Stabilizing selection on behavior and morphology masks positive selection on the signal in a salamander pheromone signaling complex

Molecular Biology and Evolution

Volumn 21, Issue 6, 2004, Pages 1032-1041

  Watts, Richard A ^a   Palmer, Catherine A ^a   Feldhoff, Richard C ^b,c   Feldhoff, Pamela W ^b,c   Houck, Lynne D ^a   Jones, Adam G ^a   Pfrender, Michael E ^d   Rollmann, Stephanie M ^e   Arnold, Stevan J ^a  

^a OREGON STATE UNIVERSITY   (United States)

^b University of Louisville School of Medicine   (United States)

^c GEORGIA INSTITUTE OF TECHNOLOGY   (United States)

^d UTAH STATE UNIVERSITY   (United States)

^e NORTH CAROLINA STATE UNIVERSITY   (United States)

Author keywords

Cytokine; Pheromone; Pheromone delivery; Plethodontid receptivity factor; Positive selection

Indexed keywords

CYTOKINE; PHEROMONE; PLETHODONTID RECEPTIVITY FACTOR; UNCLASSIFIED DRUG;

ALLELE; ALPHA HELIX; ANIMAL BEHAVIOR; ARTICLE; BINDING SITE; COURTSHIP; MOLECULAR CLONING; MOLECULAR EVOLUTION; MOLECULAR PHYLOGENY; MORPHOLOGY; NATURAL SELECTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PROTEIN FUNCTION; REPRODUCTION; SALAMANDER; VERTEBRATE;

AMINO ACID SEQUENCE; ANIMALS; BASE SEQUENCE; DNA PRIMERS; EXOCRINE GLANDS; LIKELIHOOD FUNCTIONS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PHEROMONES; PHYLOGENY; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SELECTION (GENETICS); SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS, DNA; SEXUAL BEHAVIOR, ANIMAL; SPECIES SPECIFICITY; TOOTH; URODELA;

AMPHIUMA MEANS; ANIMALIA; CAUDATA; PLETHODON; VERTEBRATA;

EID: 2442700222     PISSN: 07374038     EISSN: None     Source Type: Journal    
DOI: 10.1093/molbev/msh093     Document Type: Article

References (61)

1. Arnold, S. J. 1976. Sexual behavior, sexual interference, and sexual defense in the salamanders Ambystoma maculatum, Ambystoma tigrinum and Plethodon jordani. Z. Tierpsychol. 42:247-300.
2. -. 1977. The courtship behavior of North American salamanders with some comments on Old World salamandrids. Pp. 141-83 in D. Taylor and S. Guttman, eds. The reproductive biology of amphibians. Plenum Press, New York.
3. Arnold, S. J., and L. D. Houck 1982. Courtship pheromones: evolution by natural and sexual selection. Pp. 173-211 in M. Nitecke, ed. Biochemical aspects of evolutionary biology. University of Chicago Press, Chicago.
4. Barrier, M., C. D. Bustamante, J. Yu, and M. D. Purugganan. 2003. Selection on rapidly evolving proteins in the Arabidopsis genome. Genetics 163:723-733.
5. Behncken, S. N., S. W. Rowlinson, J. E. Rowland, B. L. Conway-Campbell, T. A. Monks, and M. J. Waters. 1997. Aspartate 171 is the major primate-specific determinant of human growth hormone: engineering porcine growth hormone to activate the human receptor. J. Biol. Chem. 272:27077-27083.
6. Boag, P. T., and P. R. Grant. 1981. Intense natural selection in a population of Darwin's finches (Geospizinae) in the Galapagos. Science 214:82-85.
7. Boulanger, M. J., A. J. Bankovich, T. Kortemme, D. Baker, and K. C. Garcia. 2003. Convergent mechanisms for recognition of divergent cytokines by the shared signaling receptor gp130. Mol Cell 12:577-589.
8. Bravo, J., and J. K. Heath. 2000. Receptor recognition by gp130 cytokines. EMBO J. 19:2399-2411.
9. Chapman, T., G. Arnqvist, J. Bangham, and L. Rowe. 2003. Sexual conflict. Trends Ecol. Evol. 18:41-47.
10. Charlesworth, B. R., R. Lande, and M. Slatkin. 1982. A neo-Darwinian commentary on macroevolution. Evolution 36:474-498.
11. Ciapponi, L., R. Graziani, G. Paonessa, A. Lahm, G. Ciliberto, and R. Savino. 1995. Definition of a composite binding site for gp130 in human interleukin-6. J. Biol. Chem. 270:31249-32154.
12. Clackson, T., and J. A. Wells. 1995. A hot spot of binding energy in a hormone-receptor interface. Science 267:383-386.
13. Clarke, M., and R. F. McMahon. 1996. Comparison of byssal attachment in dreissenid and mytilid mussels: mechanisms, morphology, secretion, biochemistry, mechanics and environmental influences. Malacol. Rev. 29:25.
14. Downes, S., and R. Shine. 1998. Sedentary snakes and gullible geckos: predator-prey coevolution in nocturnal rock-dwelling reptiles. Anim. Behav. 55:1373-1385.
15. Duda, T. F., Jr., and S. R. Palumbi. 1999. Molecular genetics of ecological diversification: duplication and rapid evolution of toxin genes of the venomous gastropod Conus. Proc. Natl. Acad. Sci. USA 96:6820-6823.
16. Endo, T., K. Ikeo, and T. Gojobori. 1996. Large-scale search for genes on which positive selection may operate. Mol Biol Evol 13:685-690.
17. Feldhoff, R. C., S. M. Rollmann, and L. D. Houck. 1999. Chemical analyses of courtship pheromones in a plethodontid salamander. Pp. 117-125 in R. E. Johnston, D. Muller-Schwarze, and P. Sorensen, eds. Advances in chemical communication in vertebrates. Plenum Press, New York.
18. Gavrilets, S. 2000. Rapid evolution of reproductive barriers driven by sexual conflict. Nature 403:886-889.
19. Gavrilets, S., and D. Waxman. 2002. Sympatric speciation by sexual conflict. Proc. Natl. Acad. Sci. USA 99:10533-10538.
20. Highton, R. 1962. Revision of North American salamanders of the genus Plethodon. Bull. Florida State Mus. 6:235-367.
21. Highton, R., and A. Larson. 1979. The genetic relationships of the salamanders of the genus Plethodon. Syst. Zool. 28:579-599.
22. Highton, R., and R. B. Peabody. 2000. Geographic protein variation and speciation in salamanders of the Plethodon jordani and Plethodon glutinosus complexes in the southern Appalachian Mountains with the descriptions of four new species. Pp. 31-94 in R. C. Bruce, R. G. Jaeger, and L. D. Houck, eds. The biology of plethdontid salamanders. Plenum Press, New York.
23. Hill, E. E., V. Morea, and C. Chothia. 2002. Sequence conservation in families whose members have little or no sequence similarity: the four-helical cytokines and cytochromes. J. Mol. Biol. 322:205-233.
24. Houck, L. D., and S. J. Arnold. 2003. Courtship and mating behavior. Pp. 383-424 in D. M. Sever, ed. Reproductive biology and phylogeny of Urodela. Science Publishers, Enfield, New Hampshire.
25. Houck, L. D., and N. L. Reagan. 1990. Male courtship pheromones increase female receptivity in a plethodontid salamander. Anim. Behav. 39:729-734.
26. Houck, L. D., and D. M. Sever. 1994. Role of the skin in reproduction and behaviour. Pp. 351-381 in H. Heatwole and G. T. Barthalmus, eds. Amphibian biology, Vol. 1. The integument. Surrey Beatty & Sons, New South Wales, Australia.
27. Hudson, K. R., A. B. Vernallis, and J. K. Heath. 1996. Characterization of the receptor binding sites of human leukemia inhibitory factor and creation of antagonists. J. Biol. Chem. 271:11971-11978.
28. Kallen, K. J., J. Grotzinger, E. Lelievre, P. Vollmer, D. Aasland, C. Renne, J. Mullberg, K. H. Myer zum Buschenfelde, H. Gascan, and S. Rose-John. 1999. Receptor recognition sites of cytokines are organized as exchangeable modules: transfer of the leukemia inhibitory factor receptor-binding site from ciliary neurotrophic factor to interleukin-6. J. Biol. Chem. 274:11859-11867.
29. Kimura, M. 1983. The neutral theory of molecular evolution. Cambridge University Press, Cambridge, UK.
30. King, D. P., M. D. Schrenzel, M. L. McKnight, T. H. Reidarson, K. D. Hanni, J. L. Stott, and D. A. Ferrick. 1996. Molecular cloning and sequencing of interleukin 6 cDNA fragments from the harbor seal (Phoca vitulina), killer whale (Orcinus orca), and southern sea otter (Enhydra lutris nereis). Immunogenetics 43:190-195.
31. Kingsolver, J. G., H. E. Hoekstra, J. M. Hoekstra, D. Berrigan, S. N. Vignieri, C. E. Hill, A. Hoang, P. Giber, and P. Beerli. 2001. The strength of phenotypic selection in natural populations. Am. Nat. 157:245-261.
32. Klauber, L. M. 1956. Rattlesnakes: their habits, life histories, and influence on mankind. University of California Press, Berkeley, Calif.
33. Lande, R. 1976. Natural selection and random genetic drift in phenotypic evolution. Evolution 30:314-334.
34. -. 1981. Models of speciation by sexual selection on polygenic traits. Proc. Natl. Acad. Sci. USA 78:3721-3725.
35. Larson, A., D. B. Wake, L. R. Maxson, and R. Highton. 1981. A molecular phylogenetic perspective on the origins of morphological novelties in the salamanders of the tribe Plethodontini. (Amphibia, Plethodontidae). Evolution 35:405-422.
36. Larson, A., D. W. Weisrock, and K. H. Kozak. 2003. Phylogenetic systematics of salamanders (Amphibia: Urodela): a review. Pp. 31-108 in D. M. Sever, ed. Reproductive biology and phylogeny of Urodela. Science Publishers, Enfield, New Hampshire.
37. Li, W.-H. 1997. Molecular evolution. Sinauer Associates, Sunderland, Mass.
38. Liu, J. C., K. D. Makova, R. M. Adkins, S. Gibson, and W. H. Li. 2001. Episodic evolution of growth hormone in primates and emergence of the species specificity of human growth hormone receptor. Mol. Biol. Evol. 18:945-953.
39. Lofstedt, C. 1993. Moth pheromone genetics and evolution. Philos. Trans. R. Soc. Lond. B Biol. Sci. 340:167-177.
40. Lynch, M. 1990. The rate of morphological evolution in mammals from the standpoint of the neutral expectation. Am. Nat. 136:727-741.
41. Miller, G. T., and S. Pitnick. 2002. Sperm-female coevolution in Drosophila. Science 298:1230-1233.
42. Moore, P. S., C. Boshoff, R. A. Weiss, and Y. Chang. 1996. Molecular mimicry of human cytokine and cytokine response pathway genes by KSHV. Science 274:1739-1744.
43. Mundy, N. I., and S. Cook. 2003. Positive selection during the diversification of class I vomeronasal receptor-like (V1RL) genes, putative pheromone receptor genes, in human and primate evolution. Mol. Biol. Evol. 20:1805-1810.
44. Olivera, B. M. 1999. Conus venom peptides: correlating chemistry and behavior. J. Comp. Physiol. A Sens. Neural. Behav. Physiol. 185:353-359.
45. Opell, B. D. 1999. Changes in spinning anatomy and thread stickiness associated with the origin of orb-weaving spiders. Biol. J. Linn. Soc. 68:593-612.
46. Panayotatos, N., E. Radziejewska, A. Acheson, R. Somogyi, A. Thadani, W. A. Hendrickson, and N. Q. McDonald. 1995. Localization of functional receptor epitopes on the structure of ciliary neurotrophic factor indicates a conserved, function-related epitope topography among helical cytokines. J Biol Chem 270:14007-14014.
47. Parker, G. A., and L. Partridge. 1998. Sexual conflict and speciation. Philos. Trans. R. Soc. Lond. B Biol. Sci. 353:261-274.
48. Roelofs, W. L., W. T. Liu, G. X. Hao, H. M. Jiao, A. P. Rooney, and C. E. Linn. 2002. Evolution of moth sex pheromones via ancestral genes. Proc. Natl. Acad. Sci. USA 99:13621-13626.
49. Rollmann, S. M., L. D. Houck, and R. C. Feldhoff. 1999. Proteinaceous pheromone affecting female receptivity in a terrestrial salamander. Science 285:1907-1909.
50. Ruben, J. A., N. L. Reagan, P. A. Verrell, and A. J. Boucot. 1993. Plethodontid salamander origins: a response to Beachy and Bruce. Am. Nat. 142:1038-1051.
51. Schubart, C. D., R. Diesel, and S. B. Hedges. 1998. Rapid evolution to terrestrial life in Jamaican crabs. Nature 393:363-365.
52. Stahl, E. A., and J. G. Bishop. 2000. Plant-pathogen arms races at the molecular level. Curr. Opin. Plant Biol. 3:299-304.
53. Swanson, W. J., and V. D. Vacquier. 2002. The rapid evolution of reproductive proteins. Nat. Rev. Genet. 3:137-144.
54. Wells, J. A. 1996. Binding in the growth hormone receptor complex. Proc. Natl. Acad. Sci. USA 93:1-6.
55. Willett, C. S. 2000. Evidence for directional selection acting on pheromone-binding proteins in the genus Choristoneura. Mol. Biol. Evol. 17:553-562.
56. Wirsig-Wiechmann, C. R., L. D. Houck, P. W. Feldhoff, and R. C. Feldhoff. 2002. Pheromonal activation of vomeronasal neurons in plethodontid salamanders. Brain Res. 952:335-344.
57. Yang, Z. H. 1997. PAML: a program package for phylogenetic analysis by maximum likelihood. Comp. Appl. Biosci. 13:555-556.
58. -. 1998. Likelihood ratio tests for detecting positive selection and application to primate lysozyme evolution. Mol. Biol. Evol. 15:568-573.
59. Yang, Z. H., and J. P. Bielawski. 2000. Statistical methods for detecting molecular adaptation. Trends Ecol. Evol. 15:496-503.
60. Yang, Z. H., and R. Nielsen. 2002. Codon-substitution models for detecting molecular adaptation at individual sites along specific lineages. Mol. Biol. Evol. 19:908-917.
61. Yang, Z. H., R. Nielsen, N. Goldman, and A. M. K. Pedersen. 2000. Codon-substitution models for heterogeneous selection pressure at amino acid sites. Genetics 155:431-449.