In the Light of Evolution Volume VI: Brain and Behavior (2013) / Chapter Skim
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9 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
9 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
Pages 153-174
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From page 153... ...
The CPG for LR swimming has been elucidated in Melibe leonina and Den dronotus iris, which are more closely related. The CPGs for the categori cally distinct DV and LR swimming behaviors consist of nonoverlapping sets of homologous identified neurons, whereas the categorically similar behaviors share some homologous identified neurons, although the exact composition of neurons and synapses in the neural circuits differ.
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From page 154... ...
We find that neural circuits underlying the behaviors of the same category are composed of overlapping sets of neurons even if they most likely evolved independently. In contrast, neural circuits underlying categorically distinct behaviors use nonoverlapping sets of neurons.
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From page 155... ...
Consideration of locomotor behavior and neural circuits may help resolve these relations. CATEGORIES OF LOCOMOTOR BEHAVIOR Crawling is the primary form of locomotion for all Nudipleura (Audesirk, 1978; Audesirk et al., 1979; Chase, 2002)
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From page 156... ...
156 Clade Family Genus Bornellidae Bornella - LR Dironidae Dirona - NS Tritonia - DV Tritoniidae Marionia - DV Tochuina - NS DendronoƟda Cladobranchia Notobryon - LR Scyllaeidae Scyllaea - LR DendronoƟdae Dendronotus - LR Melibe - LR Tethydidae Tethys - LR Phylliroë - LU Phylliroidae Cephalopyge - LU LomanoƟdae Lomanotus - LR Cumanotus - BS Flabellinidae Flabellina cynara - BS Flabellina iodinea - LR Aeolidida Nudibranchia Flabellina telja - LR Flabellina trophina - NS Aeolidiidae Aeolidella - BS Hermissenda - LR Glaucidae Pteraeolidia - LR Armina - NS Dorididae Aphelodoris - DV Diaulula - NS Discodorididae Discodoris - DV Doridoidea Nudipleura Sebadoris - DV/DU Archidoris - NS Euctenidiacea Chromodoridae Hypselodoris - NS Doridacea Cadlina - NS Goniodorididae Trapania - LR Hexabranchidae Hexabranchus - DV/DU Polyceroidea Plocamopherus - LR Tamja - LR Polyceridae Nembrotha - LR Pleurobranchomorpha Triopha fulgarans - LR Triopha catalinae - NS Pleurobranchidae Pleurobranchaea - DV Tomthompsonia - ? Burthella - NS?
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From page 157... ...
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, Phylliroë bucephala, and Cephalopyge trematoides (Lalli and Gilmer, 1989)
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From page 158... ...
Dendronotus iris LR Kjerschow-Agersborg (1922) , Haefelfinger and Kress (1967)
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From page 159... ...
Melibe leonina LR Kjerschow-Agersborg (1921) , Hurst (1968)
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From page 160... ...
Chromodoridae a Archidoris odhneri NS a Archidoris montereyensis NS a Hypselodoris picta NS a Cadlina luteomarginata NS Onchidoridoidea Goniodorididae Trapania velox LRf Cockerell (1901) , Farmer (1970)
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From page 161... ...
. 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 Watson, 2002; Sakurai et al., 2011)
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From page 162... ...
LU swimming, which otherwise is found mostly in pelagic species, may be a further refinement of LR swimming. 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.
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From page 163... ...
. PHYLOGENETIC DISTRIBUTION OF SWIMMING BEHAVIORS 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.
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From page 164... ...
EVOLUTION OF SWIMMING BEHAVIORS There are a number of possible scenarios that could account for the phylogenetic distribution of swimming behaviors among the Nudipleura. Considering the extreme rarity of swimming, it is possible, maybe even likely, that swimming evolved on multiple occasions from nonswimming species.
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From page 165... ...
Hexabranchidae - DV/DU Hexabranchidae - DV/DU LR Polyceridae - LR LR Polyceridae - LR Pleurobranchidae - DV Pleurobranchidae - DV 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.
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From page 166... ...
NEURAL CIRCUITS UNDERLYING SWIMMING 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 rhythmic DV and LR movements originates from central pattern generator (CPG)
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From page 167... ...
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 compatible with any of the phylogenetic scenarios (Fig.
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From page 168... ...
A Tritonia diomedea B L-DSI DSI R-DSI L-C2 VSI C2 R-C2 10 mV sƟm 5 sec C Pleurobranchaea californica D R-A3 As A3 L-As IVS A1 A10 L-A1 20mV sƟm 5 sec FIGURE 9.4 Neural circuits and swim motor patterns for the DV swimmers Tritonia and Pleurobranchaea.
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From page 169... ...
This suggests that the swimming CPGs were built upon previously existing neural circuits, coopting existing neurons for new functions. The DV swim CPG neurons are not members of the LR swim CPGs.
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From page 170... ...
(F) In the Dendronotus swim motor pattern, the left and right Si2 fire alternating bursts of action potentials, but the Si1s fire irregularly.
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From page 171... ...
categorically distinct behaviors are produced by CPGs containing nonoverlapping sets of neurons. It was shown that the 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)
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From page 172... ...
A Melibe leonina B Dendronotus iris R-C2 L-DSI R-DSI R-DSI L-Si1 L-Pd 50 50 R-Si1 mV R-Pd mV 5 sec 5 sec FIGURE 9.6 Homologues of the Tritonia DV swim CPG neurons are not rhythmically active during LR swim motor patterns.
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From page 173... ...
There could be functional reasons; perhaps Si1, which is not rhythmically active in Dendronotus, has an additional function that is 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.
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From page 174... ...
. If homologous neurons are repeatedly incorporated into neural circuits for analogous behaviors, it suggests that these neurons may be part of a more readily achievable state for swimming.
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