Rapid evolution of chemosensory receptor genes in a pair of sibling species of orchid bees (Apidae: Euglossini)

BMC Evolutionary Biology

Volumn 15, Issue 1, 2015, Pages

  Brand, Philipp ^a,b   Ramírez, Santiago R ^b   Leese, Florian ^a,d   Quezada Euan, J Javier G ^c   Tollrian, Ralph ^a   Eltz, Thomas ^a  

^a RUHR UNIVERSITY BOCHUM   (Germany)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSIDAD AUTÓNOMA DE YUCATÁN   (Mexico)

^d UNIVERSITY OF DUISBURG ESSEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BEE; CHEMORECEPTION; CONSPECIFIC; COURTSHIP; DIVERGENCE; GENE EXPRESSION; GENETIC VARIATION; ODOR; OLFACTION; PARALLEL EVOLUTION; PHEROMONE; RELATEDNESS; SIBLING; SPECIALIZATION;

APIDAE; APOIDEA; EUGLOSSA; EUGLOSSINI; HEXAPODA;

INSECT PROTEIN; OLFACTORY RECEPTOR; PHEROMONE;

ANIMAL; BEE; CLASSIFICATION; FEMALE; GENETICS; MALE; METABOLISM; MOLECULAR EVOLUTION; ODOR; OLFACTORY RECEPTOR; PHYLOGENY; PHYSIOLOGY;

ANIMALS; BEES; EVOLUTION, MOLECULAR; FEMALE; INSECT PROTEINS; MALE; PHEROMONES; PHYLOGENY; RECEPTORS, ODORANT; SMELL;

EID: 84940469432     PISSN: None     EISSN: 14712148     Source Type: Journal    
DOI: 10.1186/s12862-015-0451-9     Document Type: Article

References (114)

1. Hansson BS. Insect Olfaction. Heidelberg: Springer Verlag; 1999.
2. Mombaerts P. Genes and ligands for odorant, vomeronasal and taste receptors. Nat Rev Neurosci. 2004;5:263-78.
3. Birch MC, Haynes KF. Insect Pheromones. London: Hodder Arnold; 1982.
4. Wyatt TD. Fifty years of pheromones. Nature. 2009;457:262-3.
5. Dobritsa AA, van der Goes van Naters W, Warr CG, Steinbrecht RA, Carlson JR. Integrating the molecular and cellular basis of odor coding in the drosophila antenna. Neuron. 2003;37:827-41.
6. Leal WS. Odorant reception in insects: roles of receptors, binding proteins, and degrading enzymes. Annu Rev Entomol. 2013;58:373-91.
7. Smadja C, Butlin RK. On the scent of speciation: the chemosensory system and its role in premating isolation. Heredity. 2009;102:77-97.
8. Hansson BS, Stensmyr MC. Evolution of insect olfaction. Neuron. 2011;72:698-711.
9. Lassance J-M, Bogdanowicz SM, Wanner KW, Löfstedt C, Harrison RG. Gene genealogies reveal differentiation at sex pheromone olfactory receptor loci in pheromone strains of the European corn borer, Ostrinia nubilalis. Evolution. 2011;65:1583-93.
10. Vásquez GM, Syed Z, Estes PA, Leal WS, Gould F. Specificity of the receptor for the major sex pheromone component in Heliothis virescens. J Insect Sci. 2013;13:160-12.
11. Jiang X-J, Guo H, Di C, Yu S, Zhu L, Huang L-Q, et al. Sequence similarity and functional comparisons of pheromone receptor orthologs in two closely related Helicoverpa species. Insect Biochem Mol Biol. 2014;48:63-74.
12. Leary GP, Allen JE, Bunger PL, Luginbill JB, Linn CE, Macallister IE, et al. Single mutation to a sex pheromone receptor provides adaptive specificity between closely related moth species. Proc Natl Acad Sci U S A. 2012;109:14081-6.
13. Kopp A, Barmina O, Hamilton AM, Higgins L, McIntyre LM, Jones CD. Evolution of gene expression in the Drosophila olfactory system. Mol Biol Evol. 2008;25:1081-92.
14. Vásquez GM, Fischer P, Grozinger CM, Gould F. Differential expression of odorant receptor genes involved in the sexual isolation of two Heliothis moths. Insect Mol Biol. 2011;20:115-24.
15. Wang G, Vásquez GM, Schal C, Zwiebel LJ, Gould F. Functional characterization of pheromone receptors in the tobacco budworm Heliothis virescens. Insect Mol. Biol. 2011;20:125-33.
16. McBride CS. Rapid evolution of smell and taste receptor genes during host specialization in Drosophila sechellia. Proc Natl Acad Sci U S A. 2007;104:4996-5001.
17. Goldman-Huertas B, Mitchell RF, Lapoint RT, Faucher CP, Hildebrand JG, Whiteman NK. Evolution of herbivory in Drosophilidae linked to loss of behaviors, antennal responses, odorant receptors, and ancestral diet. Proc. Natl. Acad. Sci. U.S.A. 2015;112:3026-31 (2015).
18. Boake CRB. Coevolution of senders and receivers of sexual signals: genetic coupling and genetic correlations. Trends Ecol Evol. 1991;6:225-7.
19. Tillman JA, Seybold SJ, Jurenka RA, Blomquist GJ. Insect pheromones - an overview of biosynthesis and endocrine regulation. Insect Biochem Mol Biol. 1999;29:481-514.
20. Niehuis O, Buellesbach J, Gibson JD, Pothmann D, Hanner C, Mutti NS, et al. Behavioural and genetic analyses of Nasonia shed light on the evolution of sex pheromones. Nature. 2013;494:345-8.
21. Ramírez S, Dressler RL, Ospina M. Abejas euglosinas (Hymenoptera: Apidae) de la región Neotropical: listado de especies con notas sobre su biología. Biota Colombiana. 2002;3:7-118.
22. Kimsey LS. The behaviour of male orchid bees (Apidae, Hymenoptera, Insecta) and the question of leks. Anim Behav. 1980;28:996-1004.
23. Williams NH. The biology of orchids and euglossine bees in J. Arditti (ed.). OrchidBiology: Reviews and Perspectives, II. Cornell University Press, Ithaca, NY.1982;119-71.
24. Cameron SA. Phylogeny and biology of neotropical orchid bees (Euglossini). Annu Rev Entomol. 2004;49:377-404.
25. Eltz T, Ayasse M, Lunau K. Species-specific antennal responses to tibial fragrances by male orchid bees. J Chem Ecol. 2006;32:71-9.
26. Zimmermann Y, Roubik DW, Eltz T. Species-specific attraction to pheromonal analogues in orchid bees. Behav Ecol Sociobiol. 2006;60:833-43.
27. Eltz T, Zimmermann Y, Pfeiffer C, Pech JR, Twele R, Francke W, et al. An olfactory shift is associated with male perfume differentiation and species divergence in orchid bees. Curr Biol. 2008;18:1844-8.
28. Ackerman JD. Specificity and mutual dependency of the orchid-euglossine bee interaction. Biol J Linn Soc.1983;20:301-14.
29. Whitten WM, Young AM, Stern DL. Nonfloral sources of chemicals that attract male euglossine bees (Apidae: Euglossini). J Chem Ecol. 1993;19:3017-27.
30. Eltz T, Whitten WM, Roubik DW, Linsenmair KE. Fragrance collection, storage, and accumulation by individual male orchid bees. J Chem Ecol. 1999;25:157-76.
31. Pemberton RW, Wheeler GS. Orchid bees don't need orchids: evidence from the naturalization of an orchid bee in Florida. Ecology. 2006;87:1995-2001.
32. Zimmermann Y, Ramírez SR, Eltz T. Chemical niche differentiation among sympatric species of orchid bees. Ecology. 2009;90:2994-3008.
33. Kimsey LS. The behavioural and structural aspects of grooming and related activities in euglossine bees (Hymenoptera: Apidae). J Zool. 1984;204:541-50.
34. Bembé B. Functional morphology in male euglossine bees and their ability to spray fragrances (Hymenoptera, Apidae, Euglossini). Apidologie. 2004:283-291.
35. Eltz T, Sager A, Lunau K. Juggling with volatiles: exposure of perfumes by displaying male orchid bees. J Comp Physiol A. 2005;191:575-81.
36. Schorkopf DLP, Mitko L, Eltz T. Enantioselective preference and high antennal sensitivity for (-)-Ipsdienol in scent-collecting male orchid bees, Euglossa cyanura. J Chem Ecol. 2011;37:953-60.
37. Sakurai T, Nakagawa T, Mitsuno H, Mori H, Endo Y, Tanoue S, et al. Identification and functional characterization of a sex pheromone receptor in the silkmoth Bombyx mori. Proc Natl Acad Sci U S A. 2004;101:16653-8.
38. Wanner KW, Nichols AS, Walden KKO, Brockmann A, Luetje CW, Robertson HM. A honey bee odorant receptor for the queen substance 9-oxo-2-decenoic acid. Proc Natl Acad Sci U S A. 2007;104:14383-8.
39. Miura N, Nakagawa T, Touhara K, Ishikawa Y. Broadly and narrowly tuned odorant receptors are involved in female sex pheromone reception in Ostrinia moths. Insect Biochem Mol Biol. 2010;40:64-73.
40. Wanner KW, Nichols AS, Allen JE, Bunger PL, Garczynski SF, Linn CE, et al. Sex pheromone receptor specificity in the European corn borer moth, Ostrinia nubilalis. PLoS One. 2010;5:e8685.
41. Jones WD, Cayirlioglu P, Kadow IG, Vosshall LB. Two chemosensory receptors together mediate carbon dioxide detection in Drosophila. Nature. 2007;445:86-90.
42. Benton R, Vannice KS, Gomez-Diaz C, Vosshall LB. Variant ionotropic glutamate receptors as chemosensory receptors in Drosophila. Cell. 2009;136:149-62.
43. Silbering AF, Rytz R, Grosjean Y, Abuin L, Ramdya P, Jefferis GSXE, et al. Complementary function and integrated wiring of the evolutionarily distinct Drosophila olfactory subsystems. J Neurosci. 2011;31:13357-75.
44. Pelosi P, Calvello M, Ban L. Diversity of odorant-binding proteins and chemosensory proteins in insects. Chem Senses. 2005;30 Suppl 1:i291-2.
45. Ozaki M, Wada-Katsumata A, Fujikawa K, Iwasaki M, Yokohari F, Satoji Y, et al. Ant nestmate and non-nestmate discrimination by a chemosensory sensillum. Science. 2005;309:311-4.
46. Grosse-Wilde E, Svatoš A, Krieger J. A pheromone-binding protein mediates the bombykol-induced activation of a pheromone receptor in vitro. Chem Senses. 2006;31:547-55.
47. Grosse-Wilde E, Gohl T, Bouché E, Breer H, Krieger J. Candidate pheromone receptors provide the basis for the response of distinct antennal neurons to pheromonal compounds. Eur J Neurosci. 2007;25:2364-73.
48. Laughlin JD, Ha TS, Jones DNM, Smith DP. Activation of pheromone-sensitive neurons is mediated by conformational activation of pheromone-binding protein. Cell. 2008;133:1255-65.
49. Eltz T, Fritzsch F, Pech JR, Zimmermann Y, Ramírez S, Quezada-Euan JJG, et al. Characterization of the orchid bee Euglossa viridissima (Apidae: Euglossini) and a novel cryptic sibling species, by morphological, chemical, and genetic characters. Zool J Linn Soc. 2011;163:1064-76.
50. Villanueva-Gutierrez R, Quezada-Euan J, Eltz T. Pollen diets of two sibling orchid bee species, Euglossa, in Yucatán, southern Mexico. Apidologie. 2013;44:440-6.
51. Vosshall LB, Amrein H, Morozov PS, Rzhetsky A, Axel R. A spatial map of olfactory receptor expression in the Drosophila antenna. Cell. 1999;96:725-36.
52. Vosshall LB, Wong AM, Axel R. An olfactory sensory map in the fly brain. Cell. 2000;102:147-59.
53. Mitchell RF, Hughes DT, Luetje CW, Millar JG, Soriano-Agatón F, Hanks LM, et al. Sequencing and characterizing odorant receptors of the cerambycid beetle Megacyllene caryae. Insect Biochem Mol Biol. 2012;42:499-505.
54. Robertson HM, Wanner KW. The chemoreceptor superfamily in the honey bee, Apis mellifera: expansion of the odorant, but not gustatory, receptor family. Genome Res. 2006;16:1395-403.
55. Croset V, Rytz R, Cummins SF, Budd A, Brawand D, Kaessmann H, et al. Ancient protostome origin of chemosensory ionotropic glutamate receptors and the evolution of insect taste and olfaction. PLoS Genet. 2010;6:e1001064.
56. Yin X-W, Iovinella I, Marangoni R, Cattonaro F, Flamini G, Sagona S, et al. Odorant-binding proteins and olfactory coding in the solitary bee Osmia cornuta. Cell Mol Life Sci. 2013;70:3029-39.
57. Forêt S, Maleszka R. Function and evolution of a gene family encoding odorant binding-like proteins in a social insect, the honey bee (Apis mellifera). Genome Res. 2006;16:1404-13.
58. Larsson MC, Domingos AI, Jones WD, Chiappe ME, Amrein H, Vosshall LB. Or83b encodes a broadly expressed odorant receptor essential for Drosophila olfaction. Neuron. 2004;43:703-14.
59. Jones WD, Nguyen T-AT, Kloss B, Lee KJ, Vosshall LB. Functional conservation of an insect odorant receptor gene across 250 million years of evolution. Curr Biol. 2005;15:R119-21.
60. Claudianos C, Lim J, Young M, Yan S, Cristino AS, Newcomb RD, et al. Odor memories regulate olfactory receptor expression in the sensory periphery. Eur J Neurosci. 2014;39:1642-54.
61. Mugal CF, Wolf JBW, Kaj I. Why time matters: codon evolution and the temporal dynamics of dN/dS. Mol Biol Evol. 2014;31:212-31.
62. Bielawski JP, Yang Z. Maximum likelihood methods for detecting adaptive protein evolution. In: Statistical Methods in Molecular Evolution. New York: Springer New York; 2005. p. 103-24 [Statistics for Biology and Health].
63. Inomata N, Goto H, Itoh M, Isono K. A single-amino-acid change of the gustatory receptor gene, Gr5a, has a major effect on trehalose sensitivity in a natural population of Drosophila melanogaster. Genetics. 2004;167:1749-58.
64. Pellegrino M, Steinbach N, Stensmyr MC, Hansson BS, Vosshall LB. A natural polymorphism alters odour and DEET sensitivity in an insect odorant receptor. Nature. 2011;478:511-4.
65. Richgels PK, Rollmann SM. Genetic variation in odorant receptors contributes to variation in olfactory behavior in a natural population of Drosophila melanogaster. Chem Senses. 2012;37:229-40.
66. Hughes DT, Wang G, Zwiebel LJ, Luetje CW. A determinant of odorant specificity is located at the extracellular loop 2-transmembrane domain 4 interface of an Anopheles gambiae odorant receptor subunit. Chem Senses. 2014;39:761-9.
67. Xu P, Leal WS. Probing insect odorant receptors with their cognate ligands: insights into structural features. Biochem Biophys Res Commun. 2013;435:477-82.
68. Tunstall NE, Sirey T, Newcomb RD, Warr CG. Selective pressures on Drosophila chemosensory receptor genes. J Mol Evol. 2007;64:628-36.
69. Carraher C, Authier A, Steinwender B, Newcomb RD. Sequence comparisons of odorant receptors among tortricid moths reveal different rates of molecular evolution among family members. PLoS One. 2012;7:e38391.
70. Miller R, Tu Z. Odorant receptor c-terminal motifs in divergent insect species. J Insect Sci. 2008;8:1-10.
71. Gardiner A, Barker D, Butlin RK, Jordan WC, Ritchie MG. Drosophila chemoreceptor gene evolution: selection, specialization and genome size. Mol Ecol. 2008;17:1648-57.
72. Almeida FC, Sánchez-Gracia A, Campos JL, Rozas J. Family size evolution in Drosophila chemosensory gene families: a comparative analysis with a critical appraisal of methods. Genome Biol Evol. 2014;6:1669-82.
73. Guo S, Kim J. Molecular evolution of Drosophila odorant receptor genes. Mol Biol Evol. 2007;24:1198-207.
74. McBride CS, Arguello JR, O'Meara BC. Five Drosophila genomes reveal nonneutral evolution and the signature of host specialization in the chemoreceptor superfamily. Genetics. 2007;177:1395-416.
75. Willett CS. Evidence for directional selection acting on pheromone-binding proteins in the genus Choristoneura. Mol Biol Evol. 2000;17:553-62.
76. Endo T, Ikeo K, Gojobori T. Large-scale search for genes on which positive selection may operate. Mol Biol Evol. 1996;13:685-90.
77. Peterson GI, Masel J. Quantitative prediction of molecular clock and ka/ks at short timescales. Mol Biol Evol. 2009;26:2595-603.
78. Smadja C, Shi P, Butlin RK, Robertson HM. Large gene family expansions and adaptive evolution for odorant and gustatory receptors in the pea aphid, Acyrthosiphon pisum. Mol Biol Evol. 2009;26:2073-86.
79. Smadja CM, Canbäck B, Vitalis R, Gautier M, Ferrari J, Zhou J-J, et al. Large-scale candidate gene scan reveals the role of chemoreceptor genes in host plant specialization and speciation in the pea aphid. Evolution. 2012;66:2723-38.
80. Civetta A, Singh RS. Sex-related genes, directional sexual selection, and speciation. Mol Biol Evol. 1998;15:901-9.
81. Mayer ML. Glutamate receptors at atomic resolution. Nature. 2006;440:456-62.
82. Naur P, Hansen KB, Kristensen AS, Dravid SM, Pickering DS, Olsen L, et al. Ionotropic glutamate-like receptor delta2 binds D-serine and glycine. Proc Natl Acad Sci U S A. 2007;104:14116-21.
83. Wiley C, Ellison CK, Shaw KL. Widespread genetic linkage of mating signals and preferences in the Hawaiian cricket Laupala. Proc Biol Sci. 2012;279:1203-9.
84. Roubik DW, Hanson PE. Orchid Bees of Tropical America: Biology and Field Guide. Santo Domingo De Heredia: Instituto Nacional de Biodiversidad (INBio); 2004.
85. Pokorny T, Hannibal M, Quezada-Euan JJG, Hedenström E, Sjöberg N, Bång J, et al. Acquisition of species-specific perfume blends: influence of habitat-dependent compound availability on odour choices of male orchid bees (Euglossa spp.). Oecologia. 2013;172:417-25.
86. Burriesci MS, Lehnert EM, Pringle JR. Fulcrum: condensing redundant reads from high-throughput sequencing studies. Bioinformatics. 2012;28:1324-7.
87. Martin J, Bruno VM, Fang Z, Meng X, Blow M, Zhang T, et al. Rnnotator: an automated de novo transcriptome assembly pipeline from stranded RNA-Seq reads. BMC Genomics. 2010;11:663.
88. Falgueras J, Lara AJ, Fernández-Pozo N, Cantón FR, Pérez-Trabado G, Claros MG. SeqTrim: a high-throughput pipeline for pre-processing any type of sequence read. BMC Bioinformatics. 2010;11:38.
89. Kumar S, Blaxter ML. Comparing de novo assemblers for 454 transcriptome data. BMC Genomics. 2010;11:571.
90. Feldmeyer B, Wheat CW, Krezdorn N, Rotter B, Pfenninger M. Short read Illumina data for the de novo assembly of a non-model snail species transcriptome (Radix balthica, Basommatophora, Pulmonata), and a comparison of assembler performance. BMC Genomics. 2011;12:317.
91. Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, et al. Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol. 2011;29:644-52.
92. Haas BJ, Papanicolaou A, Yassour M, Grabherr M, Blood PD, Bowden J, et al. De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis. Nat Protoc. 2013;8:1494-512.
93. Zerbino DR, Birney E. Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res. 2008;18:821-9.
94. Schulz MH, Zerbino DR, Vingron M, Birney E. Oases: robust de novo RNA-seq assembly across the dynamic range of expression levels. Bioinformatics. 2012;28:1086-92.
95. Surget-Groba Y, Montoya-Burgos JI. Optimization of de novo transcriptome assembly from next-generation sequencing data. Genome Res. 2010;20:1432-40.
96. Kent WJ. BLAT-the BLAST-like alignment tool. Genome Res. 2002;12:656-64.
97. Pruitt KD, Tatusova T, Klimke W, Maglott DR. NCBI reference sequences: current status, policy and new initiatives. Nucleic Acids Res. 2009;37(Database issue):D32-6.
98. Rivera MC, Jain R, Moore JE, Lake JA. Genomic evidence for two functionally distinct gene classes. Proc Natl Acad Sci U S A. 1998;95:6239-44.
99. Robertson HM, Gadau J, Wanner KW. The insect chemoreceptor superfamily of the parasitoid jewel wasp Nasonia vitripennis. Insect Mol Biol. 2010;19 Suppl 1:121-36.
100. Vieira FG, Rozas J. Comparative genomics of the odorant-binding and chemosensory protein gene families across the Arthropoda: origin and evolutionary history of the chemosensory system. Genome Biol Evol. 2011;3:476-90.
101. Vieira FG, Forêt S, He X, Rozas J, Field LM, Zhou J-J. Unique features of odorant-binding proteins of the parasitoid wasp Nasonia vitripennis revealed by genome annotation and comparative analyses. PLoS One. 2012;7:e43034.
102. Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nat Methods. 2012;9:357-9.
103. Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, et al. Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics. 2012;28:1647-9.
104. Stamatakis A. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics. 2006;22:2688-90.
105. Katoh K, Misawa K, Kuma K-I, Miyata T. MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res. 2002;30:3059-66.
106. Katoh K, Standley DM. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol. 2013;30:772-80.
107. Katoh K, Kuma K-I, Toh H, Miyata T. MAFFT version 5: improvement in accuracy of multiple sequence alignment. Nucleic Acids Res. 2005;33:511-8.
108. Darriba D, Taboada GL, Doallo R, Posada D. ProtTest 3: fast selection of best-fit models of protein evolution. Bioinformatics. 2011;27:1164-5.
109. Bielawski JP, Yang Z. A maximum likelihood method for detecting functional divergence at individual codon sites, with application to gene family evolution. J Mol Evol. 2004;59:121-32.
110. Yang Z. PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol. 2007;24:1586-91.
111. Hoffmann K. TMBASE-A database of membrane spanning protein segments. Biol Chem Hoppe-Seyler. 1993;374:166.
112. Krogh A, Larsson B, Heijne von G, Sonnhammer EL. Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol. 2001;305:567-80.
113. Bernsel A, Viklund H, Hennerdal A, Elofsson A. TOPCONS: consensus prediction of membrane protein topology. Nucleic Acids Res. 2009;37(Web Server issue):W465-8.
114. Möller S, Croning MD, Apweiler R. Evaluation of methods for the prediction of membrane spanning regions. Bioinformatics. 2001;17:646-53.