Skip to main content
SpringerLink
Log in

Use it or lose it: molecular evolution of sensory signaling in primates

  • Invited Review
  • Published:
Pflügers Archiv Aims and scope Submit manuscript

Abstract

Sensory organs provide key and, in many cases, species-specific information that allows animals to effectively forage, find mates, and avoid hazards. The primary sensors for the vertebrate senses of vision, taste, and smell are G-protein-coupled receptors (GPCRs) expressed by sensory receptor cells that initiate intracellular signal transduction cascades in response to activation by appropriate stimuli. The identification of sensory GPCRs and their related downstream transduction components from a variety of species has provided an essential tool for understanding the molecular evolution of sensory systems. Expansion of the number of genes encoding sensory GPCRs has, in some cases, expanded the repertoire of signals that animals detect, allowing them to occupy new niches, while, in other cases, evolution has favored a reduction in the repertoire of receptors and their cognate signal transduction components when these signals no longer provide a selective advantage. This review will focus on recent studies that have identified molecular changes in vision, smell, taste, and pheromone detection during primate evolution.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  1. Blakeslee AF (1932) Genetics of sensory thresholds: taste for phenyl thio carbamide. Proc Natl Acad Sci USA, 18:120–130

    Article  PubMed  CAS  Google Scholar 

  2. Buck L, Axel R (1991) A novel multigene family may encode odorant receptors: a molecular basis for odor recognition. Cell 65:175–187

    Article  PubMed  CAS  Google Scholar 

  3. Buck LB (2000) The molecular architecture of odor and pheromone sensing in mammals. Cell 100:611–618

    Article  PubMed  CAS  Google Scholar 

  4. Bufe B, Breslin PA, Kuhn C, Reed DR, Tharp CD, Slack JP, Kim UK, Drayna D, Meyerhof W (2005) The molecular basis of individual differences in phenylthiocarbamide and propylthiouracil bitterness perception. Curr Biol 15:322–327

    Article  PubMed  CAS  Google Scholar 

  5. Caterina MJ, Schumacher MA, Tominaga M, Rosen TA, Levine JD, Julius D (1997) The capsaicin receptor: a heat-activated ion channel in the pain pathway. Nature 389:816–824

    Article  PubMed  CAS  Google Scholar 

  6. Chandrashekar J, Mueller KL, Hoon MA, Adler E, Feng L, Guo W, Zuker CS, Ryba NJ (2000) T2rs function as bitter taste receptors. Cell 100:703–711

    Article  PubMed  CAS  Google Scholar 

  7. Chess A, Simon I, Cedar H, Axel R (1994) Allelic inactivation regulates olfactory receptor gene expression. Cell 78:823–834

    Article  PubMed  CAS  Google Scholar 

  8. Del Punta K, Leinders-Zufall T, Rodriguez I, Jukam D, Wysocki CJ, Ogawa S, Zufall F, Mombaerts P (2002) Deficient pheromone responses in mice lacking a cluster of vomeronasal receptor genes. Nature 419:70–74

    Article  PubMed  CAS  Google Scholar 

  9. Drayna D (2005) Human taste genetics. Annu Rev Genomics Hum Genet 6:217–235

    Article  PubMed  CAS  Google Scholar 

  10. Dulac C, Axel R (1995) A novel family of genes encoding putative pheromone receptors in mammals. Cell 83:195–206

    Article  PubMed  CAS  Google Scholar 

  11. Fischer A, Gilad Y, Man O, Paabo S (2005) Evolution of bitter taste receptors in humans and apes. Mol Biol Evol 22:432–436

    Article  PubMed  CAS  Google Scholar 

  12. Fisher RA, Ford EB, Huxley J (1939) Taste-testing the anthropoid apes. Nature 144:750

    Google Scholar 

  13. Fox AL (1932) The relationship between chemical constitution and taste. Proc Natl Acad Sci USA 18:115–120

    Article  PubMed  CAS  Google Scholar 

  14. Gilad Y, Lancet D (2003) Population differences in the human functional olfactory repertoire. Mol Biol Evol 20:307–314

    Article  PubMed  CAS  Google Scholar 

  15. Gilad Y, Man O, Paabo S, Lancet D (2003) Human specific loss of olfactory receptor genes. Proc Natl Acad Sci USA 100:3324–3327

    Article  PubMed  CAS  Google Scholar 

  16. Gilad Y, Wiebe V, Przeworski M, Lancet D, Paabo S (2004) Loss of olfactory receptor genes coincides with the acquisition of full trichromatic vision in primates. PLoS Biol 2:E5

    Article  PubMed  Google Scholar 

  17. Go Y, Satta Y, Takenaka O, Takahata N (2005) Lineage-specific loss of function of bitter taste receptor genes in humans and nonhuman primates. Genetics 170:313–326

    Article  PubMed  CAS  Google Scholar 

  18. Godfrey PA, Malnic B, Buck LB (2004) The mouse olfactory receptor gene family. Proc Natl Acad Sci USA 101:2156–2161

    Article  PubMed  CAS  Google Scholar 

  19. Grus WE, Shi P, Zhang YP, Zhang J (2005) Dramatic variation of the vomeronasal pheromone receptor gene repertoire among five orders of placental and marsupial mammals. Proc Natl Acad Sci USA 102:5767–5772

    Article  PubMed  CAS  Google Scholar 

  20. Herrada G, Dulac C (1997) A novel family of putative pheromone receptors in mammals with a topographically organized and sexually dimorphic distribution. Cell 90:763–773

    Article  PubMed  CAS  Google Scholar 

  21. Hunt DM, Dulai KS, Cowing JA, Julliot C, Mollon JD, Bowmaker JK, Li WH, Hewett-Emmett D (1998) Molecular evolution of trichromacy in primates. Vision Res 38:3299–3306

    Article  PubMed  CAS  Google Scholar 

  22. Hurst LD (2002) The ka/ks ratio: diagnosing the form of sequence evolution. Trends Genet 18:486–487

    Article  PubMed  Google Scholar 

  23. Jacobs GH, Neitz M, Deegan JF, Neitz J (1996) Trichromatic colour vision in new world monkeys. Nature 382:156–158

    Article  PubMed  CAS  Google Scholar 

  24. Jiang P, Ji Q, Liu Z, Snyder LA, Benard LM, Margolskee RF, Max M (2004) The cysteine-rich region of t1r3 determines responses to intensely sweet proteins. J Biol Chem 279:45068–45075

    Article  PubMed  CAS  Google Scholar 

  25. Jordt SE, Julius D (2002) Molecular basis for species-specific sensitivity to “hot” chili peppers. Cell 108:421–430

    Article  PubMed  CAS  Google Scholar 

  26. Kainz PM, Neitz J, Neitz M (1998) Recent evolution of uniform trichromacy in a new world monkey. Vision Res 38:3315–3320

    Article  PubMed  CAS  Google Scholar 

  27. Kim UK, Jorgenson E, Coon H, Leppert M, Risch N, Drayna D (2003) Positional cloning of the human quantitative trait locus underlying taste sensitivity to phenylthiocarbamide. Science 299:1221–1225

    Article  PubMed  CAS  Google Scholar 

  28. Leinders-Zufall T, Brennan P, Widmayer P, S PC, Maul-Pavicic A, Jager M, Li XH, Breer H, Zufall F, Boehm T (2004) Mhc class i peptides as chemosensory signals in the vomeronasal organ. Science 306:1033–1037

    Article  PubMed  CAS  Google Scholar 

  29. Leinders-Zufall T, Lane AP, Puche AC, Ma W, Novotny MV, Shipley MT, Zufall F (2000) Ultrasensitive pheromone detection by mammalian vomeronasal neurons. Nature 405:792–796

    Article  PubMed  CAS  Google Scholar 

  30. Leypold BG, Yu CR, Leinders-Zufall T, Kim MM, Zufall F, Axel R (2002) Altered sexual and social behaviors in trp2 mutant mice. Proc Natl Acad Sci USA, 99:6376–6381

    Article  PubMed  CAS  Google Scholar 

  31. Li W-H (1997) Molecular evolution. Sinauer Associates, Sunderland, Massachusetts

    Google Scholar 

  32. Li X, Li W, Wang H, Cao J, Maehashi K, Huang L, Bachmanov AA, Reed DR, Legrand-Defretin V, Beauchamp GK, Brand JG (2005) Pseudogenization of a sweet-receptor gene accounts for cats’ indifference toward sugar. PLoS Genet 1:27–35

    Article  PubMed  CAS  Google Scholar 

  33. Li X, Staszewski L, Xu H, Durick K, Zoller M, Adler E (2002) Human receptors for sweet and umami taste. Proc Natl Acad Sci USA 99:4692–4696

    Article  PubMed  CAS  Google Scholar 

  34. Liman ER, Corey DP, Dulac C (1999) Trp2: a candidate transduction channel for mammalian pheromone sensory signaling. Proc Natl Acad Sci USA 96:5791–5796

    Article  PubMed  CAS  Google Scholar 

  35. Liman ER, Innan H (2003) Relaxed selective pressure on an essential component of pheromone transduction in primate evolution. Proc Natl Acad Sci USA 100:3328–3332

    Article  PubMed  CAS  Google Scholar 

  36. Liman ER, Zufall F (2004) Transduction channels in the vomeronasal organ. In: Frings S, Bradley J (eds) Transduction channels in sensory cells. Wiley-VCH Verlag GmbH, Weinhem, pp 135–152

    Chapter  Google Scholar 

  37. Lindemann B (2001) Receptors and transduction in taste. Nature 413:219–225

    Article  PubMed  CAS  Google Scholar 

  38. Margolskee RF (2002) Molecular mechanisms of bitter and sweet taste transduction. J Biol Chem 277:1–4

    Article  PubMed  CAS  Google Scholar 

  39. Matsunami H, Buck LB (1997) A multigene family encoding a diverse array of putative pheromone receptors in mammals. Cell 90:775–784

    Article  PubMed  CAS  Google Scholar 

  40. Meredith M (2001) Human vomeronasal organ function: a critical review of best and worst cases. Chem Senses 26:433–445

    Article  PubMed  CAS  Google Scholar 

  41. Messier W, Stewart CB (1997) Episodic adaptive evolution of primate lysozymes. Nature 385:151–154

    Article  PubMed  CAS  Google Scholar 

  42. Miyata T, Yasunaga T (1980) Molecular evolution of mrna: a method for estimating evolutionary rates of synonymous and amino acid substitutions from homologous nucleotide sequences and its application. J Mol Evol 16:23–36

    Article  PubMed  CAS  Google Scholar 

  43. Mombaerts P (1999) Seven-transmembrane proteins as odorant and chemosensory receptors. Science 286:707–711

    Article  PubMed  CAS  Google Scholar 

  44. Montmayeur JP, Matsunami H (2002) Receptors for bitter and sweet taste. Curr Opin Neurobiol 12:366–371

    Article  PubMed  CAS  Google Scholar 

  45. Mueller KL, Hoon MA, Erlenbach I, Chandrashekar J, Zuker CS, Ryba NJ (2005) The receptors and coding logic for bitter taste. Nature 434:225–229

    Article  PubMed  CAS  Google Scholar 

  46. Nathans J (1999) The evolution and physiology of human color vision: insights from molecular genetic studies of visual pigments. Neuron 24:299–312

    Article  PubMed  CAS  Google Scholar 

  47. Nei M, Kimur S (2000) Molecular evolution and phylogenetics. Oxford University Press

  48. Nelson G, Chandrashekar J, Hoon MA, Feng L, Zhao G, Ryba NJ, Zuker CS (2002) An amino-acid taste receptor. Nature 416:199–202

    Article  PubMed  CAS  Google Scholar 

  49. Nelson G, Hoon MA, Chandrashekar J, Zhang Y, Ryba NJ, Zuker CS (2001) Mammalian sweet taste receptors. Cell 106:381–390

    Article  PubMed  CAS  Google Scholar 

  50. Niimura Y, Nei M (2003) Evolution of olfactory receptor genes in the human genome, Proc Natl Acad Sci USA 100:12235–12240

    Article  PubMed  CAS  Google Scholar 

  51. Niimura Y, Nei M (2005) Evolutionary changes of the number of olfactory receptor genes in the human and mouse lineages. Gene 346:23–28

    Article  PubMed  CAS  Google Scholar 

  52. Niimura Y, Nei M (2005) Evolutionary dynamics of olfactory receptor genes in fishes and tetrapods. Proc Natl Acad Sci USA 102:6039–6044

    Article  PubMed  CAS  Google Scholar 

  53. Niimura Y, Nei M (2006) Evolutionary dynamics of olfactory and other chemosensory receptor genes in vertebrates. J Hum Genet

  54. Rodriguez I, Greer CA, Mok MY, Mombaerts P (2000) A putative pheromone receptor gene expressed in human olfactory mucosa. Nat Genet 26:18–19

    Article  PubMed  CAS  Google Scholar 

  55. Rodriguez I, Mombaerts P (2002) Novel human vomeronasal receptor-like genes reveal species-specific families. Curr Biol 12:R409–R411

    Article  PubMed  CAS  Google Scholar 

  56. Ryba NJ, Tirindelli R (1997) A new multigene family of putative pheromone receptors. Neuron 19:371–379

    Article  PubMed  CAS  Google Scholar 

  57. Shi P, Zhang J (2006) Contrasting modes of evolution between vertebrate sweet/umami receptor genes and bitter receptor genes. Mol Biol Evol 23:292–300

    Article  PubMed  CAS  Google Scholar 

  58. Stowers L, Holy TE, Meister M, Dulac C, Koentges G (2002) Loss of sex discrimination and male–male aggression in mice deficient for trp2. Science 295:1493–1500

    Article  PubMed  CAS  Google Scholar 

  59. Surridge AK, Osorio D, Mundy NI (2003) Evolution and selection of trichromatic vision in primate. Trends Ecol Evol 18:198–205

    Article  Google Scholar 

  60. Tewksbury JJ, Nabhan GP (2001) Seed dispersal. Directed deterrence by capsaicin in chilies. Nature 412:403–404

    Article  PubMed  CAS  Google Scholar 

  61. Wes PD, Chevesich J, Jeromin A, Rosenberg C, Stetten G, Montell C (1995) Trpc1, a human homolog of a drosophila store-operated channel. Proc Natl Acad Sci USA 92:9652–9656

    Article  PubMed  CAS  Google Scholar 

  62. Wooding S, Bufe B, Grassi C, Howard MT, Stone AC, Vazquez M, Dunn DM, Meyerhof W, Weiss RB, Bamshad MJ (2006) Independent evolution of bitter-taste sensitivity in humans and chimpanzees. Nature 440:930–934

    Article  PubMed  CAS  Google Scholar 

  63. Wooding S, Kim UK, Bamshad MJ, Larsen J, Jorde LB, Drayna D (2004) Natural selection and molecular evolution in ptc, a bitter-taste receptor gene. Am J Hum Genet 74:637–646

    Article  PubMed  CAS  Google Scholar 

  64. Wysocki CJ, Preti G (2004) Facts, fallacies, fears, and frustrations with human pheromones. Anat Rec 281A:1201–1211

    Article  CAS  Google Scholar 

  65. Yang H, Shi P, Zhang YP, Zhang J (2005) Composition and evolution of the v2r vomeronasal receptor gene repertoire in mice and rats. Genomics 86:306–315

    Article  PubMed  CAS  Google Scholar 

  66. Yang Z, Bielawski JP (2000) Statistical methods for detecting molecular adaptation. Trends Ecol Evol 15:496–503

    Article  PubMed  Google Scholar 

  67. Young JM, Kambere M, Trask BJ, Lane RP (2005) Divergent v1r repertoires in five species: amplification in rodents, decimation in primates, and a surprisingly small repertoire in dogs. Genome Res 15:231–240

    Article  PubMed  CAS  Google Scholar 

  68. Zhang J, Webb DM (2003) Evolutionary deterioration of the vomeronasal pheromone transduction pathway in catarrhine primates. Proc Natl Acad Sci USA 100:8337–8341

    Article  PubMed  CAS  Google Scholar 

  69. Zhang X, Firestein S (2002) The olfactory receptor gene superfamily of the mouse. Nat Neurosci 5:124–133

    PubMed  CAS  Google Scholar 

  70. Zhang Y, Hoon MA, Chandrashekar J, Mueller KL, Cook B, Wu D, Zuker CS, Ryba NJ (2003) Coding of sweet, bitter, and umami tastes: different receptor cells sharing similar signaling pathways. Cell 112:293–301

    Article  PubMed  CAS  Google Scholar 

  71. Zhang Z, Gerstein M (2004) Large-scale analysis of pseudogenes in the human genome. Curr Opin Genet Dev 14:328–335

    Article  PubMed  CAS  Google Scholar 

  72. Zhao GQ, Zhang Y, Hoon MA, Chandrashekar J, Erlenbach I, Ryba NJ, Zuker CS (2003) The receptors for mammalian sweet and umami taste. Cell 115:255–266

    Article  PubMed  CAS  Google Scholar 

  73. Zufall F, Ukhanov K, Lucas P, Liman ER, Leinders-Zufall T (2005) Neurobiology of trpc2: from gene to behavior. Pflugers Arch 451:61–71

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgment

I thank D. McKemy for helpful comments on the manuscript. Supported by grants from the National Institute of Health (USA) DC004564 and DC05000.

Author information

Authors and Affiliations

  1. Neuroscience Program, Molecular and Computational Biology Program, Department of Biological Sciences, University of Southern California, 3641 Watt Way, Los Angeles, CA, 90089, USA

    Emily R. Liman

Authors
  1. Emily R. Liman
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Emily R. Liman.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Liman, E.R. Use it or lose it: molecular evolution of sensory signaling in primates. Pflugers Arch - Eur J Physiol 453, 125–131 (2006). https://doi.org/10.1007/s00424-006-0120-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00424-006-0120-3

Keywords

Search

Navigation