... Homology and Homoplasy of Swimming Behaviors and Neural Circuits in the Nudipleura (Mollusca, Gastropoda, Opisthobranchia)...

... JAMES M. NEWCOMB,* AKIRA SAKURAI,† JOSHUA L. LILLVIS,† CHARUNI A. GUNARATNE,† AND PAUL S. KATZ†‡...

... How neural circuit evolution relates to behavioral evolution is not well understood. Here the relationship between neural circuits and behavior is explored with respect to the swimming behaviors of the Nudipleura (Mollusca, Gastropoda, Opithobranchia). Nudipleura is a diverse ... of species can swim. Swimming falls into a limited number of categories, the most prevalent of which are rhythmic left–right body flexions (LR) and rhythmic dorsal–ventral body flexions (DV). The phylogenetic distribution of these behaviors suggests a high degree of homoplasy. The central ... generator (CPG) underlying DV swimming has been well characterized in Tritonia diomedea and in Pleurobranchaea californica. The CPG for LR swimming has been elucidated in Melibe leonina and Dendronotus iris, which are more closely related. ... CPGs for the categorically distinct DV and LR swimming behaviors consist of nonoverlapping sets of homologous identified neurons, whereas the categorically similar behaviors share some ... identified neurons, although the exact composition of neurons and synapses in the neural circuits differ. The roles played by homologous identified neurons in categorically distinct behaviors differ. However, ...

... *Department of Biology, New England College, Henniker, NH 03242; and †Neuroscience Institute, Georgia State University, Atlanta, GA 30302. ‡To whom correspondence should be addressed. E-mail: pkatz@gsu....

... neurons can be multifunctional within a species. Some of those functions are shared across species, whereas others are not. The pattern of use and reuse of homologous neurons in various forms of swimming and other behaviors further demonstrates that the composition of neural circuits influences ...

... Behavior and neural mechanisms can be considered to represent two different levels of biological organization (Lauder, 1986, 1994; Striedter and Northcutt, 1991; Rendall and Di Fiore, 2007). Nevertheless, the evolution of behavior and the evolution of neural circuits underlying behavior are ... ); the evolution of particular behaviors could be constrained or promoted by the organization of neural circuits (Airey et al., 2000; Bendesky and Bargmann, 2011; Carlson et al., 2011; Katz, 2011; Yamamoto and Vernier, 2011). Darwin and the early ethologists recognized that behaviors, like ... 1899; Heinroth, 1911; Lorenz, 1981). The use of behavioral traits to determine phylogenies has been validated several times (Wenzel, 1992; De Queiroz and Wimberger, 1993; Proctor, 1996; Stuart et al., 2002), and the historical debates about homology and homoplasy of behavior have been thoroughly ... (Lauder, 1986, 1994; Wenzel, 1992; Foster et al., 1996; Proctor, 1996; Rendall and Di Fiore, 2007). Examining the neural bases for independently evolved (i.e., homoplastic) behaviors within a clade could provide insight into ...

... (Mollusca, Gastropoda, Opisthobranchia) offer such a possibility. These sea slugs exhibit well differentiated categories of swimming behaviors, and their nervous systems have large individually identifiable neurons, allowing the neural circuitry underlying the swimming behaviors to be determined ...

... Here we will summarize what is known about the phylogeny of Nudipleura, their swimming behaviors, and the neural circuits underlying swimming. We will also provide data comparing the roles of homologous neurons. We find that neural circuits underlying ...

... homologous neurons can have different functions in different behaviors and even in similar behaviors....

... The Nudipleura form a monophyletic clade within Opisthobranchia (Gastropoda) that contains two sister clades: Pleurobranchomorpha and Nudibranchia (Waegele and Willan, 2000; Wollscheid-Lengeling et al., 2001; Göbbeler and Klussmann-Kolb, 2010) (Fig. 9.1). Molecular evidence ... that the two sister groups separated approximately 125 Mya (Göbbeler and Klussmann-Kolb, 2010). Nudibranchia (or, informally, nudibranchs), which are shell-less and have a slug-shaped appearance with “naked gills,& ... as their own order. The most recently agreed-upon taxonomic classification system for nudibranchs uses unranked clades instead of orders, suborders, and superfamilies (Bouchet and Rocroi, 2005). There are at least 2,000 to 3,000 identified nudibranch species (Behrens, 2005). Studies that used ... and molecular data support the monophyly of Nudibranchia (Waegele and Willan, 2000; Wollscheid-Lengeling et al., 2001; Vonnemann et al., 2005; Dinapoli and Klussmann-Kolb, 2010; Göbbeler and Klussmann-Kolb, 2010; ... and Gosliner, 2010)....

... Within Nudibranchia, there are two monophyletic clades (Waegele and Willan, 2000): Euctenidiacea (Anthobranchia) (Thollesson, 1999; Valdes, 2003) and Cladobranchia (Pola and Gosliner, 2010). Euctenidiacea includes Doridacea, which is larger than Cladobranchia, subdividing into 25 families ( ... , 1999). Within Cladobranchia, Bornellidae forms a sister group to the other subclades (Pola and Gosliner, 2010). Aeolidida is a monophyletic clade with Lomanotidae as a sister group (Pola and Gosliner, 2010). What was traditionally called ... a paraphyletic grouping. A recent study was unable to include the nudibranch Melibe in Cladobranchia because of a 12-bp deletion in its genome (Pola and Gosliner, 2010). However, its natural affinity with Tethys in terms of shared derived characteristics strongly suggests that it belongs in ... , as we have indicated in Fig. 9.1. There are several additional unresolved relations in Nudibranchia, most notably in Dendronotida and Doridacea. Consideration of locomotor behavior and neural circuits may help resolve these relations....

... and propel the animal over a surface of secreted mucus. The speed of crawling is affected by efferent serotonergic and peptidergic neurons that control the ciliary beat frequency (Audesirk, 1978; Audesirk et al., 1979; Willows et al., 1997). Some species also use ... crawling, which relies on waves of contraction or extension and contraction of the foot. Crawling is a trait shared with most Opisthobranchia and is therefore plesiomorphic to the Nudipleura. Only three nudibranch species do not crawl because they are truly pelagic: Phylliroë atlantica, ... ë bucephala, and Cephalopyge trematoides (Lalli and Gilmer, 1989). This is also true for gastropods in general; there are ~40,000 marine gastropod species but only approximately 150 are pelagic (Lalli ...

... (DV), (iii) left–right undulation (LU), (iv) dorsal–ventral undulation (DU), (v) asymmetric undulation (AU), (vi) breaststroke (BS), and (vii) flapping (F) (Table 9.1)....

... LR swimming is characterized by the flattening of the body in the sagittal plane and repeated left–right bending near the midpoint of the body axis with the head and tail coming together laterally (Fig. 9.2A). This movement ... ; form (Farmer, 1970). Animals in the genus Plocamopherus typically have a dorsal crest at the posterior end of the body that may act as a paddle and cause the head to proceed the tail (Rudman and Darvell, 1990)....

... in Table 9.1 are shown here unless species differences exist within the genus. The phylogenic relationships are based on Thollesson (1999), Waegele and Willan (2000), Wollscheid-Lengeling et al. (2001), Vonnemann et al. (2005), Göbbeler and Klussmann-Kolb (2010), and Pola and Gosliner (2010). ... references for the behavior are listed in Table 9.1. Note that this figure represents all the known swimming species and only a tiny fraction of the more than 2,000 species that are not capable of swimming or for which there are no published reports of swimming. LR, ...

... Marcus and Marcus (1967), Farmer (1970)...

... MacFarland (1966), Farmer (1970)...

... Marcus and Marcus (1967), Farmer (1970), Ferreira and Bertsch (1972)...

... Picton and Morrow (1994)...

... Tardy and Gantes (1980)...

... Risbec (1953), Farmer (1970), Willan and Coleman (1984)...

... Kjerschow-Agersborg (1922), Haefelfinger and Kress (1967), Marcus and Marcus (1967), Farmer (1970), Robilliard (1970)...

... Marcus and Marcus (1967), Farmer (1970), Robilliard (1972)...

... Garstang (1890), Thompson and Brown (1984)...

... Lalli and Gilmer (1989)...

... Lalli and Gilmer (1989)...

... Thompson and Brown (1981)...

... Thompson and Crampton (1984)...

... Willan and Coleman (1984)...

... Kjerschow-Agersborg (1921), Hurst (1968), Farmer (1970), Lawrence and Watson (2002)...

... Haefelfinger and Kress (1967)...

... Birkeland (1974)...

... Willows and Dorsett (1975)...

...                Diaulula sandiegensis...

... Marcus (1955), Marcus and Marcus(1967)...

... Marcus and Marcus (1967), Farmer (1970)...

... Risbec (1928), Marcus and Marcus (1962)...

... Risbec (1928), Gohar and Soliman (1963), Vincente (1963), Edmunds (1968), Farmer (1970)...

... Willan and Coleman (1984), Rudman and Darvell (1990)...

... Willan and Coleman (1984), Ellis (1999a), Marshall and Willan (1999)...

... Rudman and Darvell (1990), Ellis (1999b)...

... Marshall and Willan (1999)...

... Gillette et al. (1991), Davis and Mpitsos (1971)...

... Thompson and Slinn (1959), Farmer (1970)...

... NOTE: This taxonomy is based upon that of Bouchet and Rocroi (2005). Abbreviations: AU = asymmetric undulation; BS = breaststroke; DU = dorsal–ventral undulation; DV = dorsal–ventral flexion; ...

... aTested with mechanical and salt stimuli in our laboratories....

... bA paraphyletic group (Pola and Gosliner, 2010)....

... cFarmer (1970) reported that Marionia swim via left–right flexions and cited a German reference (Haefelfinger and Kress, 1967). However, a translation of this reference into English, by P. Katz, indicates that Haefelfinger and Kress reported dorsal–ventral ...

... dFarmer (1970) categorized swimming in Sebadoris and Hexabranchus as “flapping.” However, swimming in these species appears to include dorsal–ventral flexions of the body, in addition ...

... fFarmer (1970) classified Trapania velox as an LR swimmer. However, see text for additional discussion....

... Plocamopherus ceylonicus (Rudman and Darvell, 1990; Marshall and Willan, 1999) and Plocamopherus maderae (Lowe, 1842) swim with LR flexions when dislodged from a substrate or disturbed in some way. Tambja appears to use LR swimming ... response; contact with the predacious nudibranch Roboastra will elicit swimming in Tambja (Farmer, 1970; Pola et al., 2006). LR swimming in Melibe and Dendronotus iris can be initiated in response to loss of contact with the substrate or in response to the touch of a predatory sea star (Lawrence and ...

..., where the head and tail meet under the foot. Then, it flexes so that the head and tail meet above the dorsal body surface. The foot is flattened and expanded to the width of the body. A, anterior; P, posterior....

... Melibe may also swim seasonally to disperse (Mills, 1994). The flexion cycle period for Melibe and Dendronotus is approximately 3 s, and swim bouts can last many minutes (Lawrence and Watson, 2002; Sakurai et al., 2011)....

... DV swimming involves the animal flattening its body in the horizontal plane and repeatedly bending such that the tail and head meet in alternation above and below the midpoint of the body (Fig. 9.2B). Tritonia diomedea and Pleurobranchaea californica are two examples of ... swimmers that have been extensively studied (Willows, 1967; Davis and Mpitsos, 1971; Gillette and Jing, 2001; Katz, 2009). Swim bouts for Tritonia and Pleurobranchaea last less than 1 min and are triggered by contact with a predatory sea star or in the laboratory by high salt solutions or electric ... (Katz, 2010). The flexion cycle period under natural conditions is 5 to 10 s in Tritonia (Hume et al., 1982) and 3 to 6 s in Pleurobranchaea (Jing and Gillette, 1995)....

... DU swimming, like DV swimming, involves movement in dorsal and ventral directions, but here there are progressive symmetric waves of body wall or mantle muscular contraction. The Spanish dancer, Hexabranchus ... , and other members of that genus are famous for their flamboyant swimming behavior (Gohar and Soliman, 1963; Edmunds, 1968; Farmer, 1970). Hexabranchus swimming differs in several ways from the DV swimming of Tritonia and Pleurobranchaea; in ...

... cycle period (2–4 s), swim bouts occur spontaneously, and swimming can last for long periods of time....

... F swimming is similar to DV swimming in that the movement is bilaterally symmetric and dorsal–ventral in orientation, but instead of the head and tail meeting, the lateral edges of the mantle or foot rise and fall. F swimming is much more common in Opisthobranchia outside of the Nudipleura, ... as Clione limacina (Arshavsky et al., 1986) and many species of Aplysia (Bebbington and Hughes, 1973; Donovan et al., 2006)....

... AU and BS are less common forms of locomotion. AU is characteristic of Pleurobranchus membranaceus (Thompson and Slinn, 1959) in which the animal swims upside down using its mantle as a passive keel while producing alternating muscular waves along its foot. BS ... the use of appendages including cerata and tentacles to stroke the water in a manner similar to a human swimmer’s movements. Only four nudibranch species have been described as ...

... As noted earlier, we have been unable to find reports of swimming by about 97% of nudibranch species and approximately half the major subfamilies in the Pleurobranchomorpha clade. However, this does not mean they are not capable of swimming. Some species ... only as a high threshold escape response. Still, it is highly probable that the vast majority of the Nudipleura cannot and do not swim. This discussion is limited to species for which the type of swimming has been reported or for which swimming has been explicitly tested ...

... in the scientific literature, 40 species use LR or LU (Table 9.1). These 40 species are phylogenetically disparate, encompassing species in Doridacea and Cladobranchia (Fig. 9.1). Within the latter, there are LR swimmers in Aeolidoidea and Dendronotoidea. In Doridacea, all but one of the LR swimmers ...

... Unlike LR swimming, DV swimming is found in Nudibranchia and in Pleurobranchomorpha (Fig. 9.1). DV swimming is not present outside of Nudipleura and is therefore likely to be a synapomorphy of this clade. However, it is not widely displayed within Nudibranchia, appearing in just one family of ... (Tritoniidae) and in three families of Doridacea (Discodorididae, Dorididae, and Hexibranchidae). Discodorididae and Hexibranchidae also exhibit dorsal–ventral undulations (i.e., DU)....

... gain of a function such as rhythmic movement could suggest that there is a predisposition toward these behaviors. The repeated appearance of LR and DV swimming may simply indicate that these two basic movements are the most likely to occur in a slug-shaped body with few appendages. When ...

... For the moment, we will only consider the possible evolutionary scenarios that include transformations from one swimming state to another and ignore nonswimmers. It is generally the case that members of the same genus and often the same family exhibit the same form of swimming (Table 9.1), ... us to group them together (Fig. 9.3). Here we will consider potential scenarios involving just the evolution of DV and LR swimming. It is possible that the ancestral species was able to swim using either DV or LR movements. However, this seems unlikely because there ...

... Consider scenario 1 (Fig. 9.3A) in which DV swimming arose once at the base of the Nudipleura and LR swimming evolved independently several times. In this scenario, DV swimming behaviors in Pleurobranchomorpha, Doridacea, and Cladobranchia are ... in the phylogeny, there may be fewer switches in phenotype than this. In scenario 2 (Fig. 9.3B), LR swimming evolved once in the Nudibranchia, and DV swimming reevolved independently as many as four times. Again, the number of homoplastic events could be lower if the bifurcations in the ...

... FIGURE 9.3 Possible evolutionary scenarios explaining the phylogenetic distribution of swimming behaviors. Just the families of the DV and LR swimming animals are shown. (A) In scenario 1, DV swimming is a synapomorphy of the Nudipleura that was lost and replaced six times by LR swimming....

... the surface of the water.” However, there is no indication as to the plane of movement. Farmer (1970) reported working with this rare species and being unsuccessful at making it swim, and was thus unable to provide any additional information. We were unable to find any other reports of its ...

... Redefining T. velox as a DV swimmer also suggests a fourth scenario (Fig. 9.3D), whereby LR swimming arose independently in Cladobranchia and Polyceridae. This would also involve reevolution of DV swimming in Tritoniidae. Scenario 4 would therefore be the most parsimonious explanation for ...

... With our potential scenarios about the homology and homoplasy of swimming behaviors, it is now of interest to compare the neural mechanisms for these behaviors. The neural activity that underlies ... DV and LR movements originates from central pattern generator (CPG) circuits (Delcomyn, 1980). These swim CPGs are composed of neurons whose anatomical and ... sets of characteristics can be used to identify homologous neurons in other species (Croll, 1987). This allows the composition of neural circuits and the roles of homologous neurons to be compared across species. The neural circuits underlying swimming have been determined in two DV swimmers [T. ... (Katz, 2009) and P. californica (Gillette and Jing, 2001; Jing and Gillette, 1999)] and two LR swimmers [M. leonina (Sakurai et al., 2011; Thompson and Watson, 2005) and D. iris (Sakurai et al., 2011)]. We can now begin to compare neural circuits underlying behaviors of animals to address ... and functional hypotheses....

... just three neuron types (Fig. 9.4A). On each side of the brain, there are three dorsal swim interneurons (DSIs), one ventral swim interneuron (VSI), and one cerebral interneuron 2 (C2), for a total of 10 neurons (Katz, 2009, 2010). The DSIs initiate the dorsal flexion cycle in which C2 participates. ... then excites VSI, which inhibits DSI and C2 and elicits the ventral phase of the movement. As would be expected for a DV swimmer, the contralateral counterparts for each neuron fire in relative ...

... The neurons comprising the CPG for DV swimming in P. californica include DSI and C2 homologues called As and A1, respectively (Jing and Gillette, 1995, 1999). The connectivity and activity of these homologues is similar in both species (Fig. 9.4C and D). The homologue of the Tritonia ... has not been identified in Pleurobranchaea, although there is synaptic input to As and A1 during the ventral phase of the motor pattern that may arise from such a neuron (i.e., Ivs neuron) (Jing and Gillette, 1999). Alternatively, ...

... There are also Pleurobranchaea swim CPG neurons (A3 and A10) that have not been identified in Tritonia. Despite more than 40 years of electro-physiological study concentrated in the area where the A3 and ...

... With the information available about the swim CPGs in Tritonia and Pleurobranchaea, we can currently say that some homologous neurons are used for similar functions in distantly related species. This result is ... with any of the phylogenetic scenarios (Fig. 9.3). If DV swimming is homologous (scenarios 1 or 3; Fig. 9.3A and C), the similarities in the DV swim CPGs in Tritonia and Pleurobranchaea could be a result of their homology and the potential differences in the ... of the circuit architecture. The differences in the swim CPGs may just as readily reflect independent evolutionary paths (scenarios 2 or 4; Fig. 9.3B and D), which might suggest a predisposition to use certain neurons to produce these behaviors....

... The LR swim CPG was first described in M. leonina (Watson et al., 2001; Thompson and Watson, 2005). The published circuit consists of a pair of bilaterally represented neurons: swim interneuron 1 (Si1) and swim...

... FIGURE 9.4 Neural circuits and swim motor patterns for the DV swimmers Tritonia and Pleurobranchaea. (A) The Tritonia swim CPG consists of three neuron types: DSI, C2, and VSI. (B) Simultaneous intracellular microelectrode recordings ... that two contralateral DSIs fire bursts of action potentials in phase with each other and slightly ahead of the two C2s. VSI (not recorded here) fires action potentials in the interburst interval. The motor pattern is initiated by ... stimulation of a body wall nerve (stim). (C) The Pleurobranchaea swim CPG contains five types of neurons (Jing and Gillette, 1999). The As neurons are homologues of the DSIs. A1 is homologous to C2. A10 is strongly electrically coupled to A1 and, for simplicity, ... to exist based on recordings of inhibitory postsynaptic potentials in other neurons. (D) Simultaneous intracellular recordings from an A3, As, and A1. The As neuron leads the A1 neuron just as DSI leads C2. The swim motor pattern is initiated by electrical stimulation of a body wall nerve (stim). ... In A and C, the small filled circles represent inhibitory synapses, the triangles are excitatory synapses, and combinations are mixed inhibition and excitation. The resistor symbol represents electrical synapses....

... interneuron 2 (Si2; Fig. 9.5A). Based on their anatomy and neurochemistry, these neurons are not homologous to any of the Tritonia or Pleurobranchaea swim CPG neurons....

... neuron reciprocally inhibits the two contralateral counterparts (Fig. 9.5B). There is also strong electrical coupling between the ipsilateral Si1 and Si2, causing them to fire in phase with each other and 180° out of phase with the contralateral pair (Fig. 9.5C). This bursting pattern drives ...

... Homologues of the Melibe Si1 and Si2 were identified in D. iris based on anatomical, neurochemical, and electrophysiological features (Sakurai et al., 2011). However, there are important differences in the neural circuit formed by these neurons (Fig. 9. ... , the contralateral Si2 neurons fire bursts of action potentials in alternation, but the Si1 pair fire irregularly (Fig. 9.5F). Thus, whereas both Si1 and Si2 are members of the LR swim CPG in Melibe, only Si2 is in Dendronotus....

... If LR swimming in Melibe and Dendronotus is homologous, as would be expected from scenarios 2, 3, or 4 (Fig. 9.3B–D), this would be an example in which the neural ... the same. However, it could be the case that the differences in neural mechanism reflect a different evolutionary origin for LR swimming in Melibe and Dendronotus as in scenario 1 (Fig. 9.3A)....

... DSI and C2 homologues can be recognized by using neuroanatomical and neurochemical criteria, allowing them to be identified in species that are not DV swimmers (Table 9.2). The DSIs are serotonergic (Katz et al., 1994; ... et al., 1994) and have a characteristic axon projection pattern (Getting et al., 1980). They have been identified in 10 different genera, including two opisthobranchs ... of the Nudipleura (Newcomb and Katz, 2007). Electrophysiological traits of the DSI homologues show little correlation with the type of behavior produced by the species (Newcomb and ... , 2007). C2 has been identified based on peptide immuno-reactivity and characteristic morphology in five genera within the Nudipleura (Lillvis et al., 2012). These DV swim CPG neurons are present regardless of the animal&...

... The DV swim CPG neurons are not members of the LR swim CPGs. The DSI and C2 homologs in Melibe are not rhythmically active in phase with the motor pattern (Fig. 9.6A), nor are the DSI homologues rhythmically active during ...

... FIGURE 9.5 Neural circuitry and swim motor pattern for the LR swimmers Melibe and Dendronotus. (A) In the Melibe swim CPG (Thompson and Watson, 2005), there are two bilaterally represented neurons Si1 and Si2 that are mutually inhibitory across the midline and exhibit strong ... injecting 2 nA of current into it hyperpolarizes the contralateral counterpart. (C) The Melibe swim motor pattern consists of ipsilateral synchrony and alternation with the contralateral side. (D) In Dendronotus, the inhibitory connections to and from Si1 are absent, and the electrical coupling ... ) Depolarization of an Si1 with 2-nA current injection depolarizes the contralateral counterpart. (F) In the Dendronotus swim motor pattern, the left and right Si2 fire alternating bursts of action potentials, but the Si1s fire irregularly. In A and D, the shaded boxes represent the functional CPGs....

... Melibe (Newcomb and Katz, 2007)...

... Armina (Newcomb and Katz, 2007)...

... Pleurobranchaea (Jing and Gillette, 1999)...

... Dendronotus (Newcomb and Katz, 2007)...

... Triopha (Newcomb and Katz, 2007)...

... Clione (Panchin et al., 1995; Satterlie and Norekian, 1995)...

... Tochina (Newcomb and Katz, 2007)...

... Tritonia (Getting, 1977; Taghert and Willows, 1978)...

... Pleurobranchaea (Jing and Gillette, 1995)...

... DSI homologues in Melibe do have an effect on the production of the swim motor pattern; they can initiate a motor pattern in a quiescent preparation, and hyperpolarization can temporarily halt an ongoing motor pattern (Newcomb and Katz, 2009). In contrast to Tritonia, in which the DSIs are an integral ...

... to one function even within a species. In Pleurobranchaea, the DSI homologues synapse onto serotonergic neurons that increase ciliary beating and thereby increase the speed of crawling (Jing and Gillette, 2000). In Tritonia, DSI accelerates crawling through synapses onto the efferent ... pedal neuron Pd5, which in turn increases cilia beat frequency (Popescu and Frost, 2002). DSI homologues in the nonswimming Tochuina tetraquetra and Triopha catalinae also monosynaptically excite homologues of Pd5 and presumably increase the speed of crawling (Newcomb and Katz, 2007). In ...

... FIGURE 9.6 Homologues of the Tritonia DV swim CPG neurons are not rhythmically active during LR swim motor patterns. (A) In Melibe, the C2 and DSI homologues do not display any rhythmic bursting in phase with the swim motor pattern reflected in the alternating firing pattern of the left and ... synchronous irregular spiking that shows no relation to the ongoing LR swim motor pattern displayed by two contralateral pedal motor neurons (L-Pd and R-Pd)....

... al., 2008). Whereas, in the pelagic opisthobranch, C. limacina, the DSI homologues increase the frequency of parapodial “wing” flapping and excite motor neurons that innervate the wings (Arshavsky et al., 1992; Satterlie and Norekian, 1995). Thus, the DSI homologues share common functions ... controlling the foot and/or locomotion....

... The C2 and DSI homologues have additional roles outside of locomotion. In Pleurobranchaea, the C2 homologue (A1) suppresses feeding through its connections to ... -related interneurons (Jing and Gillette, 1995). In contrast, the DSI homologues (As) have the opposite effect by exciting a number of feeding interneurons (Jing and Gillette, 2000)....

... including generating DV swimming or enhancing other types of locomotion such as enhancing LR swimming or wing flapping. They also accelerate crawling and promote feeding. It is reasonable to expect that highly interconnected interneurons would not be dedicated to a single function, but would ...

... This comparative analysis has also revealed that species with categorically similar behaviors such as the two DV swimmers, Tritonia and Pleurobranchaea, or the two LR swimmers, Melibe and Dendronotus, have overlapping sets of neurons in the swim CPG circuits. In contrast, the CPGs ... categorically distinct behaviors consist of nonoverlapping sets of neurons. However, even in species that exhibit similar behaviors such as Melibe and Dendronotus, the CPG circuits can differ in neuronal and synaptic composition. Thus, although behavior itself is not a predictor of its underlying ...

... We do not understand why the circuits in Melibe and Dendronotus differ. There could be functional reasons; perhaps Si1, which is not rhythmically active in Dendronotus, has an additional function that ... incompatible with swimming in that species. There may also be phylogenetic reasons; perhaps Melibe and Dendronotus independently evolved swim CPGs and came up with different circuit organizations. Whatever the reason, the results show that analogous behaviors can be generated by circuits with ...

... the scenarios in Fig. 9.3 indicate. It is conceivable that swimming arose independently in each family where it is found, 16 times in all (Fig. 9.1 and Table 9.1)....

... Given that Tritonia and Pleurobranchaea are very distantly related within the Nudipleura clade, it is even more likely that they independently evolved DV swim CPGs. If so, ... incorporation of DSI and C2 homologues into such a circuit represents parallel evolution, whereby...

... homologous structures independently came to have similar functions (Sanderson and Hufford, 1996; Hoekstra and Price, 2004; Scotland, 2011; Wake et al., 2011). This has been suggested for other systems as well. For example, homologous brain nuclei appear to be involved in vocal ... (Feenders et al., 2008; Hara et al., 2012). Similarly, interaural coincidence detection circuits arose independently in the brainstem nuclei of birds and mammals (Schnupp and Carr, 2009). Finally, the appearance of similar cortical areas are correlates with the independent evolution of precision hand ...

... because some configurations of existing neurons could be more robust than others. The concept of evolvability first arose from genetics (Kirschner and Gerhart, 1998; Masel and Trotter, 2010), but has since been applied to nervous systems (Airey et al., 2000; Bendesky and Bargmann, 2011; Katz, 2011; ... and Vernier, 2011). Exploring the aspects of neural organization that lead to repeated evolution of particular behaviors will point to the factors that ...

... for feedback on the manuscript. This work was supported by National Science Foundation Integrative Organismal Systems Grants 0814411, 1120950, and 1011476....