Selection on an antimicrobial peptide defensin in ants

Journal of Molecular Evolution

Volumn 67, Issue 6, 2008, Pages 643-652

  Viljakainen, Lumi ^a   Pamilo, Pekka ^a,b  

^a UNIVERSITY OF OULU   (Finland)

^b UNIVERSITY OF HELSINKI   (Finland)

Author keywords

Ant; Defensin; Formica; Hymenoptera; Immune gene; Positive selection; Social insect

Indexed keywords

DEFENSIN; ANTIINFECTIVE AGENT;

AMINO ACID SEQUENCE; ANT; ARTICLE; CODON; GENE; IMMUNE SYSTEM; INSECT GENETICS; INSECT SOCIETY; ISOPTERA; MAXIMUM LIKELIHOOD METHOD; MOLECULAR EVOLUTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; SPECIES; TERMICIN GENE; ANIMAL; CHEMICAL STRUCTURE; CHEMISTRY; GENETIC SELECTION; GENETICS; METABOLISM; MOLECULAR GENETICS; PROTEIN TERTIARY STRUCTURE; SEQUENCE ALIGNMENT;

DIPTERA; FORMICA; FORMICIDAE; HEXAPODA; HYMENOPTERA; ISOPTERA;

AMINO ACID SEQUENCE; ANIMALS; ANTI-BACTERIAL AGENTS; ANTS; DEFENSINS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PHYLOGENY; PROTEIN STRUCTURE, TERTIARY; SELECTION (GENETICS); SEQUENCE ALIGNMENT;

EID: 65349134700     PISSN: 00222844     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00239-008-9173-6     Document Type: Article

References (74)

1. M Anisimova JP Bielawski Z Yang 2002 Accuracy and power of Bayes prediction of amino acid sites under positive selection Mol Biol Evol 19 950 958 (Pubitemid 34602964)
2. B Baer P Schmid-Hempel 1999 Experimental variation in polyandry affects parasite loads and fitness in a bumblebee Nature 397 151 154
3. B Baer P Schmid-Hempel 2001 Unexpected consequences of polyandry for parasitism and fitness in the bumblebee, Bombus terrestris Evolution 55 1639 1643 (Pubitemid 32908225)
4. M Boniotto A Tossi M DelPero S Sgubin N Antcheva D Santon J Masters S Crovella 2003 Evolution of the beta defensin 2 gene in primates Genes Immun 4 251 257 (Pubitemid 39562123)
5. SG Brady TR Schultz BL Fisher PS Ward 2006 Evaluating alternative hypotheses for the early evolution and diversification of ants Proc Natl Acad Sci USA 103 18172 18177 (Pubitemid 44871631)
6. L Bromham R Leys 2005 Sociality and the rate of molecular evolution Mol Biol Evol 22 1393 1402 (Pubitemid 40740250)
7. MS Bulmer RH Crozier 2004 Duplication and diversifying selection among termite antifungal peptides Mol Biol Evol 21 2256 2264 (Pubitemid 39488896)
8. MS Bulmer RH Crozier 2006 Variation in positive selection in termite GNBPs and Relish Mol Biol Evol 23 317 326 (Pubitemid 43100046)
9. P Christe A Oppliger F Bancala G Castella M Chapuisat 2003 Evidence of collective medication in ants Ecol Lett 6 19 22
10. M Chapuisat A Opplinger P Magliano P Christe 2007 Wood ants use resin to protect themselves against pathogens Proc R Soc London B 274 2013 2017 (Pubitemid 47122202)
11. B Cornet J-M Bonmatin C Hetru JA Hoffman M Ptak F Vovelle 1995 Refined three-dimensional solution structure of insect defensin A Structure 3 435 448
12. S Cremer SAO Armitage P Schmid-Hempel 2007 Social immunity Curr Biol 17 R693 R702
13. P Da Silva L Jouvensal M Lamberty P Bulet A Caille F Vovelle 2003 Solution structure of termicin, an antimicrobial peptide from the termite Pseudacanthotermes spiniger Protein Sci 12 438 446 (Pubitemid 36241103)
14. JD Evans K Aronstein YP Chen C Hetru J-L Imler H Jiang M Kanost GJ Thompson Z Zou D Hultmark 2006 Immune pathways and defence mechanisms in honey bees Apis mellifera Insect Mol Biol 15 645 656 (Pubitemid 44652092)
15. D Ferrandon JL Imler C Hetru JA Hoffmann 2007 The Drosophila systemic immune response:sensing and signalling during bacterial and fungal infections Nat Rev Immunol 7 862 874 (Pubitemid 350006241)
16. O Froy M Gurevitz 2003 Arthropod and mollusk defensins-evolution by exon-shuffling Trends Genet 19 684 687
17. N Goldman Z Yang 1994 A codon-based model of nucleotide substitution for protein-coding DNA sequences Mol Biol Evol 11 725 736
18. AV Goropashnaya VB Fedorov P Pamilo 2004 Recent speciation in the Formica rufa group ants (Hymenoptera, Formicidae): inference from mitochondrial DNA phylogeny Mol Phylogenet Evol 32 198 206 (Pubitemid 38861672)
19. AV Goropashnaya VB Fedorov B Seifert P Pamilo 2007 Phylogeography and population structure in the ant Formica exsecta (Hymenoptera, Formicidae) across Eurasia as reflected by mitochondrial DNA variation and microsatellites Ann Zool Fenn 44 462 474
20. E Hasegawa A Tinaut F Ruano 2002 Molecular phylogeny of two slave-making ants: Rossomyrmex and Polyergus (Hymenoptera:Formicidae) Ann Zool Fenn 39 267 271 (Pubitemid 35181393)
21. EJ Hollox J Al Armour 2008 Directional and balancing selection in human beta-defensins BMC Evol Biol 8 113
22. AL Hughes M Nei 1988 Pattern of nucleotide substitution at major histocompatibility complex class I loci reveals overdominant selection Nature 335 167 170 (Pubitemid 18234851)
23. AL Hughes M Yeager 1997 Coordinated amino acid changes in the evolution of mammalian defensins J Mol Evol 44 675 682 (Pubitemid 27240861)
24. AL Hughes MK Hughes CY Howell M Nei 1994 Natural selection at the class II major histocompatibility complex loci of mammals Philos Trans R Soc Lond B 346 359 367
25. WOH Hughes JJ Boomsma 2004 Genetic diversity and disease resistance in leaf-cutting ant societies Evolution 58 1251 1260 (Pubitemid 38826278)
26. FM Jiggins K-W Kim 2005 The evolution of antifungal peptides in Drosophila Genetics 171 1847 1859
27. FM Jiggins K-W Kim 2007 A screen for immunity genes evolving under positive selection in Drosophila J Evol Biol 20 965 970 (Pubitemid 46663119)
28. RN Johnson P-M Agapow RH Crozier 2003 A tree island approach to inferring phylogeny in the ant subfamily Formicinae, with especial reference to the evolution of weaving Mol Phylogenet Evol 29 317 330 (Pubitemid 38370220)
29. J Klaudiny A Štefan K Bachanová J Kopernický J Šimúth 2005 Two structurally different defensin genes, one of them encoding a novel defensin isoform, are expressed in honeybee Apis mellifera Insect Biochem Mol 35 11 22 (Pubitemid 40015507)
30. SL Kosakovsky Pond SDW Frost 2005 Datamonkey:rapid detection of selective pressure on individual sites of codon alignments Bioinformatics 21 2531 2533 (Pubitemid 40731616)
31. SL Kosakovsky Pond SDW Frost 2005 Not so different after all: a comparison of methods for detecting amino acid sites under selection Mol Biol Evol 22 1208 1222 (Pubitemid 40577758)
32. SL Kosakovsky Pond SV Muse 2005 Site-to-site variation of synonymous substitution rates Mol Biol Evol 22 2375 2385 (Pubitemid 41661376)
33. SL Kosakovsky Pond SDW Frost SV Muse 2005 HyPhy: hypothesis testing using phylogenies Bioinformatics 25 676 679 (Pubitemid 40424796)
34. S Kumar K Tamura M Nei 2004 MEGA3: integrated software for Molecular Evolutionary Genetics Analysis and sequence alignment Brief Bioinform 5 150 163
35. BP Lazzaro AG Clark 2003 Molecular population genetics of inducible antibacterial peptide genes in Drosophila melanogaster Mol Biol Evol 20 914 923 (Pubitemid 36578718)
36. W-H Li 1993 Unbiased estimation of the rates of synonymous and nonsynonymous substitution J Mol Evol 36 96 99 (Pubitemid 23018099)
37. S Liersch P Schmid-Hempel 1998 Genetic variation within social insect colonies reduces parasite load Proc R Soc London B 265 221 225 (Pubitemid 28064453)
38. K Luenser A Ludwig 2005 Variability and evolution of bovine β-defensin genes Genes Immun 6 115 122 (Pubitemid 40439536)
39. DJ Lynn AT Lloyd MA Fares C O'Farrelly 2004 Evidence of positively selected sites in mammalian α-defensins Mol Biol Evol 21 819 827 (Pubitemid 38529724)
40. R Maget-Dana M Ptak 1997 Penetration of the insect defensin A into phospholipid monolayers and formation of defensin A-lipid complexes Biophys J 73 2527 2533 (Pubitemid 27471461)
41. JH [tmp] McDonald M Kreitman 1991 Adaptive protein evolution at the Adh locus in Drosophila Nature 351 652 654 (Pubitemid 21896661)
42. CS Moreau CD Bell R Vila B Archibald NE Pierce 2006 Phylogeny of the ants:Diversification in the age of angiosperms Science 312 101 104
43. GM Morrison CAM Semple FM Kilanowski RE Hill JR Dorin 2003 Signal sequence conservation and mature peptide divergence within subgroups of the murine β-defensin gene family Mol Biol Evol 20 460 470 (Pubitemid 36427181)
44. SV Muse BS Gaut 1994 A likelihood approach for comparing synonymous and nonsynonymous substitution rates, with application to the chloroplast genome Mol Biol Evol 11 715 724 (Pubitemid 24274880)
45. Nicholas KB, Nicholas HB (1997) GeneDoc: a tool for editing and annotating multiple sequence alignments. Distributed by the authors
46. R Nielsen Z Yang 1998 Likelihood models for detecting positively selected amino acid sites and applications to the HIV-1 envelope gene Genetics 148 929 936 (Pubitemid 28169008)
47. Nylander JAA (2004) MrModeltest 2.2. Program distributed by the author. Evolutionary Biology Centre. Uppsala University, Uppsala, Sweden
48. KA Palmer BP Oldroyd 2003 Evidence for intra-colonial genetic variance in resistance to American foulbrood of honey bees (Apis mellifera): further support for the parasite/pathogen hypothesis for the evolution of polyandry Naturwissenschaften 90 265 268 (Pubitemid 36819271)
49. P Pamilo NO Bianchi 1993 Evolution of the Zfx and Zfy genes: rates and interdependence between the genes Mol Biol Evol 10 271 281
50. A Parmakelis MA Slotman JC Marshall PH Awono-Ambene C Antonio-Nkondjio F Simard A Caccone JR Powell 2008 The molecular evolution of four anti-malarial immune genes in the Anopheles gambiae species complex BMC Evol Biol 8 79
51. A Patil AL Hughes G Zhang 2004 Rapid evolution and diversification of mammalian α-defensins as revealed by comparative analysis of rodent and primate genes Physiol Genomics 20 1 11
52. P Rice I Longden A Bleasby 2000 EMBOSS: the European Molecular Biology Open Software Suite Trends Genet 16 276 277
53. M Robinson-Rechavi D Huchon 2000 RRTree: relative-rate tests between groups of sequences on a phylogenetic tree Bioinformatics 16 296 297 (Pubitemid 30352860)
54. F Ronquist JP Huelsenbeck 2003 MrBayes 3:Bayesian phylogenetic inference under mixed models Bioinformatics 19 1572 1574 (Pubitemid 37038874)
55. WC Rothenbuhler 1964 Behavior genetics of nest cleaning in honey bees. IV. Responses of F1 and backcross generations to disease-killed brood Am Zool 4 111 123
56. J Rozas JC Sanchez-DelBarrio X Messeguer R Rozas 2003 DnaSP, DNA polymorphism analyses by the coalescent and other methods Bioinformatics 19 2496 2497 (Pubitemid 38016658)
57. TB Sackton BP Lazzarro TA Schlenke JD Evans D Hultmark AG Clark 2007 Dynamic evolution of the innate immune system in Drosophila Nature Genet 39 1461 1468 (Pubitemid 350191353)
58. TA Schlenke DJ Begun 2003 Natural selection drives Drosophila immune system evolution Genetics 164 1471 1480 (Pubitemid 37102209)
59. Schmid-Hempel P (1998) Parasites in social insects. Princeton University Press, Princeton, NJ
60. P Schmid-Hempel RH Crozier 1999 Polyandry versus polygyny versus parasites Philos Trans R Soc Lond B 354 507 515 (Pubitemid 29363325)
61. HA Schmidt K Strimmer M Vingron A von Haeseler 2002 TREE-PUZZLE:maximum likelihood phylogenetic analysis using quartets and parallel computing Bioinformatics 18 502 504 (Pubitemid 34284960)
62. TD Seeley DR Tarpy 2007 Queen promiscuity lowers disease within honeybee colonies Proc R Soc London B 274 67 72 (Pubitemid 47055497)
63. CAM Semple M Rolfe JR Dorin 2003 Duplication and selection in the evolution of primate β-defensin genes Genome Biol 4 R31
64. F Simard M Licht NJ Besansky T Lehmann 2007 Polymorphism at the defensin gene in the Anopheles gambiae complex:Testing different selection hypotheses Infect Genet Evol 7 285 292 (Pubitemid 46187503)
65. FM Steiner BC Schlick-Steiner S Schödl X Espadaler B Seifert E Christian C Stauffer 2004 Phylogeny and bionomics of Lasius austriacus (Hymenoptera, Formicidae) Insect Soc 51 24 29 (Pubitemid 38377557)
66. Swofford DL (2002) PAUP*. Phylogenetic Analysis Using Parsimony (*and other methods). Version 4. Sinauer Associates, Sunderland, MA
67. DR Tarpy 2003 Genetic diversity within honeybee colonies prevents severe infections and promotes colony growth Proc R Soc London B 270 99 103 (Pubitemid 36140428)
68. JD Thompson DG Higgins TJ Gibson 1994 Clustal-W-improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice Nucleic Acids Res 22 4673 4680 (Pubitemid 24354800)
69. J Trowsdale P Parham 2004 Defense strategies and immunity-related genes Eur J Immunol 34 7 17 (Pubitemid 38111515)
70. M Van Baalen M Beekman 2006 The costs and benefits of genetic heterogeneity in resistance against parasites in social insects Am Nat 167 568 577
71. L Viljakainen P Pamilo 2005 Identification and molecular characterization of defensin gene from the ant Formica aquilonia Insect Mol Biol 14 335 338 (Pubitemid 41577053)
72. Z Yang 2007 PAML 4: phylogenetic analysis by maximum likelihood Mol Biol Evol 24 1586 1591 (Pubitemid 47236688)
73. Z Yang R Nielsen N Goldman A-MK Pedersen 2000 Codon-substitution models for heterogeneous selection pressure at amino acid sites Genetics 155 431 449 (Pubitemid 30257141)
74. J Zhang HF Rosenberg M Nei 1998 Positive Darwinian selection after gene duplication in primate ribonuclease genes Proc Natl Acad Sci USA 95 3708 3713 (Pubitemid 28173193)