central pattern dependently. In contrast, neural circuits underlying categorically generator (CPG) underlying DV swimming has been well charac- distinct behaviors use nonoverlapping sets of neurons. Further- terized in Tritonia diomedea and in Pleurobranchaea californica. more, homologous neurons can have different functions in dif- The CPG for LR swimming has been elucidated in Melibe leonina ferent behaviors and even in similar behaviors. and Dendronotus iris, which are more closely related. The CPGs for the categorically distinct DV and LR swimming behaviors consist of Phylogeny of Nudipleura nonoverlapping sets of homologous identified neurons, whereas The Nudipleura form a monophyletic clade within Opistho- the categorically similar behaviors share some homologous iden- branchia (Gastropoda) that contains two sister clades: Pleuro- tified neurons, although the exact composition of neurons and branchomorpha and Nudibranchia (19–21) (Fig. 1). Molecular synapses in the neural circuits differ. The roles played by homolo- evidence suggests that the two sister groups separated approxi- gous identified neurons in categorically distinct behaviors differ. mately 125 Mya (21). Nudibranchia (or, informally, nudi- However, homologous identified neurons also play different roles branchs), which are shell-less and have a slug-shaped appearance even in the swim CPGs of the two LR swimming species. Individual with “naked gills,” were traditionally classified as their own or- neurons can be multifunctional within a species. Some of those der. The most recently agreed upon taxonomic classification functions are shared across species, whereas others are not. system for nudibranchs uses unranked clades instead of orders, The pattern of use and reuse of homologous neurons in various suborders, and superfamilies (22). There are at least 2,000 to forms of swimming and other behaviors further demonstrates 3,000 identified nudibranch species (23). Studies that used that the composition of neural circuits influences the evolution morphological and molecular data support the monophyly of of behaviors. Nudibranchia (19–21, 24–26). Within Nudibranchia, there are two monophyletic clades (19): evolvability | neuromodulation | rhythmic movement | Euctenidiacea (Anthobranchia) (27, 28) and Cladobranchia (25). species differences | neuroethology Euctenidiacea includes Doridacea, which is larger than Clado- branchia, subdividing into 25 families (28). Within Cladobranchia, ehavior and neural mechanisms can be considered to rep- Bornellidae forms a sister group to the other subclades (25). Bresent two different levels of biological organization (1–4). Aeolidida is a monophyletic clade with Lomanotidae as a sister Nevertheless, the evolution of behavior and the evolution of group (25). What was traditionally called Dendronotida forms neural circuits underlying behavior are intertwined. For example, a paraphyletic grouping. A recent study was unable to include it has been suggested that the properties of neural circuits affect the nudibranch Melibe in Cladobranchia because of a 12-bp de- the evolvability of behavior; the evolution of particular behaviors letion in its genome (25). However, its natural affinity with Tethys could be constrained or promoted by the organization of neural in terms of shared derived characteristics strongly suggests that it circuits (5–9). Darwin and the early ethologists recognized that belongs in Cladobranchia, as we have indicated in Fig. 1. There behaviors, like anatomical features, are heritable characters that are several additional unresolved relations in Nudibranchia, most are amenable to a phylogenetic approach (10–13). The use of behavioral traits to determine phylogenies has been validated several times (14–17), and the historical debates about homology This paper results from the Arthur M. Sackler Colloquium of the National Academy of and homoplasy of behavior have been thoroughly reviewed (2–4, Sciences, “In the Light of Evolution VI: Brain and Behavior,” held January 19–21, 2012, at the Arnold and Mabel Beckman Center of the National Academies of Sciences and Engi- 15, 17, 18). Examining the neural bases for independently neering in Irvine, CA. The complete program and audio files of most presentations are evolved (i.e., homoplastic) behaviors within a clade could pro- available on the NAS Web site at www.nasonline.org/evolution_vi. vide insight into fundamental aspects of neural circuit organi- Author contributions: J.M.N., A.S., J.L.L., C.A.G., and P.S.K. designed research; J.M.N., A.S., zation. However, it is difficult enough to determine the neural J.L.L., and C.A.G. performed research; J.M.N., A.S., J.L.L., C.A.G., and P.S.K. analyzed data; basis for behavior in one species. Doing this in several species and J.M.N., A.S., J.L.L., C.A.G., and P.S.K. wrote the paper. with quantifiable behaviors is even more challenging. The authors declare no conflict of interest. Studies of the neural bases of swimming behaviors in the This article is a PNAS Direct Submission. Nudipleura (Mollusca, Gastropoda, Opisthobranchia) offer such 1To whom correspondence should be addressed. E-mail: [email protected]. a possibility. These sea slugs exhibit well differentiated catego- This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. ries of swimming behaviors, and their nervous systems have large 1073/pnas.1201877109/-/DCSupplemental. www.pnas.org/cgi/doi/10.1073/pnas.1201877109 PNAS Early Edition | 1of8 Downloaded by guest on October 3, 2021 Clade Family Genus Cephalopyge trematoides (33). This is also true for gastropods in Bornellidae Bornella -LR general; there are ∼40,000 marine gastropod species but only approximately 150 are pelagic (33). Dironidae Dirona -NS In addition to crawling, a limited number of benthic species Tritonia - DV Tritoniidae Marionia - DV can also swim (34). We classify swimming in the Nudipleura into Tochuina -NS seven general categories: (i) left–right flexion (LR), (ii) dorsal– ventral flexion (DV), (iii) left–right undulation (LU), (iv) dorsal– Notobryon - LR Scyllaeidae Scyllaea -LR ventral undulation (DU), (v) asymmetric undulation (AU), (vi) Dendronodae Dendronotus -LR breaststroke (BS), and (vii) flapping (F) (Table S1). Dendronoda Melibe -LR LR swimming is characterized by the flattening of the body in Tethydidae Cladobranchia Tethys -LR the sagittal plane and repeated left–right bending near the Phylliroë -LU Phylliroidae midpoint of the body axis with the head and tail coming together Cephalopyge -LU laterally (Fig. 2A). This movement propels the animal through Lomanodae Lomanotus -LR the water. Some animals, such as Melibe leonina, exhibit foot-first Cumanotus - BS Flabellinidae Flabellina cynara - BS directionality, presumably because the dorsal cerata create drag. Flabellina iodinea - LR Other animals, such as Tambja eliora, proceed headfirst, with the Flabellina telja - LR tail lagging slightly, causing the body to take on an “S” form (34). Flabellina trophina - NS Animals in the genus Plocamopherus typically have a dorsal crest Aeolidida Aeolidiidae Aeolidella - BS at the posterior end of the body that may act as a paddle and Nudibranchia Hermissenda - LR Glaucidae Pteraeolidia - LR cause the head to proceed the tail (35). Plocamopherus ceylonicus (35, 36) and Plocamopherus maderae Armina - NS (37) swim with LR flexions when dislodged from a substrate or Dorididae Aphelodoris - DV disturbed in some way. Tambja appears to use LR swimming as Diaulula - NS an escape response; contact with the predacious nudibranch Discodorididae Discodoris - DV Roboastra will elicit swimming in Tambja (34, 38). LR swim- Sebadoris - DV/DU ming in Melibe and Dendronotus iris can be initiated in response Archidoris - NS to loss of contact with the substrate or in response to the touch Doridoidea Chromodoridae Hypselodoris - NS Cadlina - NS of a predatory sea star (39, 40). Melibe may also swim seasonally