Comparative genomics of chemosensory protein genes reveals rapid evolution and positive selection in ant-specific duplicates

Heredity

Volumn 110, Issue 6, 2013, Pages 538-547

  Kulmuni, J ^a,b   Wurm, Y ^c,d   Pamilo, P ^b  

^a UNIVERSITY OF OULU   (Finland)

^b UNIVERSITY OF HELSINKI   (Finland)

^c QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^d UNIVERSITY OF LAUSANNE   (Switzerland)

Author keywords

chemosensory protein; Formicidae; gene duplication; gene family; positive selection

Indexed keywords

INSECT PROTEIN;

ADAPTATION; ANT; CHEMICAL CUE; CHEMORECEPTION; EVOLUTIONARY BIOLOGY; GENE EXPRESSION; GENOMICS; NATURAL SELECTION; NESTMATE RECOGNITION; PHYLOGENETICS; PROTEIN; SOCIAL INSECT;

ANIMAL; ANT; ARTICLE; GENE DUPLICATION; GENETIC SELECTION; GENETICS; GENOME; GENOMICS; MOLECULAR EVOLUTION; MOLECULAR GENETICS; PHYLOGENY; PSEUDOGENE;

ANIMALS; ANTS; EVOLUTION, MOLECULAR; GENE DUPLICATION; GENOME; GENOMICS; INSECT PROTEINS; MOLECULAR SEQUENCE ANNOTATION; PHYLOGENY; PSEUDOGENES; SELECTION, GENETIC;

FORMICIDAE; HEXAPODA;

EID: 84878548316     PISSN: 0018067X     EISSN: 13652540     Source Type: Journal    
DOI: 10.1038/hdy.2012.122     Document Type: Article

References (60)

1. Bielawski JP, Yang Z (2005). Maximum likelihood methods for detecting adaptive protein evolution. In: Nielsen R (ed) Statistical Methods in Molecular Evolution. Springer: New York, USA.
2. Bonasio R, Zhang G, Ye C, Mutti S, Fang X, Qin Net al. (2010). Genomic comparison of the ants Camponotus floridanus and Harpegnathos saltator. Science 329: 1068-1031.
3. Brady SG, Schultz TR, Fisher BL, Ward PS (2006). Evaluating alternative hypotheses for the early evolution and diversification of ants. Proc Natl Acad Sci USA 103: 18172-18177. (Pubitemid 44871631)
4. Campanacci V, Lartique A, Hällberg BM, Jones TA, Giudici-Orticoni MT, Tegoni Met al. (2003). Moth chemosensory protein exhibits drastic conformational changes and cooperativity on ligand binding. Proc Natl Acad Sci USA 100: 5069-5074. (Pubitemid 36542659)
5. Chen FC, Chen CJ, Li WH, Chuang TJ (2010). Gene family size conservation is a good indicator of evolutionary rates. Mol Biol Evol 27: 1750-1758.
6. Demuth JP, Hahn MW (2009). The life and death of gene families. BioEssays 31: 29-39.
7. Edgar RC (2004). MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32: 1792-1797. (Pubitemid 38832724)
8. Engsontia P, Sanderson AP, Cobb M, Walden KKO, Robertson HM, Brown S (2008). The red flour beetle's large nose: an expanded odorant receptor gene family in Tribolium castaneum. Insect Biochem Mol Biol 38: 387-397.
9. Forê t S, Maleszka R (2006). Function and evolution of a gene family encoding odorant binding-like proteins in a social insect, the honey bee (Apis mellifera). Genome Res 16: 1404-1413. (Pubitemid 44664683)
10. Forê t S, Wanner KW, Maleszka R (2007). Chemosensory proteins in the honey bee: insights from the annotated genome, comparative analyses and expressional profiling. Insect Biochem Mol Biol 37: 19-28. (Pubitemid 44908971)
11. Gardiner A, Barker D, Butlin RK, Jordan CJ, Ritchie MG (2008). Drosophila chemoreceptor gene evolution: selection, specialization and genome size. Mol Ecol 17: 1648-1657. (Pubitemid 351441718)
12. Gong DP, Zhang H, Zhao P, Lin Y, Xia QY, Xiang ZH (2007). Identification and expression pattern of the chemosensory protein gene family in the silkworm, Bombyx mori. Insect Biochem Mol Biol 37: 266-277. (Pubitemid 46216818)
13. Gonza'lez D, Zhao Q, McMahan C, Velasquez D, Haskins WE, Sponsel Vet al. (2009). The major antennal chemosensory protein of red imported fire ant workers. Insect Mol Biol 18: 395-404.
14. He X, Zhang J (2006). Higher duplicability of less important genes in yeast genomes. Mol Biol Evol 23: 144-151. (Pubitemid 41785961)
15. Holman L, Jorgensen CG, Nielsen J, d'Ettorre P (2010). Identification of an ant queen pheromone regulating worker sterility. Proc R Soc B 277: 3793-3800.
16. Hunt BG, Ometto L, Wurm Y, Shoemaker D, Yi SV, Keller Let al. (2011). Relaxed selection is a precursor to the evolution of phenotypic plasticity. Proc Natl Acad Sci USA 108: 15936-15941.
17. Innan H, Kondrashov F (2010). The evolution of gene duplications: classifying and distinguishing between models. Nat Rev Genet 11: 97-108.
18. Ishida Y, Chiang V, Leal WS (2002). Protein that makes sense in the Argentine ant. Naturwissenschaften 89: 505-507. (Pubitemid 35454367)
19. Jordan G, Goldman N (2012). The effects of alignment error and alignment filtering on the sitewise detection of positive selection. Mol Biol Evol 29: 1125-1139.
20. Katoh K, Kuma K, Toh H, Miyata T (2005). MAFFT version 5: improvement in accuracy of multiple sequence alignment. Nucleic Acids Res 33: 511-518. (Pubitemid 40360980)
21. Kelley LA, Sternberg MJE (2009). Protein structure prediction on the web: a case study using the Phyre server. Nat Protoc 4: 363-371.
22. Kosakovsky Pond SL, Frost SDW (2005a). Datamonkey: rapid detection of selective pressure on individual sites of codon alignments. Bioinformatics 21: 2531-2533. (Pubitemid 40731616)
23. Kosakovsky Pond SL, Frost SDW (2005b). Not so different after all: a comparison of methods for detecting amino acid sites under selection. Mol Biol Evol 22: 1208-1222. (Pubitemid 40577758)
24. Lahav S, Soroker V, Hefetz A, Vander MRK (1999). Direct behavioral evidence for hydrocarbons as ant recognition discriminators. Naturwissenschaften 86: 246-249. (Pubitemid 29251878)
25. Leal WS, Chen AM, Ishida Y, Chiang VP, Erickson ML, Morgan TIet al. (2005). Kinetics and molecular properties of pheromone binding and release. Proc Natl Acad Sci USA 102: 5386-5391. (Pubitemid 40530267)
26. Librado P, Vieira FG, Rozas J (2011). BadiRate: estimating family turnover rates by likelihood-based methods. Bioinformatics 28: 279-281.
27. Lo?ytynoja A, Goldman N (2005). An algorithm for progressive multiple alignment of sequences with insertions. Proc Natl Acad Sci USA 102: 10557-10562. (Pubitemid 41061593)
28. Maleszka J, Forê t S, Saint R, Maleszka R (2007). RNAi-induced phenotypes suggest a novel role for a chemosensory protein CSP5 in the development of embryonic integument in the honey bee (Apis mellifera). Dev Genes Evol 217: 189-196.
29. Marchler-Bauer A, Lu S, Anderson JB, Chitsaz F, Derbyshire MK, DeWeese-Scott Cet al. (2011). CDD: a conserved domain database for the functional annotation of proteins. Nucleic Acids Res 39: D225-D229.
30. Moreau CS, Bell CD, Vila R, Archibald SB, Pierce NE (2006). Phylogeny of the ants: Diversification in the age of angiosperms. Science 312: 101-104.
31. Munoz-Torres MC, Reese JT, Childers CP, Bennett AK, Sundaram JP, Childs KLet al. (2011). Hymenoptera genome database: integrated community resources for insect species of the order Hymenoptera. Nucleic Acids Res 39: D658-D662.
32. Nei M, Niimura Y, Nozawa M (2008). The evolution of animal chemosensory receptor gene repertoires: roles of chance and necessity. Nature Rev Genet 9: 951-963. (Pubitemid 50329069)
33. Nei M, Rooney AP (2005). Concerted and birth-and-death evolution of multigene families. Annu Rev Genet 39: 121-152. (Pubitemid 43011110)
34. Nozawa M, Nei M (2007). Evolutionary dynamics of olfactory receptor genes in Drosophila species. Proc Natl Acad Sci USA 104: 7122-7127. (Pubitemid 47186019)
35. Nygaard S, Zhang G, Schiøtt M, Li C, Wurm Y, Hu Het al. (2011). The genome of the leafcutting ant Acromyrmex echinatior suggests key adaptations to advanced social life and fungus farming. Genome Res 21: 1339-1348.
36. Ozaki M, Wada-Katsumata A, Fujikawa K, Iwasaki M, Yokohari F, Satoji Yet al. (2005). Ant nestmate and non-nestmate discrimination by a chemosensory sensillum. Science 309: 311-314. (Pubitemid 40967870)
37. Pal C, Papp B, Hurst LD (2001). Highly expressed genes in yeast evolve slowly. Genetics 158: 927-931. (Pubitemid 32552328)
38. Pelosi P, Zhou JJ, Ban LP, Calvello M (2006). Soluble proteins in insect chemical communication. Cell Mol Life Sci 63: 1658-1676. (Pubitemid 44252179)
39. Penn O, Privman E, Ashkenazy H, Landan G, Graur D, Pupko T (2010). GUIDANCE: a web server for assessing alignment confidence scores. Nucleic Acids Res 38: W23-W28.
40. Privman E, Penn O, Pupko T (2012). Improving the performance of positive selection inference by filtering unreliable alignment regions. Mol Biol Evol 29: 1-5.
41. Sackton TB, Lazzarro BP, Schlenke TA, Evans JD, Hultmark D, Clark AG (2007). Dynamic evolution of the innate immune system in Drosophila. Nature Genet 39: 1461-1468. (Pubitemid 350191353)
42. Schrider DR, Hahn MW (2010). Gene copy-number polymorphism in nature. Proc R Soc B 277: 3213-3221.
43. Smadja C, Canba?ck B, Vitalis R, Gautier M, Ferrari J, Zhou JJet al. (2012). Large-scale candidate gene scan reveals the role of chemoreceptor genes in host plant specialisation and speciation in the pea aphid. Evolution 66: 2723-2738.
44. Smadja C, Shi P, Butlin RK, Robertson HM (2009). Large gene family expansions and adaptive evolution for odorant and gustatory receptors in the pea aphid, Acyrthosiphon pisum. Mol Biol Evol 26: 2073-2086.
45. Smith CD, Zimin A, Holt C, Abouheif E, Benton R, Cash Eet al. (2011). Draft genome of the globally widespread and invasive Argentine ant (Linepithema humile). Proc Natl Acad Sci USA 108: 5673-5678.
46. Smith CR, Smith CD, Robertson HM, Helmkampf M, Zimin A, Yandell Met al. (2011). A draft genome of the red harvester ant, Pogonomyrmex barbatus. Proc Natl Acad Sci USA 108: 5667-5672.
47. Stamatakis A (2006). RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22: 2688-2690. (Pubitemid 44642609)
48. Stamatakis A, Hoover P, Rougemont J (2008). A rapid bootstrap algorithm for the RAxML Web servers. Syst Biol 57: 758-771.
49. Suen G, Teiling C, Li L, Holt C, Abouheif E, Bornberg-Bauer Eet al. (2011). The genome sequence of the leaf-cutter ant Atta cephalotes reveals insights into its obligate symbiotic lifestyle. Plos Genet 7: e1002007.
50. Swanson WJ, Vacquier VD (2002). Rapid evolution of reproductive proteins. Nature Rev Genet 3: 137-144.
51. Sa'nchez-Gracia A, Vieira FG, Rozas J (2009). Molecular evolution of the major chemosensory gene families in insects. Heredity 103: 208-216.
52. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011). MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28: 2731-2739.
53. Vieira FG, Rozas J (2011). 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 3: 476-490.
54. Vieira FG, Sa'nchez-Gracia A, Rozas J (2007). Comparative genomic analysis of the odorant-binding protein family in 12 Drosophila genomes: purifying selection and birthand- death evolution. Genome Biol 8: R235.
55. Vosshall LB, Stocker RE (2007). Molecular architecture of smell and taste in Drosophila. Annu Rev Neurosci 30: 505-533. (Pubitemid 47218766)
56. Wurm Y, Wang J, Riba-Grognuz O, Corona M, Nygaard S, Hunt BGet al. (2011). Genome of the fire ant Solenopsis invicta. Proc Natl Acad Sci USA 108: 5679-5684.
57. Xu YL, He P, Zhang L, Fang SQ, Dong SL, Zhang YJet al. (2009). Large-scale identification of odorant-binding proteins and chemosensory proteins from expressed sequence tags in insects. BMC Genomics 10: 632.
58. Yang ZH (2007). PAML 4: a program package for phylogenetic analysis by maximum likelihood. Mol Biol Evol 24: 1586-1591.
59. Zhou JJ, Kan Y, Antyoniw J, Pickett JA, Field LM (2006). Genome and EST analyses and expression of a gene family with putative functions in insect chemoreception. Chem Senses 31: 453-465. (Pubitemid 43978556)
60. Zhou JJ, Vieira FG, He XL, Smadja C, Liu R, Rozas Jet al. (2010). Genome annotation and comparative analyses of the odorant-binding proteins and chemosensory proteins in the pea aphid Acyrthosiphon pisum. Insect Mol Biol 19: 113-122.