Neural mechanisms underlying the evolvability of behaviour

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 366, Issue 1574, 2011, Pages 2086-2099

  Katz, Paul S ^a  

^a GEORGIA STATE UNIVERSITY   (United States)

Author keywords

Convergent evolution; Evolutionary development; Homologous neurons; Homoplasy; Neural circuits; Neuromodulation

Indexed keywords

ANATOMY; BEHAVIORAL ECOLOGY; CONVERGENT EVOLUTION; DEVELOPMENTAL BIOLOGY; GENETIC ANALYSIS; IDENTIFICATION METHOD; INVERTEBRATE; NERVOUS SYSTEM; NEUROLOGY; PHYLOGENETICS; SENSITIVITY ANALYSIS; VISUAL ANALYSIS;

ANIMAL; ANIMAL BEHAVIOR; EVOLUTION; GENE EXPRESSION REGULATION; GENETICS; NERVE CELL; NERVOUS SYSTEM FUNCTION; PHYSIOLOGY; REVIEW; SPECIES DIFFERENCE;

ANIMALS; BEHAVIOR, ANIMAL; BIOLOGICAL EVOLUTION; GENE EXPRESSION REGULATION, DEVELOPMENTAL; NERVOUS SYSTEM PHYSIOLOGICAL PHENOMENA; NEURONS; SPECIES SPECIFICITY;

ANIMALIA; INVERTEBRATA;

EID: 79959414305     PISSN: 09628436     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rstb.2010.0336     Document Type: Review

References (169)

1. Gilbert, S. F., Opitz, J. M. & Raff, R. A. 1996 Resynthesizing evolutionary and developmental biology. Dev. Biol. 173, 357-372. (doi:10.1006/dbio.1996.0032)
2. Hall, B. K. 1998 Evolutionary developmental biology, 2nd edn. London, UK: Chapman & Hall.
3. Raff, R. A. 2000 Evo-devo: the evolution of a new discipline. Nat.Rev. Genet. 1, 74-79. (doi:10.1038/35049594)
4. Kirschner, M. & Gerhart, J. 1998 Evolvability. Proc. Natl Acad. Sci. USA 95, 8420-8427. (doi:10.1073/ pnas.95.15.8420)
5. Hendrikse, J. L., Parsons, T. E. & Hallgrimsson, B. 2007 Evolvability as the proper focus of evolutionary developmental biology. Evol. Dev. 9, 393-401. (doi:10.1111/j.1525-142X.2007.00176.x)
6. von Dassow, G. & Munro, E. 1999 Modularity in animal development and evolution: elements of a conceptual framework for EvoDevo. J. Exp. Zool. 285, 307-325. (doi:10.1002/(SICI)1097-010X(19991215) 285:4,307::AID-JEZ2.3.0.CO;2-V)
7. Brakefield, P. M. 2006 Evo-devo and constraints on selection. Trends Ecol. Evol. 21, 362-368. (doi:10. 1016/j.tree.2006.05.001)
8. Wagner, A. 2005 Robustness, evolvability, and neutrality. FEBS Lett. 579, 1772-1778. (doi:10.1016/j. febslet.2005.01.063)
9. Pigliucci, M. 2008 Opinion: is evolvability evolvable? Nat. Rev. Genet. 9, 75-82. (doi:10.1038/nrg2278)
10. Wagner, A. 2008 Robustness and evolvability: a paradox resolved. Proc. R. Soc. B 275, 91-100. (doi:10.1098/ rspb.2007.1137)
11. Jones, A. G., Arnold, S. J. & Buerger, R. 2007 The mutation matrix and the evolution of evolvability. Evolution 61, 727-745. (doi:10.1111/j.1558-5646.2007. 00071.x)
12. Salazar-Ciudad, I. 2007 On the origins of morphological variation, canalization, robustness, and evolvability. Integr.Comp. Biol. 47, 390-400. (doi:10.1093/icb/icm075)
13. Earl, D. J. & Deem, M. W. 2004 Evolvability is a selectable trait. Proc. Natl Acad. Sci. USA 101, 11531-11536. (doi:10.1073/pnas.0404656101)
14. Niven, J. E., Graham, C. M. & Burrows, M. 2008 Diversity and evolution of the insect ventral nerve cord. Annu. Rev. Entomol. 53, 253-271. (doi:10.1146/annurev.ento.52.110405.091322)
15. Striedter, G. F. 2006 Pre ́cis of principles of brain evolution. Behav. Brain Sci. 29, 1-12. (doi:10.1017/ S0140525X06009010)
16. Bell, C. C., Han, V. & Sawtell, N. B. 2008 Cerebellumlike structures and their implications for cerebellar function. Annu. Rev. Neurosci. 31, 1-24. (doi:10.1146/annurev.neuro.30.051606.094225)
17. Kim, J. Y., Marzban, H., Chung, S. H., Watanabe, M., Eisenman, L. M. & Hawkes, R. 2009 Purkinje cell compartmentation of the cerebellum of microchiropteran bats. J. Comp. Neurol. 517, 193-209. (doi:10.1002/ cne.22147)
18. Johnson, J. I., Kirsch, J. A., Reep, R. L. & Switzer III, R. C. 1994 Phylogeny through brain traits: more characters for the analysis of mammalian evolution. Brain Behav. Evol. 43, 319-347. (doi:10.1159/000113643)
19. Buschbeck, E. K. 2000 Neurobiological constraints and fly systematics: how different types of neural characters can contribute to a higher level dipteran phylogeny. Evolution 54, 888-898. (doi:10.1111/j.0014-3820. 2000.tb00089.x)
20. Sinakevitch, I., Douglass, J. K., Scholtz, G., Loesel, R. & Strausfeld, N. J. 2003 Conserved and convergent organization in the optic lobes of insects and isopods, with reference to other crustacean taxa. J. Comp. Neurol. 467, 150-172. (doi:10.1002/cne.10925)
21. Arendt, D. 2008 The evolution of cell types in animals: emerging principles from molecular studies. Nat. Rev. Genet. 9, 868-882. (doi:10.1038/nrg2416)
22. Denes, A. S., Jekely, G., Steinmetz, P. R., Raible, F., Snyman, H., Prud'homme, B., Ferrier, D. E., Balavoine, G. & Arendt, D. 2007 Molecular architecture of annelid nerve cord supports common origin of nervous system centralization in bilateria. Cell 129, 277-288. (doi:10.1016/j.cell.2007.02.040)
23. Reichert, H. 2009 Evolutionary conservation of mechanisms for neural regionalization, proliferation and interconnection in brain development. Biol. Lett. 5, 112-116. (doi:10.1098/rsbl.2008.0337)
24. Buschbeck, E. K. & Strausfeld, N. J. 1997 The relevance of neural architecture to visual performance: phylogenetic conservation and variation in dipteran visual systems. J. Comp. Neurol. 383, 282-304. (doi:10.1002/ (SICI)1096-9861(19970707)383:3,282::AID-CNE2. 3.0.CO;2-#)
25. Strausfeld, N. J., Sinakevitch, I., Brown, S. M. & Farris, S. M. 2009 Ground plan of the insect mushroom body: functional and evolutionary implications. J. Comp. Neurol. 513, 265-291. (doi:10.1002/cne.21948)
26. Farris, S. M. & Roberts, N. S. 2005 Coevolution of generalist feeding ecologies and gyrencephalic mushroom bodies in insects. Proc. Natl Acad. Sci. USA 102, 17394-17399. (doi:10.1073/pnas.0508430102)
27. Shaw, S. R. & Meinertzhagen, I. A. 1986 Evolutionary progression at synaptic connections made by identified homologus neurones. Proc. Natl Acad. Sci. USA 83, 7961-7965. (doi:10.1073/pnas.83.20.7961)
28. Shaw, S. R. & Moore, D. 1989 Evolutionary remodeling in a visual-system through extensive changes in the synaptic connectivity of homologous neurons. Vis. Neurosci. 3, 405-410. (doi:10.1017/S0952523800005903)
29. Tierney, A. J. 1995 Evolutionary implications of neural circuit structure and function. Behav. Processes 35, 173-182. (doi:10.1016/0376-6357(95)00041-0)
30. Kavanau, J. L. 1990 Conservative behavioral evolution, the neural substrate. Anim. Behav. 39, 758-767.(doi:10.1016/S0003-3472(05)80387-2)
31. Wilczynski, W. 1984 Central neural systems subserving a homoplasous periphery. Am. Zool. 24, 755-763. (doi:10.1093/icb/24.3.755)
32. Catania, K. C. 2007 Epigenetic responses to a changing periphery: wagging the dog. In Evolution of nervous systems (ed. J. Kaas), pp. 143-151. Oxford, UK: Academic Press.
33. Pallas, S. L. 2007 Compensatory innervation in development and evolution. In Evolution of nervous systems (ed. J. Kaas), pp. 153-167. Oxford,UK: Academic Press.
34. Krubitzer, L. 2009 In search of a unifying theory of complex brain evolution. Ann. NY Acad. Sci. 1156, 44-67. (doi:10.1111/j.1749-6632.2009.04421.x)
35. Sison-Mangus, M. P., Bernard, G. D., Lampel, J. & Briscoe, A. D. 2006 Beauty in the eye of the beholder: the two blue opsins of lycaenid butterflies and the opsingene-driven evolution of sexually dimorphic eyes. J. Exp. Biol. 209, 3079-3090. (doi:10.1242/jeb.02360)
36. Caine, N. G. & Mundy, N. I. 2000 Demonstration of a foraging advantage for trichromatic marmosets (Callithrix geoffroyi) dependent on food colour. Proc. R. Soc. Lond. B 267, 439-444. (doi:10.1098/rspb.2000.1019)
37. Regan, B. C., Julliot, C., Simmen, B., Vienot, F., Charles-Dominique, P. & Mollon, J. D. 2001 Fruits, foliage and the evolution of primate colour vision. Phil. Trans. R. Soc. Lond. B 356, 229-283. (doi:10. 1098/rstb.2000.0773)
38. Lucas, P.W. et al. 2003 Evolution and function of routine trichromatic vision in primates. Evolution 57, 2636-2643. (doi:10.1111/j.0014-3820.2003.tb01506.x)
39. Smith, A. C., Buchanan-Smith, H. M., Surridge, A. K., Osorio, D. & Mundy, N. I. 2003 The effect of colour vision status on the detection and selection of fruits by tamarins (Saguinus spp.). J. Exp. Biol. 206, 3159-3165. (doi:10.1242/jeb.00536)
40. Pichaud, F., Briscoe, A. & Desplan, C. 1999 Evolution of color vision. Curr. Opin. Neurobiol. 9, 622-627. (doi:10.1016/S0959-4388(99)00014-8)
41. Briscoe, A. D. & Chittka, L. 2001 The evolution of color vision in insects. Annu. Rev. Entomol. 46, 471-510. (doi:10.1146/annurev.ento.46.1.471)
42. Awata, H., Wakakuwa, M. & Arikawa, K. 2009 Evolution of color vision in pierid butterflies: blue opsin duplication, ommatidial heterogeneity and eye regionalization in Colias erate. J. Comp. Physiol. A 195, 401-408. (doi:10.1007/s00359-009-0418-7)
43. Spaethe, J. & Briscoe, A. D. 2004 Early duplication and functional diversification of the opsin gene family in insects. Mol. Biol. Evol. 21, 1583-1594. (doi:10.1093/ molbev/msh162)
44. Frentiu, F. D., Bernard, G. D., Sison-Mangus, M. P., Brower, A. V. & Briscoe, A. D. 2007 Gene duplication is an evolutionary mechanism for expanding spectral diversity in the long-wavelength photopigments of butterflies. Mol. Biol. Evol. 24, 2016-2028. (doi:10.1093/ molbev/msm132)
45. Briscoe, A. D. 2000 Six opsins from the butterfly Papilio glaucus: molecular phylogenetic evidence for paralogous origins of red-sensitive visual pigments in insects. J. Mol. Evol. 51, 110-121. (doi:10.1007/s0023 90010071)
46. Briscoe, A. D. 2001 Functional diversification of lepidopteran opsins following gene duplication. Mol. Biol. Evol. 18, 2270-2279.
47. Briscoe, A. D. 2002 Homology modeling suggests a functional role for parallel amino acid substitutions between bee and butterfly red- and green-sensitive opsins. Mol. Biol. Evol. 19, 983-986.
48. Zhukovsky, E. A., Robinson, P. R. & Oprian, D. D. 1992 Changing the location of the Schiff base counterion in rhodopsin. Biochemistry 31, 10400-10405. (doi:10.1021/bi00157a030)
49. Frentiu, F. D., Bernard, G. D., Cuevas, C. I., Sison-Mangus, M. P., Prudic, K. L.& Briscoe,A.D. 2007 Adaptive evolution of color vision as seen through the eyes of butterflies. Proc. Natl Acad. Sci. USA 104(Suppl. 1), 8634-8640. (doi:10.1073/pnas.0701447104)
50. Wang, Y., Smallwood, P. M., Cowan, M., Blesh, D., Lawler, A. & Nathans, J. 1999 Mutually exclusive expression of human red and green visual pigmentreporter transgenes occurs at high frequency in murine cone photoreceptors. Proc. Natl Acad. Sci. USA 96, 5251-5256. (doi:10.1073/pnas.96.9.5251)
51. Smallwood, P. M., Wang, Y. & Nathans, J. 2002 Role of a locus control region in the mutually exclusive expression of human red and green cone pigment genes. Proc. Natl Acad. Sci. USA 99, 1008-1011. (doi:10.1073/pnas.022629799)
52. Smallwood, P. M., Olveczky, B. P., Williams, G. L., Jacobs, G. H., Reese, B. E., Meister, M. & Nathans, J. 2003 Genetically engineered mice with an additional class of cone photoreceptors: implications for the evolution of color vision. Proc. Natl Acad. Sci. USA 100, 11706-11711. (doi:10.1073/pnas.1934712100)
53. Jacobs, G. H., Williams, G. A., Cahill, H. & Nathans, J. 2007 Emergence of novel color vision in mice engineered to express a human cone photopigment. Science 315, 1723-1725. (doi:10.1126/science.1138838)
54. Mazzoni, E. O., Desplan, C. & Celik, A. 2004 'One receptor' rules in sensory neurons. Dev. Neurosci. 26, 388-395. (doi:10.1159/000082281)
55. Serizawa, S., Miyamichi, K., Nakatani, H., Suzuki, M., Saito, M., Yoshihara, Y. & Sakano, H. 2003 Negative feedback regulation ensures the one receptor-one olfactory neuron rule in mouse. Science 302, 2088-2094. (doi:10.1126/science.1089122)
56. Serizawa, S., Miyamichi, K. & Sakano, H. 2004 One neuron-one receptor rule in the mouse olfactory system. Trends Genet. 20, 648-653. (doi:10.1016/j.tig. 2004.09.006)
57. Mancuso, K., Hauswirth, W. W., Li, Q., Connor, T. B., Kuchenbecker, J. A., Mauck, M. C., Neitz, J. &Neitz M.2009 Gene therapy for red-green colour blindness in adult primates. Nature 461, 784-787. (doi:10.1038/ nature08401)
58. Neitz, J., Carroll, J., Yamauchi, Y., Neitz, M. & Williams, D. R. 2002 Color perception is mediated by a plastic neural mechanism that is adjustable in adults. Neuron 35, 783-792. (doi:10.1016/S0896-6273(02) 00818-8)
59. Wainwright, P. C., Sanford, C. P., Reilly, S. M. & Lauder, G. V. 1989 Evolution of motor patterns: aquatic feeding in salamanders and ray-finned fishes. Brain Behav. Evol. 34, 329-341. (doi:10.1159/ 000116519)
60. Friel, J. P. & Wainwright, P. C. 1998 Evolution of motor patterns in tetraodontiform fishes: does muscle duplication lead to functional diversification? Brain Behav. Evol. 52, 159-170. (doi:10.1159/000006560)
61. Wainwright, P. C. 2002 The evolution of feeding motor patterns in vertebrates. Curr. Opin. Neurobiol. 12, 691-695. (doi:10.1016/S0959-4388(02)00383-5)
62. Nishikawa, K. C., Anderson, C. W., Deban, S. M. & O'Reilly, J. C. 1992 The evolution of neural circuits controlling feeding behavior in frogs. Brain Behav. Evol. 40, 125-140. (doi:10.1159/000113908).
63. Smith, K. K. 1994 Are neuromotor systems conserved in evolution? Brain Behav. Evol. 43, 293-305. (doi:10. 1159/000113641)
64. Herrel, A., Meyers, J. J., Nishikawa, K. C. & De Vree, F. 2001 The evolution of feeding motor patterns in lizards:modulatory complexity and possible constraints. Am. Zool. 41, 1311-1320. (doi:10.1668/0003-1569(2001) 041[1311:TEOFMP]2.0.CO;2)
65. Konow, N. & Sanford, C. P. J. 2008 Is a convergently derived muscle-activity pattern driving novel raking behaviours in teleost fishes? J. Exp. Biol. 211, 989-999. (doi:10.1242/jeb.013078)
66. Rast, G. F. & Bräunig, P. 2001 Insect mouthpart motor patterns: central circuits modified for highly derived appendages? Neuroscience 108, 167-176. (doi:10.1016/ S0306-4522(01)00406-7)
67. Schaerlaeken, V., Meyers, J. J. & Herrel, A. 2007 Modulation of prey capture kinematics and the role of lingual sensory feedback in the lizard Pogona vitticeps. Zoology 110, 127-138. (doi:10.1016/j.zool.2006.09.002)
68. Lingle, S. 1992 Escape gaits of white-tailed deer, mule deer and their hybrids: gaits observed and patterns of limb coordination. Behaviour 122, 153-181. (doi:10. 1163/156853992X00499)
69. Hoy, R. R., Hahn, J. & Paul, R. C. 1977 Hybrid cricket auditory behavior: evidence for genetic coupling in animal communication. Science 195, 82-84. (doi:10. 1126/science.831260)
70. Graham Brown, T. 1911 The intrinsic factors in the act of progression in the mammal. Proc. R. Soc. Lond. B 84, 308-319. (doi:10.1098/rspb.1911.0077)
71. Stuart, D. G. & Hultborn, H. 2008 Thomas Graham Brown (1882-1965), Anders Lundberg 1920-), and the neural control of stepping. Brain Res. Rev. 59,74-95. (doi:10.1016/j.brainresrev.2008.06.001)
72. Kiehn, O. 2006 Locomotor circuits in the mammalian spinal cord. Annu. Rev. Neurosci. 29, 279-306. (doi:10.1146/annurev.neuro.29.051605.112910)
73. Kwan, A. C., Dietz, S. B., Webb, W. W. & Harris- Warrick, R. M. 2009 Activity of Hb9 interneurons during fictive locomotion in mouse spinal cord. J. Neurosci. 29, 11601-11613. (doi:10.1523/JNEUROSCI. 1612-09.2009)
74. Guertin, P. A. 2009 The mammalian central pattern generator for locomotion. Brain Res. Rev. 62, 45-56. (doi:10.1016/j.brainresrev.2009.08.002)
75. Brodfuehrer, P. D. & Thorogood, M. S. E. 2001 Identified neurons and leech swimming behavior. Prog. Neurobiol. 63, 371-381. (doi:10.1016/S0301-0082(00) 00048-4)
76. Comer, C. M. & Robertson, R. M. 2001 Identified nerve cells and insect behavior. Prog. Neurobiol. 63, 409-439. (doi:10.1016/S0301-0082(00)00051-4)
77. Croll, R. P. 1987 Identified neurons and cellular homologies. In Nervous systems in invertebrates (ed. M. A. Ali), pp. 41-59. New York, NY: Plenum Publishing Corporation.
78. Weiss, K. R. & Kupfermann, I. 1976 Homology of the giant serotonergic neurons (metacerebral cells) in Aplysia and pulmonate molluscs. Brain Res. 117, 33-49. (doi:10.1016/0006-8993(76)90554-0)
79. Benjamin, P. R. 1983 Gastropod feeding: behavioural and neural analysis of a complex multicomponent system. In Neural origin of rhythmic movements (eds A. Roberts & B. L. Roberts), pp. 159-193. Cambridge, UK: Cambridge University Press.
80. Wentzell, M. M., Martinez-Rubio, C., Miller, M. W. & Murphy, A. D. 2009 Comparative neurobiology of feeding in the opisthobranch sea slug, Aplysia, and the pulmonate snail, Helisoma: evolutionary considerations. Brain Behav. Evol. 74, 219-230. (doi:10.1159/ 000258668)
81. Katz, P. S. & Tazaki, K. 1992 Comparative and evolutionary aspects of the crustacean stomatogastric system. In Dynamic biological networks: the stomatogastric nervous system (eds R. M. Harris-Warrick, E. Marder, A. I. Selverston & M. Moulins), pp. 221-261. Cambridge, MA: MIT Press.
82. Paul, D. H. 1989 A neurophylogenist's view of decapod crustacea. Bull. Mar. Sci. 45, 487-504.
83. Paul, D. H. 1991 Pedigrees of neurobehavioral circuits: tracing the evolution of novel behaviors by comparing motor patterns, muscles, and neurons in members of related taxa. Brain Behav. Evol. 38, 226-239. (doi:10. 1159/000114390)
84. Paul, D. H. & Wilson, L. J. 1994 Replacement of an inherited stretch receptor by a newly evolved stretch receptor in hippid sand crabs. J. Comp. Neurol. 350, 150-160. (doi:10.1002/cne.903500111)
85. Paul, D. H. 2007 Evolutionary neuroethology: a case study: origins and evolution of novel forms of locomotion in Hippid sand crabs. In Evolution of nervous systems (ed. J. Kaas), pp. 99-119. Oxford, UK: Academic Press.
86. Golowasch, J., Goldman, M. S., Abbott, L. F. & Marder, E. 2002 Failure of averaging in the construction of a conductance-based neuron model. J. Neurophysiol. 87,129-1131.
87. Prinz, A. A., Bucher, D. & Marder, E. 2004 Similar network activity from disparate circuit parameters. Nat. Neurosci. 7, 1345-1352. (doi:10.1038/nn1352)
88. Marder, E. & Prinz, A. A. 2002 Modeling stability in neuron and network function: the role of activity in homeostasis. BioEssays 24, 1145-1154. (doi:10.1002/ bies.10185)
89. Saideman, S. R., Blitz, D. M. & Nusbaum, M. P. 2007 Convergent motor patterns from divergent circuits. J. Neurosci. 27, 6664-6674. (doi:10.1523/JNEUROSCI. 0315-07.2007)
90. Goaillard, J. M., Taylor, A. L., Schulz, D. J. & Marder, E. 2009 Functional consequences of animal-to-animal variation in circuit parameters. Nat. Neurosci. 12, 1424-1430. (doi:10.1038/nn.2404)
91. Marder, E. & Goaillard, J. M. 2006 Variability, compensation and homeostasis in neuron and network function. Nat. Rev. Neurosci. 7, 563-574. (doi:10. 1038/nrn1949)
92. Bucher, D., Prinz, A. A. & Marder, E. 2005 Animal-toanimal variability in motor pattern production in adults and during growth. J. Neurosci. 25, 1611-1619. (doi:10.1523/JNEUROSCI.3679-04.2005)
93. Marder, E. & Prinz, A. A. 2003 Current compensation in neuronal homeostasis. Neuron 37, 2-4. (doi:10.1016/ S0896-6273(02)01173-X)
94. Harris-Warrick, R. M. & Marder, E. 1991 Modulation of neural networks for behavior. Annu. Rev. Neurosci. 14, 39-57. (doi:10.1146/annurev.ne.14.030191.000351)
95. Marder, E. & Bucher, D. 2007 Understanding circuit dynamics using the stomatogastric nervous system of lobsters and crabs. Annu. Rev. Physiol. 69, 291-316. (doi:10.1146/annurev.physiol.69.031905.161516)
96. Katz, P. S. & Calin-Jageman, R. 2008 Neuromodulation. In New Encyclopedia of neuroscience (ed. L. R. Squire), pp. 497-503. New York, NY: Academic Press.
97. Katz, P. S. 1991 Neuromodulation and the evolution of a simple motor system. Semin. Neurosci. 3, 379-389. (doi:10.1016/1044-5765(91)90028-M)
98. Arbas, E. A., Meinertzhagen, I. A. & Shaw, S. R. 1991 Evolution in nervous systems. Annu. Rev. Neurosci. 14, 9-38. (doi:10.1146/annurev.ne.14.030191.000301)
99. Meyrand, P., Faumont, S., Simmers, J., Christie, A. E. & Nusbaum, M. P. 2000 Species-specificmodulation of pattern- generating circuits. Eur. J. Neurosci. 12, 2585-2596. (doi:10.1046/j.1460-9568.2000.00121.x)
100. Fenelon, V. S., Le Feuvre, Y. & Meyrand, P. 2004 Phylogenetic, ontogenetic and adult adaptive plasticity of rhythmic neural networks: a common neuromodulatory mechanism? J. Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol. 190, 691-705.
101. Beltz, B., Eisen, J. S., Flamm, R. E., Harris-Warrick, R. M., Hooper, S. L. & Marder, E. 1984 Serotonergic innervation and modulation of the stomatogastric ganglion of three decapod crustaceans (Panulirus interruptus, Homarus americanus and Cancer irroratus). J. Exp. Biol. 109, 35-54.
102. Wright,W.G., Kirschman, D., Rozen, D. & Maynard, B. 1996 Phylogenetic analysis of learning-related neuromodulation in molluscan mechanosensory neurons. Evolution 50, 2248-2263. (doi:10.2307/2410695)
103. Wright, W. G. 1998 Evolution of non-associative learning: behavioral analysis of a phylogenetic lesion. Neurobiol. Learn. Mem. 69, 326-337. (doi:10.1006/ nlme.1998.3829)
104. Erixon, N. J., Demartini, L. J. & Wright, W. G. 1999 Dissociation between sensitization and learning-related neuromodulation in an aplysiid species. J. Comp. Neurol. 408, 506-514. (doi:10.1002/(SICI)1096-9861 (19990614)408:4,506::AID-CNE5.3.0.CO;2-P)
105. McLean, D. L. & Sillar, K. T. 2004 Divergent actions of serotonin receptor activation during fictive swimming in frog embryos. J. Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol. 190, 391-402. (doi:10.1007/ s00359-004-0504-9)
106. Merrywest, S. D., McLean, D. L., Buchanan, J. T. & Sillar, K. T. 2004 Evolutionary divergence in developmental strategies and neuromodulatory control systems of two amphibian locomotor networks. Integr. Comp. Biol. 44, 47-56. (doi:10.1093/icb/44.1.47)
107. Newcomb, J. M. & Katz, P. S. 2009 Different functions for homologous serotonergic interneurons and serotonin in species-specific rhythmic behaviours. Proc. R. Soc.B 276, 99-108. (doi:10.1098/rspb.2008.0683)
108. Katz, P. S. & Newcomb, J. M. 2007 A tale of two CPGs: phylogenetically polymorphic networks. In Evolution of nervous systems (ed. J. H. Kaas), pp. 367-374. Oxford, UK: Academic Press.
109. Jing, J. & Gillette, R. 1999 Central pattern generator for escape swimming in the notaspid sea slug Pleurobranchaea californica. J. Neurophysiol. 81, 654-667.
110. Katz, P. S. 2009 Tritonia swim network. Scholarpedia 4, 3638. (doi:10.4249/scholarpedia.3638)
111. Getting, P. A., Lennard, P. R. & Hume, R. I. 1980 Central pattern generator mediating swimming in Tritonia. I. Identification and synaptic interactions. J. Neurophysiol. 44, 151-164.
112. Jing, J. & Gillette, R. 1995 Neuronal elements that mediate escape swimming and suppress feeding behavior in the predatory sea slug Pleurobranchaea. J. Neurophysiol. 74, 1900-1910.
113. Wollscheid, E. & Waegele, H. 1999 Initial results on the molecular phylogeny of the Nudibranchia (Gastropoda, Opisthobranchia) based on 18S rDNA data. Mol Phylogenet Evol 13, 215-226. (doi:10.1006/mpev.1999.0664)
114. Vonnemann, V., Schrodl, M., Klussmann-Kolb, A. & Wagele, H. 2005 Reconstruction of the phylogeny of the Opisthobranchia (Mollusca: Gastropoda) by means of 18S and 28S rRNA gene sequences. J. Mollus Stud. 71, 113-125. (doi:10.1093/mollus/ eyi014)
115. Bouchet, P., Rocroi, J. P., Fryda, J., Hausdorf, B., Ponder, W., Valdes, A. & Waren, A. 2005 Classification and nomenclator of gastropod families. Malacologia 47, 1-368.
116. Waegele, H. & Willan, R. C. 2000 Phylogeny of the nudibranchia. Zool. J. Linnean Soc. 130, 83-181. (doi:10.1111/j.1096-3642.2000.tb02196.x)
117. Wollscheid-Lengeling, E., Boore, J., Brown, W. & Waegele, H. 2001 The phylogeny of Nudibranchia (Opisthobranchia, Gastropoda, Mollusca) reconstructed by three molecular markers. Organ. Divers. Evol. 1, 241-256. (doi:10.1078/1439-6092-00022)
118. Grande, C., Templado, J., Cervera, J. L. & Zardoya, R. 2004 Phylogenetic relationships among Opisthobranchia (Mollusca: Gastropoda) based on mitochondrial cox 1, trnV, and rrnL genes. Mol. Phylogenet. Evol. 33, 378-388. (doi:10.1016/j.ympev.2004.06.008)
119. Newcomb, J. M. & Katz, P. S. 2007 Homologues of serotonergic central pattern generator neurons in related nudibranch molluscs with divergent behaviors. J. Comp. Physiol. A 193, 425-443. (doi:10.1007/ s00359-006-0196-4)
120. Watson, W. H., Lawrence, K. A. & Newcomb, J. M. 2001 Neuroethology of Melibe leonina swimming behavior. Am. Zool. 41, 1026-1035. (doi:10.1668/0003- 1569(2001)041[1026:NOMLSB]2.0.CO;2)
121. Lawrence, K. A. & Watson, W. H. 2002 Swimming behavior of the nudibranch Melibe leonina. Biol. Bull. 203, 144-151. (doi:10.2307/1543383)
122. Thompson, S. & Watson, W. H. 2005 Central pattern generator for swimming in Melibe. J. Exp. Biol. 208, 1347-1361. (doi:10.1242/jeb.01500)
123. Katz, P. S., Getting, P. A. & Frost,W. N. 1994 Dynamic neuromodulation of synaptic strength intrinsic to a central pattern generator circuit. Nature 367, 729-731. (doi:10.1038/367729a0)
124. Katz, P. S. & Frost,W.N. 1995 Intrinsic neuromodulation in the Tritonia swimCPG: serotoninmediates both neuromodulation and neurotransmission by the dorsal swim interneurons. J. Neurophysiol. 74, 2281-2294.
125. Katz, P. S. & Frost, W. N. 1995 Intrinsic neuromodulation in the Tritonia swim CPG: the serotonergic dorsal swim interneurons act presynaptically to enhance transmitter release from interneuron C2. J. Neurosci. 15, 6035-6045.
126. Sakurai, A. & Katz, P. S. 2003 Spike timing-dependent serotonergic neuromodulation of synaptic strength intrinsic to a central pattern generator circuit. J. Neurosci. 23, 10745-10755.
127. McClellan, A. D., Brown, G. D. & Getting, P. A. 1994 Modulation of swimming in Tritonia: excitatory and inhibitory effects of serotonin. J. Comp. Physiol. A 174, 257-266. (doi:10.1007/BF00193792)
128. Fickbohm, D. J. & Katz, P. S. 2000 Paradoxical actions of the serotonin precursor 5-hydroxytryptophan on the activity of identified serotonergic neurons in a simple motor circuit. J. Neurosci. 20, 1622-1634.
129. Jing, J., Vilim, F. S., Cropper, E. C. &Weiss, K. R. 2008 Neural analog of arousal: persistent conditional activation of a feeding modulator by serotonergic initiators of locomotion. J. Neurosci. 28, 12349-12361. (doi:10. 1523/JNEUROSCI.3855-08.2008)
130. Tian, L. M., Kawai, R. & Crow, T. 2006 Serotoninimmunoreactive CPT interneurons in Hermissenda: identification of sensory input and motor projections. J. Neurophysiol. 96, 327-335. (doi:10.1152/jn. 00035.2006)
131. Satterlie, R.A., Norekian,T. P., Jordan, S.& Kazilek, C. J. 1995 Serotonergic modulation of swimming speed in the pteropod mollusc Clione limacina. I. Serotonin immunoreactivity in the central nervous system and wings. J. Exp. Biol. 198, 895-904.
132. Popescu, I. R. & Frost, W. N. 2002 Highly dissimilar behaviors mediated by a multifunctional network in the marine mollusk Tritonia diomedea. J. Neurosci. 22, 1985-1993.
133. Jing, J. & Gillette, R. 2000 Escape swim network interneurons have diverse roles in behavioral switching and putative arousal in Pleurobranchaea. J. Neurophysiol. 83, 1346-1355.
134. Nishikawa, K. C. 2002 Evolutionary convergence in nervous systems: insights from comparative phylogenetic studies. Brain Behav. Evol. 59, 240-249. (doi:10.1159/000063561)
135. Kivell, T. L. & Schmitt, D. 2009 Independent evolution of knuckle-walking in African apes shows that humans did not evolve from a knuckle-walking ancestor. Proc. Natl Acad. Sci. USA 106, 14241-14246. (doi:10. 1073/pnas.0901280106)
136. Janis, C. M., Theodor, J. M. & Boisvert, B. 2002 Locomotor evolution in camels revisited: a quantitative analysis of pedal anatomy and the acquisition of the pacing gait. J. Vertebr. Paleontol. 22, 110-121. (doi:10. 1671/0272-4634(2002)022[0110:LEICRA]2.0.CO;2)
137. Whiting, M. F., Bradler, S. & Maxwell, T. 2003 Loss and recovery of wings in stick insects. Nature 421, 264-267. (doi:10.1038/nature01313)
138. Padberg, J., Franca, J. G., Cooke, D. F., Soares, J. G., Rosa, M. G., Fiorani Jr, M., Gattass, R. & Krubitzer, L. 2007 Parallel evolution of cortical areas involved in skilled hand use. J. Neurosci. 27, 10106-10115. (doi:10.1523/ JNEUROSCI.2632-07.2007)
139. Catania, K. C. 2000 Cortical organization in Insectivora: the parallel evolution of the sensory periphery and the brain. Brain Behav. Evol. 55, 311-321. (doi:10.1159/000006666)
140. Karlen, S. J. & Krubitzer, L. 2007 The functional and anatomical organization of marsupial neocortex: evidence for parallel evolution across mammals. Prog. Neurobiol. 502, 414-426.
141. Wullimann, M., Hofmann, M. H. & Meyer, D. L. 1991 Histochemical connectional and cytoarchitectonic evidence for a secondary reduction of the pretectum in the European eel Anguilla anguilla: a case of parallel evolution. Brain Behav. Evol. 38, 290-301. (doi:10. 1159/000114395)
142. Jarvis, E. D. &Mello, C. V. 2000 Molecular mapping of brain areas involved in parrot vocal communication. J. Comp. Neurol. 419, 1-31. (doi:10.1002/(SICI)1096- 9861(20000327)419:1,1::AID-CNE1.3.0.CO;2-M)
143. Jarvis, E. D. 2007 Neural systems for vocal learning in birds and humans: a synopsis. J. Ornithol. 148, 35-44. (doi:10.1007/s10336-007-0243-0)
144. Feenders, G., Liedvogel, M., Rivas, M., Zapka, M., Horita, H., Hara, E., Wada, K., Mouritsen, H. & Jarvis, E. D. 2008 Molecular mapping of movementassociated areas in the avian brain: a motor theory for vocal learning origin. PLoS ONE 3, 1768. (doi:10. 1371/journal.pone.0001768)
145. Bullock, T. H., Bodznick, D. A. & Northcutt, R. G. 1983 The phylogenetic distribution of electroreception: evidence for convergent evolution of a primitive vertebrate sense modality. Brain Res. 287, 25-46.
146. Kawasaki, M. 1993 Independently evolved jamming avoidance responses employ identical computational algorithms: a behavioral study of the African electric fish, Gymnarchus niloticus. J. Comp. Physiol. A 173, 9-22. (doi:10.1007/BF00209614)
147. Alves-Gomes, J. A., Orti, G., Haygood, M., Heiligenberg, W. & Meyer, A. 1995 Phylogenetic analysis of the South American electric fishes (order Gymnotiformes) and the evolution of their electrogenic system: a synthesis based on morphology, electrophysiology, and mitochondrial sequence data. Mol. Biol. Evol. 12, 298-318.
148. Hopkins, C. D. 1995 Convergent designs for electrogenesis and electroreception. Curr. Opin. Neurobiol. 5, 769-777. (doi:10.1016/0959-4388(95)80105-7)
149. Kawasaki, M. 1996 Comparative analysis of the jamming avoidance response in African and South American wave-type electric fishes. Biol. Bull. 191, 103-108. (doi:10.2307/1543070)
150. New, J. G. 1997 The evolution of vertebrate electrosensory systems. Brain Behav. Evol. 50, 244-252. (doi:10. 1159/000113338)
151. Kawasaki, M. 2009 Evolution of time-coding systems in weakly electric fishes. Zool. Sci. 26, 587-599. (doi:10. 2108/zsj.26.587)
152. Zakon, H. H., Zwickl, D. J., Lu, Y. & Hillis, D. M. 2008 Molecular evolution of communication signals in electric fish. J. Exp. Biol. 211, 1814-1818. (doi:10.1242/ jeb.015982)
153. Rose, G. J. 2004 Insights into neural mechanisms and evolution of behaviour from electric fish. Nat. Rev. Neurosci. 5, 943-951. (doi:10.1038/nrn1558)
154. Zakon, H. H., Lu, Y., Zwickl, D. J. & Hillis, D. M. 2006 Sodium channel genes and the evolution of diversity in communication signals of electric fishes: convergent molecular evolution. Proc. Natl Acad. Sci. USA 103, 3675-3680. (doi:10.1073/pnas. 0600160103)
155. Hammock, E. A. 2007 Gene regulation as a modulator of social preference in voles. Adv. Genet. 59, 107-127. (doi:10.1016/S0065-2660(07)59004-8)
156. Lim, M. M. & Young, L. J. 2006 Neuropeptidergic regulation of affiliative behavior and social bonding in animals. Horm. Behav. 50, 506-517. (doi:10.1016/j. yhbeh.2006.06.028)
157. Nair, H. P. & Young, L. J. 2006 Vasopressin and pairbond formation: genes to brain to behavior. Physiology (Bethesda) 21, 146-152.
158. Lim, M. M., Hammock, E. A. & Young, L. J. 2004 The role of vasopressin in the genetic and neural regulation of monogamy. J. Neuroendocrinol. 16, 325-332. (doi:10. 1111/j.0953-8194.2004.01162.x)
159. Young, L. J. & Wang, Z. 2004 The neurobiology of pair bonding. Nat. Neurosci. 7, 1048-1054. (doi:10. 1038/nn1327)
160. Young, L. J., Murphy Young, A. Z. & Hammock, E. A. 2005 Anatomy and neurochemistry of the pair bond. J. Comp. Neurol. 493, 51-57. (doi:10.1002/cne.20771)
161. Lim, M. M., Wang, Z., Olazabal, D. E., Ren, X., Terwilliger, E. F. & Young, L. J. 2004 Enhanced partner preference in a promiscuous species by manipulating the expression of a single gene. Nature 429, 754-757. (doi:10.1038/nature02539)
162. Young, L. J. 1999 Oxytocin and vasopressin receptors and species-typical social behaviors. Horm. Behav. 36, 212-221. (doi:10.1006/hbeh.1999.1548)
163. Smith, K. S., Tindell, A. J., Aldridge, J. W. & Berridge, K. C. 2009 Ventral pallidum roles in reward and motivation. Behav. Brain Res. 196, 155-167. (doi:10.1016/j. bbr.2008.09.038)
164. Hammock, E. A. & Young, L. J. 2002 Variation in the vasopressin V1a receptor promoter and expression: implications for inter- and intraspecific variation in social behaviour. Eur. J. Neurosci. 16, 399-402. (doi:10.1046/j.1460-9568.2002.02083.x)
165. Hammock, E. A. & Young, L. J. 2004 Functional microsatellite polymorphism associated with divergent social structure in vole species. Mol. Biol. Evol. 21, 1057-1063. (doi:10.1093/molbev/msh104)
166. Hammock, E. A. & Young, L. J. 2005 Microsatellite instability generates diversity in brain and sociobehavioral traits. Science 308, 1630-1634. (doi:10.1126/ science.1111427)
167. Donaldson, Z. R., Kondrashov, F. A., Putnam, A., Bai, Y., Stoinski, T. L., Hammock, E. A. & Young, L. J. 2008 Evolution of a behavior-linked microsatellite-containing element in the 50 flanking region of the primate AVPR1A gene. BMC Evol. Biol. 8, 180. (doi:10.1186/ 1471-2148-8-180)
168. Heckel, G. & Fink, S. 2008 Evolution of the arginine vasopressin 1a receptor and implications for mammalian social behaviour. Prog. Brain Res. 170, 321-330. (doi:10.1016/S0079-6123(08)00426-3)
169. Orr, H. A. 2005 The probability of parallel evolution. Evolution 59, 216-220. (doi:10.1111/j.0014-3820. 2005.tb00907.x)