1932
0
  1. Home
  2. A-Z Publications
  3. Annual Review of Animal Biosciences
  4. Volume 5, 2017
  5. Article

Annual Review of Animal Biosciences

Volume 5, 2017

Vomeronasal Receptors in Vertebrates and the Evolution of Pheromone Detection

Abstract

Pheromones were identified as chemical signals used for intraspecific communication in insects (e.g., sexual attraction) in the 1950s. However, only almost 40 years later the vomeronasal receptors type-1 (V1R) and type-2 (V2R) were identified, usually associated with the presence of a vomeronasal organ (VNO). VRs are widespread in amphibians, reptiles, and mammals, but birds lost the VNO. Similarly, fishes lack VRs and a VNO but can still detect pheromones, instead using the olfactory receptors related to class A and class C G protein–coupled receptors. Here, we review recent evidence on VR repertoire contraction/expansion in vertebrates. We assess the association between VNO development and VR repertoire size. Phylogenetic relationships and selective pressures illuminate the dynamic evolutionary history of the VRs in vertebrates.

Keyword(s): olfactory receptor related to class C GPCRs, olfactory receptors related to class A GPCRs, OlfC, Ora, transient receptor potential channel 2, TRPC2, VNO, vomeronasal organ, vomeronasal receptor, VR
Loading

Article metrics loading...

/content/journals/10.1146/annurev-animal-022516-022801
2017-02-08
2024-04-28
Loading full text...

Full text loading...

/deliver/fulltext/animal/5/1/annurev-animal-022516-022801.html?itemId=/content/journals/10.1146/annurev-animal-022516-022801&mimeType=html&fmt=ahah

Literature Cited

  1. Karlson P, Luscher M. 1.  1959. Pheromones: a new term for a class of biologically active substances. Nature 183:55–56 [Google Scholar]
  2. Shi P, Zhang J. 2.  2007. Comparative genomic analysis identifies an evolutionary shift of vomeronasal receptor gene repertoires in the vertebrate transition from water to land. Genome Res 17:166–74 [Google Scholar]
  3. Chamero P, Leinders-Zufall T, Zufall F. 3.  2012. From genes to social communication: molecular sensing by the vomeronasal organ. Trends Neurosci 35:597–606 [Google Scholar]
  4. Dong D, Jin K, Wu X, Zhong Y. 4.  2012. CRDB: database of chemosensory receptor gene families in vertebrate. PLOS ONE 7:e31540 [Google Scholar]
  5. Dulac C, Axel R. 5.  1995. A novel family of genes encoding putative pheromone receptors in mammals. Cell 63:195–206 [Google Scholar]
  6. Herrada G, Dulac C. 6.  1997. A novel family of putative pheromone receptors in mammals with a topographically organized and sexually dimorphic distribution. Cell 90:763–73 [Google Scholar]
  7. Matsunami H, Buck LB. 7.  1997. A multigene family encoding a diverse array of putative pheromone receptors in mammals. Cell 90:775–84 [Google Scholar]
  8. Ryba NJP, Tirindelli R. 8.  1997. A new multigene family of putative pheromone receptors. Neuron 19:371–79 [Google Scholar]
  9. Koh T-W, Carlson JR. 16.  2011. Chemoreception: identifying friends and foes. Curr. Biol. 24:R998–99 [Google Scholar]
  10. Papes F, Logan DW, Stowers L. 9.  2010. The vomeronasal organ mediates interspecies defensive behaviors through detection of protein pheromone homologs. Cell 141:692–703 [Google Scholar]
  11. Baxi KN, Dorries KM, Eisthen HL. 10.  2006. Is the vomeronasal system really specialized for detecting pheromones?. Trends Neurosci 29:1–7 [Google Scholar]
  12. Johnstone KA, Lubieniecki KP, Koop BF, Davidson WS. 11.  2012. Identification of olfactory receptor genes in Atlantic salmon Salmo salar. J. Fish Biol. 81:559–75 [Google Scholar]
  13. Hino H, Miles NG, Bandoh H, Ueda H. 12.  2009. Molecular biological research on olfactory chemoreception in fishes. J. Fish Biol. 75:945–59 [Google Scholar]
  14. Gomez-Diaz C, Benton R. 13.  2013. The joy of sex pheromones. EMBO Rep 14:874–83 [Google Scholar]
  15. Benton R. 14.  2008. Chemical sensing in Drosophila. Curr. Opin. Neurobiol. 18:357–63 [Google Scholar]
  16. Mori K. 15.  1997. Pheromones: synthesis and bioactivity. Chem. Commun. 1997:1153–58 [Google Scholar]
  17. Rajchard J. 17.  2013. Kairomones—important substances in interspecific communication in vertebrates: a review. Vet. Med. 58:561–66 [Google Scholar]
  18. Aksoy S, Omolo MO, Hassanali A, Mpiana S, Esterhuizen J. 18.  et al. 2009. Building endogenous capacity for the management of neglected tropical diseases in Africa: the pioneering role of ICIPE. PLOS Negl. Trop. Dis. 3:e435 [Google Scholar]
  19. Yang H, Shi P, Zhang YP, Zhang J. 19.  2005. Composition and evolution of the V2r vomeronasal receptor gene repertoire in mice and rats. Genomics 86:306–15 [Google Scholar]
  20. Keverne EB. 20.  2004. Importance of olfactory and vomeronasal systems for male sexual function. Physiol. Behav. 83:177–87 [Google Scholar]
  21. Grus WE, Zhang J. 21.  2004. Rapid turnover and species-specificity of vomeronasal pheromone receptor genes in mice and rats. Gene 340:303–12 [Google Scholar]
  22. Young JM, Trask BJ. 22.  2005. V2r gene families degenerated in primates, dog and cow, but expanded in opossum. Trends Genet 23:212–15 [Google Scholar]
  23. Syed AS, Sansone A, Nadler W, Manzini I, Korsching SI. 23.  2013. Ancestral amphibian v2rs are expressed in the main olfactory epithelium. PNAS 110:7714–19 [Google Scholar]
  24. Hagino-Yamagishi K, Moriya K, Kubo H, Wakabayashi Y, Isobe N. 24.  et al. 2004. Expression of vomeronasal receptor genes in Xenopus laevis. J. Comp. Neurol. 472:246–56 [Google Scholar]
  25. Young JM, Massa HF, Hsu L, Trask BJ. 25.  2010. Extreme variability among mammalian V1r gene families. Genome Res 20:10–18 [Google Scholar]
  26. Yildirim E, Birnbaumer L. 26.  2007. TRPC2: molecular biology and functional importance. Handb. Exp. Pharmacol. 179:53–75 [Google Scholar]
  27. Halpern M. 27.  2003. Structure and function of the vomeronasal system: an update. Prog. Neurobiol. 70:245–318 [Google Scholar]
  28. Grus WE, Zhang J. 28.  2006. Origin and evolution of the vertebrate vomeronasal system viewed through system-specific genes. Bioessays 28:709–18 [Google Scholar]
  29. Zhang G, Li C, Li Q, Li B, Larkin DM. 29.  et al. 2014. Comparative genomics reveals insights into avian genome evolution and adaptation. Science 346:1311–20 [Google Scholar]
  30. Hashiguchi Y, Nishida M. 30.  2005. Evolution of vomeronasal-type odorant receptor genes in the zebrafish genome. Gene 362:19–28 [Google Scholar]
  31. Hashiguchi Y, Nishida M. 31.  2006. Evolution and origin of vomeronasal-type odorant receptor gene repertoire in fishes. BMC Evol. Biol. 6:76 [Google Scholar]
  32. Saraiva LR, Korsching SI. 32.  2007. A novel olfactory receptor gene family in teleost fish. Genome Res 17:1448–57 [Google Scholar]
  33. Johnstone KA, Lubieniecki KP, Chow W, Phillips RB, Koop BF, Davidson WS. 33.  2008. Genomic organization and characterization of two vomeronasal 1 receptor-like genes (ora1 and ora2) in Atlantic salmon Salmo salar. Mar. Genom. 1:23–31 [Google Scholar]
  34. Johnstone KA, Ciborowski KL, Lubieniecki KP, Chow W, Phillips RB. 34.  et al. 2009. Genomic organization and evolution of the vomeronasal type 2 receptor-like (OlfC) gene clusters in Atlantic salmon, Salmo salar. Mol. Biol. Evol. 26:1117–25 [Google Scholar]
  35. Johnstone KA, Lubieniecki KP, Koop BF, Davidson WS. 35.  2012. Identification of olfactory receptor genes in Atlantic salmon Salmo salar. J. Fish Biol. 81:559–75 [Google Scholar]
  36. Alioto TS, Ngai J. 36.  2006. The repertoire of olfactory C family G protein-coupled receptors in zebrafish: candidate chemosensory receptors for amino acids. BMC Genom. 7:309 [Google Scholar]
  37. Liberles SD. 37.  2014. Mammalian pheromones. Annu. Rev. Physiol. 76:151–75 [Google Scholar]
  38. Boschat C, Pelofi C, Randin O, Roppolo D, Luscher C. 38.  et al. 2002. Pheromone detection mediated by a V1r vomeronasal receptor. Nat. Neurosci. 5:1261–62 [Google Scholar]
  39. Emes RD, Beatson SA, Ponting CP, Goodstadt L. 39.  2004. Evolution and comparative genomics of odorant- and pheromone-associated genes in rodents. Genome Res 14:591–602 [Google Scholar]
  40. Francia S, Silvotti L, Ghirardi F, Catzeflis F, Percudani R, Tirindelli R. 40.  2015. Evolution of spatially coexpressed families of type-2 vomeronasal receptors in rodents. Genome Biol. Evol. 7:272–85 [Google Scholar]
  41. Hohenbrink P, Radespiel U, Mundy NI. 41.  2012. Pervasive and ongoing positive selection in the vomeronasal-1 receptor (V1R) repertoire of mouse lemurs. Mol. Biol. Evol. 29:3807–16 [Google Scholar]
  42. Giorgi D, Rouquier S. 42.  2002. Identification of V1R-like putative pheromone receptor sequences in non-human primates. Characterization of V1R pseudogenes in marmoset, a primate species that possesses an intact vomeronasal organ. Chem. Senses 27:529–37 [Google Scholar]
  43. Ohara H, Nikaido M, Date-Ito A, Mogi K, Okamura H. 43.  et al. 2009. Conserved repertoire of orthologous vomeronasal type 1 receptor genes in ruminant species. BMC Evol. Biol. 9:233 [Google Scholar]
  44. Wakabayashi Y, Mori Y, Ichikawa M, Yazaki K, Hagino-Yamagishi K. 44.  2002. A putative pheromone receptor gene is expressed in two distinct olfactory organs in goats. Chem. Senses 27:207–13 [Google Scholar]
  45. Hohenbrink P, Mundy NI, Zimmermann E, Radespiel U. 45.  2013. First evidence for functional vomeronasal 2 receptor genes in primates. Biol. Lett. 9:1006 [Google Scholar]
  46. Salazar I, Sánchez-Quinteiro P, Alemañ N, Prieto D. 46.  2008. Anatomical, immunohistochemical and physiological characteristics of the vomeronasal vessels in cows and their possible role in vomeronasal reception. J. Anat. 212:686–96 [Google Scholar]
  47. Brykczynska U, Tzika AC, Rodriguez I, Milinkovitch MC. 47.  2013. Contrasted evolution of the vomeronasal receptor repertoires in mammals and squamate reptiles. Genome Biol. Evol. 5:389–401 [Google Scholar]
  48. Schneider NY. 48.  2011. The development of the olfactory organs in newly hatched monotremes and neonate marsupials. J. Anat. 219:229–42 [Google Scholar]
  49. Schneider NY, Fletcher TP, Shaw G, Renfree MB. 49.  2009. The olfactory system of the tammar wallaby is developed at birth and directs the neonate to its mother's pouch odours. Reproduction 138:849–57 [Google Scholar]
  50. Warren WC, Hillier LW, Marshall Graves JA, Birney E, Ponting CP. 50.  et al. 2008. Genome analysis of the platypus reveals unique signatures of evolution. Nature 453:175–83 [Google Scholar]
  51. Grus WE, Shi P, Zhang J. 51.  2007. Largest vertebrate vomeronasal type 1 receptor gene repertoire in the semiaquatic platypus. Mol. Biol. Evol. 24:2153–57 [Google Scholar]
  52. Goodstadt L, Heger A, Webber C, Ponting CP. 52.  2007. An analysis of the gene complement of a marsupial, Monodelphis domestica: evolution of lineage-specific genes and giant chromosomes. Genome Res 17:969–81 [Google Scholar]
  53. Schneider NY, Fletcher TP, Shaw G, Renfree MB. 53.  2008. The vomeronasal organ of the tammar wallaby. J. Anat. 213:93–105 [Google Scholar]
  54. Dawley EM, Fingerlin A, Hwang D, John SS, Stankiewicz CA. 54.  2000. Seasonal cell proliferation in the chemosensory epithelium and brain of red-backed salamanders, Plethodon cinereus. Brain Behav. Evol. 56:1–13 [Google Scholar]
  55. Kiemnec-Tyburczy KM, Woodley SK, Watts RA, Arnold SJ, Houck LD. 55.  2012. Expression of vomeronasal receptors and related signaling molecules in the nasal cavity of a caudate amphibian (Plethodon shermani). Chem. Senses 37:335–46 [Google Scholar]
  56. Park D, McGuire JM, Majchrzak AL, Ziobro JM, Eisthen HL. 56.  2004. Discrimination of conspecific sex and reproductive condition using chemical cues in axolotls (Ambystoma mexicanum). J. Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol. 190:415–27 [Google Scholar]
  57. Janssenswillen S, Willaert B, Treer D, Vandebergh W, Bossuyt F, Van Bocxlaer I. 57.  2015. High pheromone diversity in the male cheek gland of the red-spotted newt Notophthalmus viridescens (Salamandridae). BMC Evol. Biol. 15:54 [Google Scholar]
  58. Woodley SK. 58.  2010. Pheromonal communication in amphibians. J. Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol. 196:713–27 [Google Scholar]
  59. Gliem S, Syed AS, Sansone A, Kludt E, Tantalaki E. 59.  et al. 2013. Bimodal processing of olfactory information in an amphibian nose: odor responses segregate into a medial and a lateral stream. Cell. Mol. Life Sci. 70:1965–84 [Google Scholar]
  60. Date-Ito A, Ohara H, Ichikawa M, Mori Y, Hagino-Yamagishi K. 60.  2008. Xenopus V1R vomeronasal receptor family is expressed in the main olfactory system. Chem. Senses 33:339–46 [Google Scholar]
  61. Ji Y, Zhang Z, Hu Y. 61.  2009. The repertoire of G-protein-coupled receptors in Xenopus tropicalis. BMC Genom. 10:263 [Google Scholar]
  62. Schwenk K. 62.  1995. Of tongues and noses: chemoreception in lizards and snakes. Trends Ecol. Evol. 10:7–12 [Google Scholar]
  63. Filoramo NI, Schwenk K. 63.  2009. The mechanism of chemical delivery to the vomeronasal organs in squamate reptiles: a comparative morphological approach. J. Exp. Zool. A Ecol. Genet. Physiol. 311:20–34 [Google Scholar]
  64. Saito S, Oikawa T, Taniguchi K, Taniguchi K. 64.  2010. Fine structure of the vomeronasal organ in the grass lizard, Takydromus tachydromoides. Tissue Cell 42:322–27 [Google Scholar]
  65. Takami S. 65.  2002. Recent progress in the neurobiology of the vomeronasal organ. Microsc. Res. Tech. 58:228–50 [Google Scholar]
  66. Rehorek SJ, Firth BT, Hutchinson MN. 66.  2009. Assessing the contribution of heterogeneous distributions of oligomers to aggregation mechanisms of polyglutamine peptides. J. Biophys. Chem. 159:14–23 [Google Scholar]
  67. Dennis JC, Allgier JG, Desouza LS, Eward WC, Morrison EE. 67.  2003. Immunohistochemistry of the canine vomeronasal organ. J. Anat. 203:329–38 [Google Scholar]
  68. Grus WE, Shi P, Zhang YP, Zhang J. 68.  2005. Dramatic variation of the vomeronasal pheromone receptor gene repertoire among five orders of placental and marsupial mammals. PNAS 102:5767–72 [Google Scholar]
  69. Barrios AW, Sanchez-Quinteiro P, Salazar I. 69.  2014. Dog and mouse: toward a balanced view of the mammalian olfactory system. Front. Neuroanat. 8:106 [Google Scholar]
  70. Quignon P, Rimbault M, Robin S, Galibert F. 70.  2012. Genetics of canine olfaction and receptor diversity. Mamm. Genome 23:132–43 [Google Scholar]
  71. Arnason U, Gullberg A, Janke A, Kullberg M. 71.  2007. Mitogenomic analyses of caniform relationships. Mol. Phylogenet. Evol. 45:863–74 [Google Scholar]
  72. Nyakatura K, Bininda-Emonds ORP. 72.  2012. The structural and photosynthetic characteristics of the exposed peduncle of wheat (Triticum aestivum L.): an important photosynthate source for grain-filling. BMC Biol 10:141 [Google Scholar]
  73. Skoglund P, Ersmark E, Palkopoulou E, Dalén L. 73.  2015. Ancient wolf genome reveals an early divergence of domestic dog ancestors and admixture into high-latitude breeds. Curr. Biol. 25:1515–19 [Google Scholar]
  74. Salazar I, Sanchez-Quinteiro P. 74.  2011. A detailed morphological study of the vomeronasal organ and the accessory olfactory bulb of cats. Microsc. Res. Tech. 74:1109–20 [Google Scholar]
  75. Bibi F. 75.  2013. A multi-calibrated mitochondrial phylogeny of extant Bovidae (Artiodactyla, Ruminantia) and the importance of the fossil record to systematics. BMC Biol 13:166 [Google Scholar]
  76. Waterston R, Lindblad-Toh K, Birney E, Rogers J, Abril J. 76.  et al. 2002. Initial sequencing and comparative analysis of the mouse genome. Nature 420:520–62 [Google Scholar]
  77. Yoder AD, Larsen PA. 77.  2014. The molecular evolutionary dynamics of the vomeronasal receptor (class 1) genes in primates: a gene family on the verge of a functional breakdown. Front. Neuroanat. 8:153 [Google Scholar]
  78. Zhang X, Rodriguez I, Mombaerts P, Firestein S. 78.  2004. Odorant and vomeronasal receptor genes in two mouse genome assemblies. Genomics 83:802–11 [Google Scholar]
  79. Lane RP, Young J, Newman T, Trask BJ. 79.  2004. Species specificity in rodent pheromone receptor repertoires. Genome Res. 14:603–8 [Google Scholar]
  80. Zhang J, Webb DM. 80.  2003. Evolutionary deterioration of the vomeronasal pheromone transduction pathway in catarrhine primates. PNAS 100:8337–41 [Google Scholar]
  81. Shi P, Bielawski JP, Yang H, Zhang YP. 81.  2005. Adaptive diversification of vomeronasal receptor 1 genes in rodents. J. Mol. Evol. 60:566–76 [Google Scholar]
  82. Park SH, Podlaha O, Grus WE, Zhang J. 82.  2011. The microevolution of V1r vomeronasal receptor genes in mice. Genome Biol. Evol. 3:401–12 [Google Scholar]
  83. Døving KB, Trotier D. 83.  1998. Structure and function of the vomeronasal organ. J. Exp. Biol. 201:2913–25 [Google Scholar]
  84. Khan I, Yang Z, Maldonado E, Li C, Zhan G. 84.  et al. 2015. Olfactory receptor subgenomes linked with broad ecological adaptations in Sauropsida. Mol. Biol. Evol. 32:2832–43 [Google Scholar]
  85. Caro SP, Balthazart J. 85.  2010. Pheromones in birds: Myth or reality?. J. Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol. 196:751–66 [Google Scholar]
  86. Smith TD, Garrett EC, Bhatnagar KP, Bonar CJ, Bruening AE. 86.  et al. 2011. The vomeronasal organ of New World monkeys (Platyrrhini). Anat. Rec. Adv. Integr. Anat. Evol. Biol. 294:2158–78 [Google Scholar]
  87. Kambere MB, Lane RP. 87.  2007. Co-regulation of a large and rapidly evolving repertoire of odorant receptor genes. BMC Neurosci 8:Suppl. 3S2 [Google Scholar]
  88. Bhatnagar KP, Meisami E. 88.  1998. Vomeronasal organ in bats and primates: extremes of structural variability and its phylogenetic implications. Microsc. Res. Tech. 43:465–75 [Google Scholar]
  89. Wible JR, Bhatnagar KP. 89.  1996. Chiropteran vomeronasal complex and the interfamilial relationships of bats. J. Mamm. Evol. 3:285–314 [Google Scholar]
  90. Zhao H, Xu D, Zhang S, Zhang J. 90.  2011. Widespread losses of vomeronasal signal transduction in bats. Mol. Biol. Evol. 28:7–12 [Google Scholar]
  91. Jones G, Teeling EC, Rossiter SJ. 91.  2013. From the ultrasonic to the infrared: molecular evolution and the sensory biology of bats. Front. Physiol. 4:117 [Google Scholar]
  92. Swaney WT, Keverne EB. 92.  2009. The evolution of pheromonal communication. Behav. Brain Res. 200:239–47 [Google Scholar]
  93. Oelschläger HA. 93.  1989. Early development of the olfactory and terminalis systems in baleen whales. Brain Behav. Evol. 34:171–83 [Google Scholar]
  94. Suarez R, Fernández-Aburto P, Manger PR, Mpodozis J. 94.  2011. Deterioration of the Gαo vomeronasal pathway in sexually dimorphic mammals. PLOS ONE 6:e26436 [Google Scholar]
  95. Oelschläger H. 95.  1992. Development of the olfactory and terminalis systems in whales and dolphins. Chemical Signals in Vertebrates 6 R Doty, D Müller-Schwarze 141–47 New York: Springer [Google Scholar]
  96. Meisami E, Bhatnagar AP. 96.  1998. Structure and diversity in mammalian accessory olfactory bulb. Microsc. Res. Tech. 43:476–99 [Google Scholar]
  97. Li W. 97.  2005. Potential multiple functions of a male sea lamprey pheromone. Chem. Senses 30:Suppl. 1i307–8 [Google Scholar]
  98. Fine JM, Sorensen PW. 98.  2008. Isolation and biological activity of the multi-component sea lamprey migratory pheromone. J. Chem. Ecol. 34:1259–67 [Google Scholar]
  99. Cummins SF, Bowie JH. 99.  2012. Pheromones, attractans and other chemical cues of aquatic organisms and amphibians. Nat. Prod. Rep. 29:642–58 [Google Scholar]
  100. Bazáes A, Schmachtenberg O. 100.  2012. Odorant tuning of olfactory crypt cells from juvenile and adult rainbow trout. J. Exp. Biol. 215:1740–48 [Google Scholar]
  101. Pfister P, Rodriguez I. 101.  2005. Olfactory expression of a single and highly variable V1r pheromone receptor-like gene in fish species. PNAS 102:5489–94 [Google Scholar]
  102. Pfister P, Randall J, Montoya-Burgos JI, Rodriguez I. 102.  2007. Divergent evolution among teleost V1r receptor genes. PLOS ONE 2:e379 [Google Scholar]
  103. Ota T, Nikaido M, Suzuki H, Hagino-Yamagishi K, Okada N. 103.  2012. Characterization of V1R receptor (ora) genes in Lake Victoria cichlids. Gene 499:273–79 [Google Scholar]
  104. Johnson MA, Banks MA. 104.  2011. Sequence conservation among orthologous vomeronasal type 1 receptor-like (ora) genes does not support the differential tuning hypothesis in Salmonidae. Gene 485:16–21 [Google Scholar]
  105. Johansson ML, Banks MA. 105.  2011. Olfactory receptor related to class A, type 2 (V1r-like Ora2) genes are conserved between distantly related rockfishes (genus Sebastes). J. Hered. 102:113–17 [Google Scholar]
  106. Nikaido M, Suzuki H, Toyoda A, Fujiyama A, Hagino-Yamagishi K. 106.  et al. 2013. Lineage-specific expansion of vomeronasal type 2 receptor-like (OlfC) genes in cichlids may contribute to diversification of amino acid detection systems. Genome Biol. Evol. 5:711–22 [Google Scholar]
  107. Speca DJ, Lin DM, Sorensen PW, Isacoff EY, Ngai J, Dittman AH. 107.  1999. Functional identification of a goldfish odorant receptor. Neuron 23:487–98 [Google Scholar]
  108. Luu P, Acher F, Bertrand HO, Fan J, Ngai J. 108.  2004. Molecular determinants of ligand selectivity in a vertebrate odorant receptor. J. Neurosci. 24:10128–37 [Google Scholar]
  109. Acher FC, Bertrand HO. 109.  2005. Amino acid recognition by Venus flytrap domains is encoded in an 8-residue motif. Biopolymers 80:357–66 [Google Scholar]
  110. Chang S, Chung-Davidson YW, Libants S, Nanlohy KG, Kiupel M. 110.  et al. 2013. The sea lamprey has a primordial accessory olfactory system BMC Evol. Biol. 13:172 [Google Scholar]
  111. Laframboise AJ, Ren X, Chang S, Dubuc R, Zielinski BS. 111.  2007. Olfactory sensory neurons in the sea lamprey display polymorphisms. Neurosci. Lett. 414:277–81 [Google Scholar]
  112. Kamesh N, Aradhyam GK, Manoj N. 112.  2008. The repertoire of G protein-coupled receptors in the sea squirt Ciona intestinalis. BMC Evol. Biol. 8:129 [Google Scholar]
  113. Nordstrom KJ, Fredriksson R, Schioth HB. 113.  2008. The amphioxus (Branchiostoma floridae) genome contains a highly diversified set of G protein-coupled receptors. BMC Evol. Biol. 8:9 [Google Scholar]
  114. Saviola AJ, Chiszar D, Busch C, Mackessy SP. 114.  2013. Molecular basis for prey relocation in viperid snakes. BMC Biol 11:20 [Google Scholar]
  115. Cooper WE. 115.  1994. Chemical discrimination by tongue-flicking in lizards: a review with hypotheses on its origin and its ecological and phylogenetic relationships. J. Chem. Ecol. 20:439–87 [Google Scholar]
  116. Shine R, Mason RT. 116.  2012. An airborne sex pheromone in snakes. Biol. Lett. 8:183–85 [Google Scholar]
  117. Murphy FA, Tucker K, Fadool DA. 117.  2001. Sexual dimorphism and developmental expression of signal-transduction machinery in the vomeronasal organ. J. Comp. Neurol. 432:61–64 [Google Scholar]
  118. Graziadei PPC, Tucker D. 118.  1970. Vomeronasal receptors in turtles. Z. Zellforsch. 105:498–514 [Google Scholar]
  119. Saito K, Shoji T, Uchida I, Ueda H. 119.  2000. Structure of the olfactory and vomeronasal epithelia in the loggerhead turtle Caretta caretta. Fish. Sci. 66:409–11 [Google Scholar]
  120. Bertmar G. 120.  1981. Evolution of vomeronasal organs in vertebrates. Evolution 35:359–66 [Google Scholar]
  121. Wang Z, Pascual-Anaya J, Zadissa A, Li W, Niimura Y. 121.  et al. 2013. The draft genomes of soft-shell turtle and green sea turtle yield insights into the development and evolution of the turtle-specific body plan. Nat. Genet. 45:701–6 [Google Scholar]
  122. Shaffer HB, Minx P, Warren DE, Shedlock AM, Thomson RC. 122.  et al. 2013. The western painted turtle genome, a model for the evolution of extreme physiological adaptations in a slowly evolving lineage. Genome Biol 14:R28 [Google Scholar]
  123. Green RE, Braun EL, Armstrong J, Earl D, Nguyen N. 123.  et al. 2014. Three crocodilian genomes reveal ancestral patterns of evolution among archosaurs. Science 346:1254449 [Google Scholar]
  124. Picone B, Hesse U, Panji S, Van Heusden P, Jonas M, Christoffels A. 124.  2014. Taste and odorant receptors of the coelacanth—a gene repertoire in transition. J. Exp. Zool. B Mol. Dev. Evol. 322:403–14 [Google Scholar]
  125. Amemiya CT, Alfoldi J, Lee AP, Fan S, Philippe H. 125.  et al. 2013. The African coelacanth genome provides insights into tetrapod evolution. Nature 496:311–16 [Google Scholar]
  126. Koepfli K, Paten B. 126.  Genome 10K Commun. Sci., O'Brien SJ 2015. The Genome 10K Project: a way forward. Annu. Rev. Anim. Biosci. 3:57–111 [Google Scholar]
/content/journals/10.1146/annurev-animal-022516-022801
Loading
Vomeronasal Receptors in Vertebrates and the Evolution of Pheromone Detection
Annual Review of Animal Biosciences 5, 353 (2017); https://doi.org/10.1146/annurev-animal-022516-022801
/content/journals/10.1146/annurev-animal-022516-022801
/content/journals/10.1146/annurev-animal-022516-022801
Loading

Data & Media loading...

  • Article Type: Review Article

Most Cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error