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Abstract:

Abstract: Previous comparative genomic studies of genes involved in olfactory behavior in Drosophila focused only on particular gene families such as odorant receptor and/or odorant binding proteins. However, olfactory behavior has a complex genetic architecture that is orchestrated by many interacting genes. In this paper, we present a comparative genomic study of olfactory behavior in Drosophila including an extended set of genes known to affect olfactory behavior. We took advantage of the recent burst of whole genome sequences and the development of powerful statistical tools to analyze genomic data and test evolutionary and functional hypotheses of olfactory genes in the six species of the Drosophila melanogaster species group for which whole genome sequences are available. Our study reveals widespread purifying selection and limited incidence of positive selection on olfactory genes. We show that the pace of evolution of olfactory genes is mostly independent of the life cycle stage, and of the number of life cycle stages, in which they participate in olfaction. However, we detected a relationship between evolutionary rates and the position that the gene products occupy in the olfactory system, genes occupying central positions tend to be more constrained than peripheral genes. Finally, we demonstrate that specialization to one host does not seem to be associated with bursts of adaptive evolution in olfactory genes in D. sechellia and D. erecta, the two specialists species analyzed, but rather different lineages have idiosyncratic evolutionary histories in which both historical and ecological factors have been involved. © the author(s), publisher and licensee Libertas Academica Ltd.

Registro:

Documento: Artículo
Título:Evolutionary genomics of genes involved in olfactory behavior in the Drosophila melanogaster species group
Autor:Lavagnino, N.; Serra, F.; Arbiza, L.; Dopazo, H.; Hasson, E.
Filiación:Departamento de Ecología, Genética y Evolución, Facultad de Ciencias Exactas y Naturales, Buenos Aires, Argentina
Instituto de Ecología, Genética y Evolución (IEGEBA), CONICET, Buenos Aires, Argentina
Evolutionary Genomics Unit, Bioinformatics and Genomic Department, Centro de Investigación Príncipe Felipe, Valencia, Spain
Palabras clave:Adaptation; Drosophila melanogaster species group; Evolutionary genomics; Insects; Olfactory behavior; arthropod life cycle stage; article; controlled study; Drosophila; Drosophila ananassae; drosophila erecta; Drosophila melanogaster; Drosophila sechellia; Drosophila simulans; Drosophila yakuba; evolutionary rate; gene sequence; insect genetics; insect genome; molecular evolution; nonhuman; olfactory system; smelling; Drosophila erecta; Drosophila melanogaster; Drosophila sechellia; Hexapoda
Año:2011
Volumen:2011
Número:7
Página de inicio:89
Página de fin:104
DOI: http://dx.doi.org/10.4137/EBO.S8484
Título revista:Evolutionary Bioinformatics
Título revista abreviado:Evol. Bioinformatics
ISSN:11769343
PDF:https://bibliotecadigital.exactas.uba.ar/download/paper/paper_11769343_v2011_n7_p89_Lavagnino.pdf
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_11769343_v2011_n7_p89_Lavagnino

Referencias:

  • Hallem, E.A., Dahanukar, A., Carlson, J.R., Insect odor and taste receptors (2006) Annu Rev Entomol, 51, pp. 113-135
  • Vosshall, L.B., Stocker, R.F., Molecular architecture of smell and taste in Drosophila (2007) Annu Rev Neurosci, 30, pp. 505-533
  • Young, J.M., Trask, B.J., The sense of smell: Genomics of vertebrate odorant receptors (2002) Hum Mol Genet, 11, pp. 1153-1160
  • Buck, L.B., The search for odorant receptors (2004) Cell, 116, pp. 117-119
  • Halász, N., (1990) The Vertebrate Olfactory System: Chemical Neuroanatomy, Function, and Development, , Budapest: Akadémiai Kiadó
  • Pelosi, P., Maida, R., Odorant-binding proteins in insects (1995) Comp Biochem Physiol B Biochem Mol Biol, 111, pp. 503-514
  • Steinbrecht, R.A., Odorant-binding proteins: Expression and function (1998) Ann N Y Acad Sci, 855, pp. 323-332
  • Anholt, R.R., Fanara, J.J., Fedorowicz, G.M., Functional genomics of odor-guided behavior in Drosophila melanogaster (2001) Chem Senses, 26, pp. 215-221
  • Anholt, R.R., Lyman, R.F., Mackay, T.F., Effects of single P-element insertions on olfactory behavior in Drosophila melanogaster (1996) Genetics, 143, pp. 293-301
  • Goulding, S.E., Zur, L.P., Jarman, A.P., Amos, a proneural gene for Drosophila olfactory sense organs that is regulated by lozenge (2000) Neuron, 25, pp. 69-78
  • Zur, L.P.I., Prentice, D.R., Holohan, E.E., Jarman, A.P., The Drosophila proneural gene amos promotes olfactory sensillum formation and suppresses bristle formation (2003) Development, 130, pp. 4683-4693
  • Shiraiwa, T., Nitasaka, E., Yamazaki, T., Geko, a novel gene involved in olfaction in Drosophila melanogaster (2000) J Neurogenet, 14, pp. 145-164
  • Stoltzfus, J.R., Horton, W.J., Grotewiel, M.S., Odor-guided behavior in Drosophila requires calreticulin (2003) J Comp Physiol a Neuroethol Sens Neural Behav Physiol, 189, pp. 471-483
  • Sambandan, D., Yamamoto, A., Fanara, J.J., Mackay, T.F., Anholt, R.R., Dynamic genetic interactions determine odor-guided behavior in Drosophila melanogaster (2006) Genetics, 174, pp. 1349-1363
  • Anholt, R.R., Mackay, T.F., Quantitative genetic analyses of complex behaviours in Drosophila (2004) Nat Rev Genet, 5, pp. 838-849
  • Hansen, T.F., The evolution of genetic architecture (2006) Annu Rev Ecol Evol Syst, 37, pp. 123-157
  • Anholt, R.R., Dilda, C.L., Chang, S., The genetic architecture of odor-guided behavior in Drosophila: Epistasis and the transcriptome (2003) Nat Genet, 35, pp. 180-184
  • Anholt, R.R., Mackay, T.F., The genetic architecture of odor-guided behavior in Drosophila melanogaster (2001) Behav Genet, 31, pp. 17-27
  • Fedorowicz, G.M., Fry, J.D., Anholt, R.R., Mackay, T.F., Epistatic interactions between smell-impaired loci in Drosophila melanogaster (1998) Genetics, 148, pp. 1885-1891
  • Lavagnino, N.J., Anholt, R.R., Fanara, J.J., Variation in genetic architecture of olfactory behaviour among wild-derived populations of Drosophila melanogaster (2008) J Evol Biol, 21, pp. 988-996
  • Sambandan, D., Carbone, M.A., Anholt, R.R., Mackay, T.F., Phenotypic plasticity and genotype by environment interaction for olfactory behavior in Drosophila melanogaster (2008) Genetics, 179, pp. 1079-1088
  • Guo, S., Kim, J., Molecular evolution of Drosophila odorant receptor genes (2007) Mol Biol Evol, 24, pp. 1198-1207
  • McBride, C.S., Rapid evolution of smell and taste receptor genes during host specialization in Drosophila sechellia (2007) Proc Natl Acad Sci U S A, 104, pp. 4996-5001
  • McBride, C.S., Arguello, J.R., Five Drosophila genomes reveal nonneutral evolution and the signature of host specialization in the chemoreceptor super-family (2007) Genetics, 177, pp. 1395-1416
  • Tunstall, N.E., Sirey, T., Newcomb, R.D., Warr, C.G., Selective pressures on Drosophila chemosensory receptor genes (2007) J Mol Evol, 64, pp. 628-636
  • Gardiner, A., Barker, D., Butlin, R.K., Jordan, W.C., Ritchie, M.G., Drosophila chemoreceptor gene evolution: Selection, specialization and genome size (2008) Mol Ecol, 17, pp. 1648-1657
  • Vieira, F.G., Sanchez-Gracia, A., Rozas, J., Comparative genomic analysis of the odorant-binding protein family in 12 Drosophila genomes: Purifying selection and birth-and-death evolution (2007) Genome Biol, 8, pp. R235
  • Yang, Z., PAML 4: Phylogenetic analysis by maximum likelihood (2007) Mol Biol Evol, 24, pp. 1586-1591
  • Yang, Z., Adaptive Molecular Evolution (2003) Handbook of Statistical Genetics, pp. 229-254. , In: Balding D, Bishop M, Cannings C, eds., 2nd ed. New York: John Wiley & Sons, Ltd
  • Clark, A.G., Eisen, M.B., Smith, D.R., Evolution of genes and genomes on the Drosophila phylogeny (2007) Nature, 450, pp. 203-218
  • Andruss, B.F., Lu, A.Q., Beckingham, K., Expression of calmodulin in Drosophila is highly regulated in a stage-and tissue-specific manner (1997) Development Genes and Evolution, 206, pp. 541-545
  • Shaver, S.A., Varnam, C.J., Hilliker, A.J., Sokolowski, M.B., The foraging gene affects adult but not larval olfactory-related behavior in Drosophila melanogaster (1998) Behav Brain Res, 95, pp. 23-29
  • Hodgkin, J., Seven types of pleiotropy (1998) Int J Dev Biol, 42, pp. 501-505
  • Louis, J., David, J.R., Ecological specialization in the Drosophila melanogaster species subgroup: A case study of Drosophila sechellia (1986) Acta Oecol, 7, pp. 215-230
  • Tsacas, L., Bächli, G., Drosophila sechellia, n. sp., huitième espèce du sous-groupe melanogaster des Iles Seychelles (Diptera, Drosophilidae) (1981) Rev Fr Entomol, 3, pp. 146-150
  • R'kha, S., Capy, P., David, J.R., Host-plant specialization in the Drosophila melanogaster species complex: A physiological, behavioral, and genetical analysis (1991) Proc Natl Acad Sci U S A, 88, pp. 1835-1839
  • Rio, B., Couturier, G., Lemeunier, F., Lachaise, D., Evolution d'une specialisation saisonniere chez Drosophila erecta (Dipt., Drosophilidae) (1983) Annls Soc Ent Fr (NS), 19, pp. 235-248
  • Lachaise, D., Silvain, J.F., How two Afrotropical endemics made two cosmopolitan human commensals: The Drosophila melanogaster-D. simulans palaeogeographic riddle (2004) Genetica, 120, pp. 17-39
  • Markow, T.A., O'Grady, P.M., Drosophila biology in the genomic age (2007) Genetics, 177, pp. 1269-1276
  • Pollard, D.A., Iyer, V.N., Moses, A.M., Eisen, M.B., Widespread discordance of gene trees with species tree in Drosophila: Evidence for incomplete lineage sorting (2006) PLoS Genet, 2, p. 173
  • Edgar, R.C., MUSCLE: Multiple sequence alignment with high accuracy and high throughput (2004) Nucleic Acids Res, 32, pp. 1792-1797
  • Edgar, R.C., MUSCLE: A multiple sequence alignment method with reduced time and space complexity (2004) BMC Bioinformatics, 5, p. 113
  • Zhang, J., Nielsen, R., Yang, Z., Evaluation of an improved branch-site likeli-hood method for detecting positive selection at the molecular level (2005) Mol Biol Evol, 22, pp. 2472-2479
  • Zhang, J., Frequent false detection of positive selection by the likelihood method with branch-site models (2004) Mol Biol Evol, 21, pp. 1332-1339
  • (2010) A Language and Environment For Statistical Computing, , R Development Core Team, Vienna, Austria: R Foundation for Statistical Computing
  • Benjamini, Y., Hochberg, Y., Controlling the false discovery rate: A practical and powerful approach to multiple testing (1995) J Roy Stat Soc B Stat Meth, 57, pp. 289-300
  • Chintapalli, V.R., Wang, J., Dow, J.A., Using FlyAtlas to identify better Drosophila melanogaster models of human disease (2007) Nat Genet, 39, pp. 715-720
  • Whiteman, N.K., Pierce, N.E., Delicious poison: Genetics of Drosophila host plant preference (2008) Trends Ecol Evol, 23, pp. 473-478
  • Artieri, C.G., Haerty, W., Singh, R.S., Ontogeny and phylogeny: Molecular signatures of selection, constraint, and temporal pleiotropy in the development of Drosophila (2009) BMC Biol, 7, p. 42
  • Ayer Jr., R.K., Carlson, J., Acj6: A gene affecting olfactory physiology and behavior in Drosophila (1991) Proc Natl Acad Sci U S A, 88, pp. 5467-5471
  • Tissot, M., Stocker, R.F., Metamorphosis in Drosophila and other insects: The fate of neurons throughout the stages (2000) Prog Neurobiol, 62, pp. 89-111
  • Shanbhag, S.R., Muller, B., Steinbrecht, R.A., Atlas of olfactory organs of Drosophila melanogaster 1. Types, external organization, innervation and distribution of olfactory sensilla (1999) Int J Insect Morphol Embryol, 28, pp. 377-397
  • Python, F., Stocker, R.F., Adult-like complexity of the larval antennal lobe of D. melanogaster despite markedly low numbers of odorant receptor neurons (2002) J Comp Neurol, 445 (4), pp. 374-387
  • Arbeitman, M.N., Furlong, E.E., Imam, F., Gene expression during the life cycle of Drosophila melanogaster (2002) Science, 297, pp. 2270-2275
  • Kliman, R.M., Andolfatto, P., Coyne, J.A., The population genetics of the origin and divergence of the Drosophila simulans complex species (2000) Genetics, 156, pp. 1913-1931
  • Morton, R.A., Choudhary, M., Cariou, M.L., Singh, R.S., A reanalysis of protein polymorphism in Drosophila melanogaster, D. simulans, D. sechellia and D. mauritiana: Effects of population size and selection (2004) Genetica, 120, pp. 101-104
  • Alvarez-Ponce, D., Aguade, M., Rozas, J., Network-level molecular evolutionary analysis of the insulin/TOR signal transduction pathway across 12 Drosophila genomes (2009) Genome Res, 19, pp. 234-242
  • Salathe, M., Ackermann, M., Bonhoeffer, S., The effect of multifunctionality on the rate of evolution in yeast (2006) Mol Biol Evol, 23, pp. 721-722
  • He, X., Zhang, J., Toward a molecular understanding of pleiotropy (2006) Genetics, 173, pp. 1885-1891
  • Otto, S.P., Two steps forward, one step back: The pleiotropic effects of favoured alleles (2004) Proc R Soc Lond B Biol Sci, 271. , 705-514
  • Gu, X., Evolutionary framework for protein sequence evolution and gene pleiotropy (2007) Genetics, 175, pp. 1813-1822
  • Proulx, S.R., Promislow, D.E., Phillips, P.C., Network thinking in ecology and evolution (2005) Trends Ecol Evol, 20, pp. 345-353
  • Cariou, M.L., Solignac, M., Monnerot, M., David, J.R., Low allozyme and mtDNA variability in the island endemic species Drosophila sechellia (D. melanogaster complex) (1990) Experientia, 46, pp. 101-104
  • Lavagnino, N.J., (2011) Evolución De La Arquitectura Genética Del Comportamiento Olfativo En Drosophila, , http://digital.bl.fcen.uba.ar/Download/Tesis/Tesis_4849_Lavagnino.pdf, [PhD. Thesis], Facultad de Ciencias Exactas y Naturales. Universidad de Buenos Aires, Avalaible at
  • Fanara, J.J., Robinson, K.O., Rollmann, S.M., Anholt, R.R., Mackay, T.F., Vanaso is a candidate quantitative trait gene for Drosophila olfactory behavior (2002) Genetics, 162, pp. 1321-1328
  • Pielage, J., Stork, T., Bunse, I., Klambt, C., The Drosophila cell survival gene discs lost encodes a cytoplasmic Codanin-1-like protein, not a homolog of tight junction PDZ protein Patj (2003) Dev Cell, 5, pp. 841-851
  • Rollmann, S.M., Mackay, T.F., Anholt, R.R., Pinocchio, a novel protein expressed in the antenna, contributes to olfactory behavior in Drosophila melanogaster (2005) J Neurobiol, 63, pp. 146-158
  • Galindo, K., Smith, D.P., A large family of divergent Drosophila odorant- binding proteins expressed in gustatory and olfactory sensilla (2001) Genetics, 159, pp. 1059-1072
  • Hekmat-Scafe, D.S., Scafe, C.R., McKinney, A.J., Tanouye, M.A., Genome- wide analysis of the odorant-binding protein gene family in Drosophila melanogaster (2002) Genome Res, 12, pp. 1357-1369
  • Pikielny, C.W., Hasan, G., Rouyer, F., Rosbash, M., Members of a family of Drosophila putative odorant-binding proteins are expressed in different subsets of olfactory hairs (1994) Neuron, 12, pp. 35-49
  • Park, S.K., Shanbhag, S.R., Wang, Q., Hasan, G., Steinbrecht, R.A., Pikielny, C.W., Expression patterns of two putative odorant-binding proteins in the olfactory organs of Drosophila melanogaster have different implications for their functions (2000) Cell Tissue Res, 300, pp. 181-192

Citas:

---------- APA ----------
Lavagnino, N., Serra, F., Arbiza, L., Dopazo, H. & Hasson, E. (2011) . Evolutionary genomics of genes involved in olfactory behavior in the Drosophila melanogaster species group. Evolutionary Bioinformatics, 2011(7), 89-104.
http://dx.doi.org/10.4137/EBO.S8484
---------- CHICAGO ----------
Lavagnino, N., Serra, F., Arbiza, L., Dopazo, H., Hasson, E. "Evolutionary genomics of genes involved in olfactory behavior in the Drosophila melanogaster species group" . Evolutionary Bioinformatics 2011, no. 7 (2011) : 89-104.
http://dx.doi.org/10.4137/EBO.S8484
---------- MLA ----------
Lavagnino, N., Serra, F., Arbiza, L., Dopazo, H., Hasson, E. "Evolutionary genomics of genes involved in olfactory behavior in the Drosophila melanogaster species group" . Evolutionary Bioinformatics, vol. 2011, no. 7, 2011, pp. 89-104.
http://dx.doi.org/10.4137/EBO.S8484
---------- VANCOUVER ----------
Lavagnino, N., Serra, F., Arbiza, L., Dopazo, H., Hasson, E. Evolutionary genomics of genes involved in olfactory behavior in the Drosophila melanogaster species group. Evol. Bioinformatics. 2011;2011(7):89-104.
http://dx.doi.org/10.4137/EBO.S8484