Contrasted evolutionary histories of two Toll-like receptors (Tlr4 and Tlr7) in wild rodents (MURINAE)

BMC Evolutionary Biology

Volumn 13, Issue 1, 2013, Pages

  Fornůsková, Alena ^a,b,c   Vinkler, Michal ^d   Pagès, Marie ^c,e   Galan, Maxime ^c   Jousselin, Emmanuelle ^c   Cerqueira, Frederique ^f   Morand, Serge ^c,g,h   Charbonnel, Nathalie ^c   Bryja, Josef ^a,b   Cosson, Jean François ^c  

^a INSTITUTE OF VERTEBRATE BIOLOGY   (Czech Republic)

^b MASARYK UNIVERSITY   (Czech Republic)

^c INSTITUT DE RECHERCHE POUR LE DÉVELOPPEMENT   (France)

^d CHARLES UNIVERSITY   (Czech Republic)

^e UNIVERSITY OF LIÈGE   (Belgium)

^f UNIV MONTPELLIER   (France)

^g INSTITUT DES SCIENCES DE L EVOLUTION   (France)

^h CIRAD   (France)

Author keywords

Adaptive evolution; Arms race; Host pathogen interaction; Pathogen Associated Molecular Pattern (PAMP); Pattern recognition receptors

Indexed keywords

DATA SET; GENE EXPRESSION; HOST-PATHOGEN INTERACTION; IMMUNITY; MOLECULAR ANALYSIS; NUCLEIC ACID; PATHOGEN; PHYLOGENY; POLYSACCHARIDE; PROTEIN; PURIFICATION; RODENT; WILD POPULATION;

BACTERIA (MICROORGANISMS); MURINAE; NEGIBACTERIA; RODENTIA; VERTEBRATA;

TOLL LIKE RECEPTOR 4; TOLL LIKE RECEPTOR 7;

ANIMAL; ARTICLE; CHEMISTRY; CLASSIFICATION; GENETICS; IMMUNOLOGY; INNATE IMMUNITY; MOLECULAR EVOLUTION; MURINAE; PHYLOGENY; PROTEIN TERTIARY STRUCTURE; SPECIES DIFFERENCE;

ANIMALS; EVOLUTION, MOLECULAR; IMMUNITY, INNATE; MURINAE; PHYLOGENY; PROTEIN STRUCTURE, TERTIARY; SPECIES SPECIFICITY; TOLL-LIKE RECEPTOR 4; TOLL-LIKE RECEPTOR 7;

EID: 84883732182     PISSN: None     EISSN: 14712148     Source Type: Journal    
DOI: 10.1186/1471-2148-13-194     Document Type: Article

References (115)

1. Systems biology of innate immunity. Zak DE, Aderem A, Immunol Rev 2009 227 264 282
2. From evolutionary genetics to human immunology: how selection shapes host defence genes. Barreiro LB, Quintana-Murci L, Nat Rev Genet 2010 11 17 30
3. Pathogen recognition and innate immunity. Akira S, Uematsu S, Takeuchi O, Cell 2006 124 783 801 (Pubitemid 43261452)
4. Single nucleotide polymorphisms of Toll-like receptors and susceptibility to infectious disease. Schröder NWJ, Schumann RR, Lancet Infect Dis 2005 5 156 164 (Pubitemid 40568671)
5. Immunobiology of Toll-like receptors: emerging trends. Pandey S, Agrawal DK, Immunol Cell Biol 2006 84 333 341 (Pubitemid 43882838)
6. Innate immunogenetics: a tool for exploring new frontiers of host defence. Bochud P-Y, Bochud M, Telenti A, Calandra T, Lancet Infect Dis 2007 7 531 542 (Pubitemid 47077714)
7. Immune signaling by RIG-I-like receptors. Loo Y-M, Gale M Jr, Immunity 2011 34 680 692
8. Genetic variation in Toll-like receptors and disease susceptibility. Netea MG, Wijmenga C, O'Neill LAJ, Nat Immunol 2012 13 535 542
9. Adaptation and constraint at Toll-like receptors in primates. Wlasiuk G, Nachman MW, Mol Biol Evol 2010 27 2172 2186
10. Molecular evolution of the Toll-like receptor multigene family in birds. Alcaide M, Edwards SV, Mol Biol Evol 2011 28 1703 1715
11. Signatures of selection acting on the innate immunity gene Toll-like receptor 2 (TLR2) during the evolutionary history of rodents. Tschirren B, Råberg L, Westerdahl H, J Evol Biol 2011 24 1232 1240
12. Variation at innate immunity Toll-like receptor genes in a bottlenecked population of a New Zealand robin. Grueber CE, Wallis GP, King TM, Jamieson IG, PLoS ONE 2012 7 45011
13. Contrasting patterns of diversity and population differentiation at the innate immunity gene Toll-like receptor 2 (TLR2) in two sympatric rodent species. Tschirren B, Andersson M, Scherman K, Westerdahl H, Råberg L, Evolution 2012 66 720 731
14. Polymorphisms at the innate immune receptor TLR2 are associated with Borrelia infection in a wild rodent population. Tschirren B, Andersson M, Scherman K, Westerdahl H, Mittl PRE, Råberg L, Proc Biol Sci 2013 280 20130364
15. Malaria: disease and evolution. Haldane JBS, Genetic and Evolutionary Aspects Boston: Kluwer Academic Publishers 2006 175 187
16. The nature of selection on the major histocompatibility complex. Apanius V, Penn D, Slev PR, Ruff LR, Potts WK, Crit Rev Immunol 1997 17 179 224 (Pubitemid 27161351)
17. MHC studies in nonmodel vertebrates: what have we learned about natural selection in 15 years? Bernatchez L, Landry C, J Evol Biol 2003 16 363 377 (Pubitemid 36567968)
18. High MHC diversity maintained by balancing selection in an otherwise genetically monomorphic mammal. Aguilar A, Roemer G, Debenham S, Binns M, Garcelon D, Wayne RK, Proc Natl Acad Sci USA 2004 101 3490 3494 (Pubitemid 38338222)
19. Duplication, balancing selection and trans-species evolution explain the high levels of polymorphism of the DQA MHC class II gene in voles (Arvicolinae). Bryja J, Galan M, Charbonnel N, Cosson JF, Immunogenetics 2006 58 191 202
20. The evolutionary ecology of the major histocompatibility complex. Piertney SB, Oliver MK, Heredity (Edinb) 2006 96 7 21
21. How pathogens drive genetic diversity: MHC, mechanisms and misunderstandings. Spurgin LG, Richardson DS, Proc Biol Sci 2010 277 979 988
22. Genetic structure and contrasting selection pattern at two major histocompatibility complex genes in wild house mouse populations. Cížková D, Gouy de Bellocq J, Baird SJE, Piálek J, Bryja J, Heredity (Edinb) 2011 106 727 740
23. Pathogen-mediated selection for MHC variability in wild zebrafish. Smith C, Ondračková M, Spence R, Adams S, Betts DS, Mallon E, Evol Ecol Res 2011 67 217 218
24. A human homologue of the Drosophila Toll protein signals activation of adaptive immunity. Medzhitov R, Preston-Hurlburt P, Janeway CA Jr, Nature 1997 388 394 397 (Pubitemid 27334820)
25. The acquired immune system: a vantage from beneath. Hedrick SM, Immunity 2004 21 607 615 (Pubitemid 39487886)
26. TLRs: Professor Mechnikov, sit on your hat. O'Neill LAJ, Trends Immunol 2004 25 687 693 (Pubitemid 39457983)
27. Introduction. Bassett EH, Rich T, Toll and Toll-Like Receptors: An Immunologic Perspective Boston, MA: Springer US 2005 1 17
28. Is MHC enough for understanding wildlife immunogenetics? Acevedo-Whitehouse K, Cunningham AA, Trends Ecol Evol (Amst) 2006 21 433 438 (Pubitemid 44066618)
29. Evolutionary dynamics of human Toll-like receptors and their different contributions to host defense. Barreiro LB, Ben-Ali M, Quach H, Laval G, Patin E, Pickrell JK, Bouchier C, Tichit M, Neyrolles O, Gicquel B, Kidd JR, Kidd KK, Alcaïs A, Ragimbeau J, Pellegrini S, Abel L, Casanova J-L, Quintana-Murci L, PLoS Genet 2009 5 1000562
30. The question waiting to be asked: innate immunity receptors in the perspective of zoological research. Vinkler M, Albrecht T, Folia Zool 2009 58 15 28
31. Role of Toll-like receptors in pathogen recognition. Janssens S, Beyaert R, Clin Microbiol Rev 2003 16 637 646 (Pubitemid 37296552)
32. The evolution of vertebrate Toll-like receptors. Roach JC, Glusman G, Rowen L, Kaur A, Purcell MK, Smith KD, Hood LE, Aderem A, Proc Natl Acad Sci USA 2005 102 9577 9582 (Pubitemid 40981723)
33. Functional diversification of the toll-like receptor gene family. Hughes AL, Piontkivska H, Immunogenetics 2008 60 249 256
34. Toll-like receptors-taking an evolutionary approach. Leulier F, Lemaitre B, Nat Rev Genet 2008 9 165 178
35. Evolution of the chicken Toll-like receptor gene family: a story of gene gain and gene loss. Temperley ND, Berlin S, Paton IR, Griffin DK, Burt DW, BMC Genomics 2008 9 62
36. Molecular evolution of the vertebrate TLR1 gene family-a complex history of gene duplication, gene conversion, positive selection and co-evolution. Huang Y, Temperley ND, Ren L, Smith J, Li N, Burt DW, BMC Evol Biol 2011 11 149
37. Variation matters: TLR structure and species-specific pathogen recognition. Werling D, Jann OC, Offord V, Glass EJ, Coffey TJ, Trends Immunol 2009 30 124 130
38. Genome bioinformatic analysis of nonsynonymous SNPs. Burke DF, Worth CL, Priego E-M, Cheng T, Smink LJ, Todd JA, Blundell TL, BMC Bioinforma 2007 8 301
39. The structural basis of lipopolysaccharide recognition by the TLR4-MD-2 complex. Park BS, Song DH, Kim HM, Choi B-S, Lee H, Lee J-O, Nature 2009 458 1191 1195
40. Unique properties of the chicken TLR4/MD-2 complex: selective lipopolysaccharide activation of the MyD88-dependent pathway. Keestra AM, van Putten JPM, J Immunol 2008 181 4354 4362
41. Elucidation of the MD-2/TLR4 interface required for signaling by lipid IVa. Walsh C, Gangloff M, Monie T, Smyth T, Wei B, McKinley TJ, Maskell D, Gay N, Bryant C, J Immunol 2008 181 1245 1254
42. Characterization of bovine Toll-like receptor 8: ligand specificity, signaling essential sites and dimerization. Zhu J, Brownlie R, Liu Q, Babiuk LA, Potter A, Mutwiri GK, Mol Immunol 2009 46 978 990
43. The structural biology of Toll-like receptors. Botos I, Segal DM, Davies DR, Structure 2011 19 447 459
44. Structural biology of the Toll-like receptor family. Kang JY, Lee J-O, Annu Rev Biochem 2011 80 917 941
45. Toll pathway-dependent blockade of CD4+CD25+ T cell-mediated suppression by dendritic cells. Pasare C, Medzhitov R, Science 2003 299 1033 1036 (Pubitemid 36222922)
46. Translational mini-review series on Toll-like receptors: networks regulated by Toll-like receptors mediate innate and adaptive immunity. Parker LC, Prince LR, Sabroe I, Clin Exp Immunol 2007 147 199 207 (Pubitemid 46095996)
47. The role of pattern-recognition receptors in innate immunity: update on Toll-like receptors. Kawai T, Akira S, Nat Immunol 2010 11 373 384
48. Toll-like receptors and acquired immunity. Pasare C, Medzhitov R, Semin Immunol 2004 16 23 26 (Pubitemid 38147430)
49. Nucleotide-binding oligomerization domain-2 modulates specific TLR pathways for the induction of cytokine release. Netea MG, Ferwerda G, de Jong DJ, Jansen T, Jacobs L, Kramer M, Naber THJ, Drenth JPH, Girardin SE, Kullberg BJ, Adema GJ, Van der Meer JWM, J Immunol 2005 174 6518 6523 (Pubitemid 40663847)
50. Phylogenetic variation and polymorphism at the Toll-like receptor 4 locus (TLR4). Smirnova I, Poltorak A, Chan EK, McBride C, Beutler B, Genome Biol 2000 1 002.1 002.10
51. TLR4 polymorphisms, infectious diseases, and evolutionary pressure during migration of modern humans. Ferwerda B, McCall MBB, Alonso S, Giamarellos-Bourboulis EJ, Mouktaroudi M, Izagirre N, Syafruddin D, Kibiki G, Cristea T, Hijmans A, Hamann L, Israel S, ElGhazali G, Troye-Blomberg M, Kumpf O, Maiga B, Dolo A, Doumbo O, Hermsen CC, Stalenhoef AFH, van Crevel R, Brunner HG, Oh D-Y, Schumann RR, de la Rúa C, Sauerwein R, Kullberg B-J, van der Ven AJAM, van der Meer JWM, Netea MG, Proc Natl Acad Sci USA 2007 104 16645 16650 (Pubitemid 350211070)
52. Identification of the first Toll-like receptor gene in passerine birds: TLR4 orthologue in zebra finch (Taeniopygia guttata). Vinkler M, Bryjová A, Albrecht T, Bryja J, Tissue Antigens 2009 74 32 41
53. Toll-like receptors 7, 8, and 9: linking innate immunity to autoimmunity. Krieg AM, Vollmer J, Immunol Rev 2007 220 251 269 (Pubitemid 350045572)
54. Development of TLR inhibitors for the treatment of autoimmune diseases. Barrat FJ, Coffman RL, Immunol Rev 2008 223 271 283 (Pubitemid 351986175)
55. The role of innate immune responses in autoimmune disease development. Waldner H, Autoimmun Rev 2009 8 400 404
56. Molecular evolution of vertebrate Toll-like receptors: evolutionary rate difference between their leucine-rich repeats and their TIR domains. Mikami T, Miyashita H, Takatsuka S, Kuroki Y, Matsushima N, Gene 2012 503 235 243
57. Point, counterpoint: the evolution of pathogenic viruses and their human hosts. Worobey M, Bjork A, Wertheim JO, Annu Rev Ecol Evol Syst 2007 38 515 540
58. Defective LPS signaling in C3H/HeJ and C57BL/10ScCr mice: mutations in Tlr4 gene. Poltorak A, He X, Smirnova I, Liu MY, Van Huffel C, Du X, Birdwell D, Alejos E, Silva M, Galanos C, Freudenberg M, Ricciardi-Castagnoli P, Layton B, Beutler B, Science 1998 282 2085 2088 (Pubitemid 29001265)
59. Reis e Sousa C: Innate antiviral responses by means of TLR7-mediated recognition of single-stranded RNA. Diebold SS, Kaisho T, Hemmi H, Akira S, Science 2004 303 1529 1531 (Pubitemid 38314425)
60. Species-specific recognition of single-stranded RNA via Toll-like receptor 7 and 8. Heil F, Hemmi H, Hochrein H, Ampenberger F, Kirschning C, Akira S, Lipford G, Wagner H, Bauer S, Science 2004 303 1526 1529 (Pubitemid 38314424)
61. Global trends in emerging infectious diseases. Jones KE, Patel NG, Levy MA, Storeygard A, Balk D, Gittleman JL, Daszak P, Nature 2008 451 990 993 (Pubitemid 351301726)
62. Biodiversity loss and emerging infectious disease: an example from the rodent-borne hemorrhagic fevers. Mills JN, Biodiversity 2006 7 9 17
63. A comparison of bats and rodents as reservoirs of zoonotic viruses: are bats special? Luis AD, Hayman DTS, O'Shea TJ, Cryan PM, Gilbert AT, Pulliam JRC, Mills JN, Timonin ME, Willis CKR, Cunningham AA, Fooks AR, Rupprecht CE, Wood JLN, Webb CT, Proc Biol Sci 2013 280 20122753
64. Evolution of the TIR domain-containing adaptors in humans: swinging between constraint and adaptation. Fornarino S, Laval G, Barreiro LB, Manry J, Vasseur E, Quintana-Murci L, Mol Biol Evol 2011 28 3087 3097
65. Comparative analysis of species-specific ligand recognition in Toll-like receptor 8 signaling: a hypothesis. Govindaraj RG, Manavalan B, Basith S, Choi S, PLoS ONE 2011 6 25118
66. Datamonkey: rapid detection of selective pressure on individual sites of codon alignments. Pond SLK, Frost SDW, Bioinformatics 2005 21 2531 2533 (Pubitemid 40731616)
67. Kosakovsky Pond SL: Detecting individual sites subject to episodic diversifying selection. Murrell B, Wertheim JO, Moola S, Weighill T, Scheffler K, PLoS Genet 2012 8 1002764
68. Homology modeling of human Toll-like receptors TLR7, 8, and 9 ligand-binding domains. Wei T, Gong J, Jamitzky F, Heckl WM, Stark RW, Rössle SC, Protein Sci 2009 18 1684 1691
69. Revisiting the taxonomy of the Rattini tribe: a phylogeny-based delimitation of species boundaries. Pagès M, Chaval Y, Herbreteau V, Waengsothorn S, Cosson J-F, Hugot J-P, Morand S, Michaux J, BMC Evol Biol 2010 10 184
70. Multiple geographic origins of commensalism and complex dispersal history of Black Rats. Aplin KP, Suzuki H, Chinen AA, Chesser RT, Ten Have J, Donnellan SC, Austin J, Frost A, Gonzalez JP, Herbreteau V, Catzeflis F, Soubrier J, Fang Y-P, Robins J, Matisoo-Smith E, Bastos ADS, Maryanto I, Sinaga MH, Denys C, Van Den Bussche RA, Conroy C, Rowe K, Cooper A, PLoS ONE 2011 6 26357
71. Inferring phylogenies from mtDNA variation: mitochondrial-gene trees versus nuclear-gene trees. Moore WS, Evolution 1995 49 718 726
72. Incomplete lineage sorting patterns among human, chimpanzee, and orangutan suggest recent orangutan speciation and widespread selection. Hobolth A, Dutheil JY, Hawks J, Schierup MH, Mailund T, Genome Res 2011 21 349 356
73. Cytonuclear discordance among Southeast Asian black rats (Rattus rattus complex). Pagès M, Bazin E, Galan M, Chaval Y, Claude J, Herbreteau V, Michaux J, Piry S, Morand S, Cosson J-F, Mol Ecol 2013 22 1019 1034
74. Invasion facilitates hybridization with introgression in the Rattus rattus species complex. Lack JB, Greene DU, Conroy CJ, Hamilton MJ, Braun JK, Mares MA, Van Den Bussche RA, Mol Ecol 2012 21 3545 3561
75. Gene trees and species trees are not the same. Nichols R, Trends Ecol Evol 2001 16 358 364 (Pubitemid 32525776)
76. Natural selection and phylogenetic analysis. Edwards SV, PNAS 2009 106 8799 8800
77. Signatures of positive selection in Toll-like receptor (TLR) genes in mammals. Areal H, Abrantes J, Esteves PJ, BMC Evol Biol 2011 11 368
78. Adaptive evolution of Toll-like receptor 5 in domesticated mammals. Smith SA, Jann OC, Haig D, Russell GC, Werling D, Glass EJ, Emes RD, BMC Evol Biol 2012 12 122
79. The differential evolutionary dynamics of avian cytokine and TLR gene classes. Downing T, Lloyd AT, O'Farrelly C, Bradley DG, J Immunol 2010 184 6993 7000
80. Crystal structure of the TLR4-MD-2 complex with bound endotoxin antagonist Eritoran. Kim HM, Park BS, Kim J-I, Kim SE, Lee J, Oh SC, Enkhbayar P, Matsushima N, Lee H, Yoo OJ, Lee J-O, Cell 2007 130 906 917 (Pubitemid 47332573)
81. Essential roles of hydrophobic residues in both MD-2 and Toll-like receptor 4 in activation by endotoxin. Resman N, Vasl J, Oblak A, Pristovsek P, Gioannini TL, Weiss JP, Jerala R, J Biol Chem 2009 284 15052 15060
82. Structural basis of species-specific endotoxin sensing by innate immune receptor TLR4/MD-2. Ohto U, Fukase K, Miyake K, Shimizu T, Proc Natl Acad Sci USA 2012 109 7421 7426
83. Lipopolysaccharide endotoxins. Raetz CRH, Whitfield C, Annu Rev Biochem 2002 71 635 700 (Pubitemid 34800232)
84. Phase and antigenic variation in bacteria. van der Woude MW, Bäumler AJ, Clin Microbiol Rev 2004 17 581 611 (Pubitemid 38970684)
85. Evasion of Toll-like receptor 5 by flagellated bacteria. Andersen-Nissen E, Smith KD, Strobe KL, Barrett SLR, Cookson BT, Logan SM, Aderem A, Proc Natl Acad Sci USA 2005 102 9247 9252 (Pubitemid 40923549)
86. Within-species flagellin polymorphism in Xanthomonas campestris pv campestris and its impact on elicitation of Arabidopsis flagellin sensinG2-dependent defenses. Sun W, Dunning FM, Pfund C, Weingarten R, Bent AF, Plant Cell 2006 18 764 779 (Pubitemid 43956176)
87. Recognition of lipid A variants by the TLR4-MD-2 receptor complex. Maeshima N, Fernandez RC, Front Cell Infect Microbiol 2013 3 doi:10.3389/fcimb.2013.00003
88. Zwickl DJ, Genetic algorithm approaches for the phylogenetic analysis of large biological sequence datasets under the maximum likelihood criterion The University of Texas at Austin. 2006 Ph.D. dissertation
89. The effect of deleterious mutations on neutral molecular variation. Charlesworth B, Morgan MT, Charlesworth D, Genetics 1993 134 1289 1303 (Pubitemid 23220050)
90. Nucleotide variation in wild and inbred mice. Salcedo T, Geraldes A, Nachman MW, Genetics 2007 177 2277 2291
91. Phylogeny and biogeography of African Murinae based on mitochondrial and nuclear gene sequences, with a new tribal classification of the subfamily. Lecompte E, Aplin K, Denys C, Catzeflis F, Chades M, Chevret P, BMC Evol Biol 2008 8 199
92. Next-generation sequencing for rodent barcoding: species identification from fresh, degraded and environmental samples. Galan M, Pagès M, Cosson J-F, PLoS ONE 2012 7 48374
93. Primer3 on the WWW for general users and for biologist programmers. Rozen S, Skaletsky H, Methods Mol Biol 2000 132 365 386
94. A Comparison of bayesian methods for haplotype reconstruction from population genotype data. Stephens M, Donnelly P, Am J Hum Genet 2003 73 1162 1169 (Pubitemid 37414228)
95. DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Librado P, Rozas J, Bioinformatics 2009 25 1451 1452
96. FaBox: an online toolbox for fasta sequences. Villesen P, Mol Ecol Notes 2007 7 965 968 (Pubitemid 350059223)
97. SMART, a simple modular architecture research tool: identification of signaling domains. Schultz J, Milpetz F, Bork P, Ponting CP, Proc Natl Acad Sci USA 1998 95 5857 5864 (Pubitemid 28248931)
98. Protein structure prediction on the Web: a case study using the Phyre server. Kelley LA, Sternberg MJE, Nat Protoc 2009 4 363 371
99. Datamonkey 2010: a suite of phylogenetic analysis tools for evolutionary biology. Delport W, Poon AFY, Frost SDW, Kosakovsky Pond SL, Bioinformatics 2010 26 2455 2457
100. Automated phylogenetic detection of recombination using a genetic algorithm. Pond SLK, Posada D, Gravenor MB, Woelk CH, Frost SDW, Mol Biol Evol 2006 23 1891 1901 (Pubitemid 44412875)
101. GARD: a genetic algorithm for recombination detection. Pond SLK, Posada D, Gravenor MB, Woelk CH, Frost SDW, Bioinformatics 2006 22 3096 3098 (Pubitemid 44884087)
102. jModelTest: phylogenetic model averaging. Posada D, Mol Biol Evol 2008 25 1253 1256 (Pubitemid 351882013)
103. A rapid bootstrap algorithm for the RAxML web servers. Stamatakis A, Hoover P, Rougemont J, Syst Biol 2008 57 758 771
104. MRBAYES: Bayesian inference of phylogenetic trees. Huelsenbeck JP, Ronquist F, Bioinformatics 2001 17 754 755 (Pubitemid 32851390)
105. AIR: a batch-oriented web program package for construction of supermatrices ready for phylogenomic analyses. Kumar S, Skjaeveland A, Orr RJS, Enger P, Ruden T, Mevik B-H, Burki F, Botnen A, Shalchian-Tabrizi K, BMC Bioinforma 2009 10 357
106. Rambaut A, Drummond AJ, Tracer v1.4 2007 Available from http://beast.bio.ed.ac.uk/Tracer
107. Rambaut A, FigTree v1.3.1 2006-2009 2009 Available with the program package at http://tree.bio.ed.ac.uk/software/figtree
108. Jane: a new tool for the cophylogeny reconstruction problem. Conow C, Fielder D, Ovadia Y, Libeskind-Hadas R, Algorithms Mol Biol 2010 5 16
109. An extreme case of plant-insect codiversification: figs and fig-pollinating wasps. Cruaud A, Rønsted N, Chantarasuwan B, Chou LS, Clement WL, Couloux A, Cousins B, Genson G, Harrison RD, Hanson PE, Hossaert-McKey M, Jabbour-Zahab R, Jousselin E, Kerdelhué C, Kjellberg F, Lopez-Vaamonde C, Peebles J, Peng Y-Q, Pereira RAS, Schramm T, Ubaidillah R, van Noort S, Weiblen GD, Yang D-R, Yodpinyanee A, Libeskind-Hadas R, Cook JM, Rasplus J-Y, Savolainen V, Syst Biol 2012 61 1029 1047
110. Multiple comparisons of log-likelihoods with applications to phylogenetic inference. Shimodaira H, Hasegawa M, Mol Biol Evol 1999 16 1114 1116 (Pubitemid 29368141)
111. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S, Mol Biol Evol 2011 28 2731 2739
112. ConSurf 2010: calculating evolutionary conservation in sequence and structure of proteins and nucleic acids. Ashkenazy H, Erez E, Martz E, Pupko T, Ben-Tal N, Nucleic Acids Res 2010 38 529 533
113. Searching protein structure databases with DaliLite v.3. Holm L, Kääriäinen S, Rosenström P, Schenkel A, Bioinformatics 2008 24 2780 2781 (Pubitemid 352722625)
114. How well do evolutionary trees describe genetic relationships among populations? Kalinowski ST, Heredity (Edinb) 2009 102 506 513
115. LRRfinder: a web application for the identification of leucine-rich repeats and an integrative Toll-like receptor database. Offord V, Coffey TJ, Werling D, Dev Comp Immunol 2010 34 1035 1041