Whole-genome sequencing of drugresistant Salmonella enterica isolates from dairy cattle and humans in New York and Washington States reveals source and geographic associations

Applied and Environmental Microbiology

Volumn 83, Issue 12, 2017, Pages

  Carroll, Laura M ^a   Wiedmann, Martin ^a   den Bakker, Henk ^b   Siler, Julie ^a   Warchocki, Steven ^a   Kent, David ^a   Lyalina, Svetlana ^c   Davis, Margaret ^d   Sischo, William ^d   Besser, Thomas ^d   Warnick, Lorin D ^a   Pereira, Richard V ^e  

^a Cornell University ^*  (United States)

^b TEXAS TECH UNIVERSITY   (United States)

^c GLADSTONE INSTITUTES   (United States)

^d WASHINGTON STATE UNIVERSITY   (United States)

^e UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Dairy cattle; Drug resistance evolution; Genomics; Nontyphoidal Salmonella; Whole genome sequencing; Zoonosis

Indexed keywords

ANIMALS; DRUG THERAPY; GENES; HEALTH RISKS;

DAIRY CATTLES; DRUG RESISTANCE; GENOMICS; WHOLE GENOME SEQUENCING; ZOONOSIS;

SALMONELLA;

ANTIBIOTIC RESISTANCE; BACTERIUM; CATTLE; DRUG RESISTANCE; GENETIC ANALYSIS; GENOME; GENOMICS; ISOLATED POPULATION; PLASMID;

NEW YORK [UNITED STATES]; UNITED STATES; WASHINGTON [UNITED STATES];

ANIMALIA; BOS; SALMONELLA; SALMONELLA ENTERICA; SALMONELLA TYPHIMURIUM;

ANTIINFECTIVE AGENT;

ANIMAL; ANIMAL SALMONELLOSIS; BACTERIAL GENOME; BOVINE; CATTLE DISEASE; CLASSIFICATION; DNA SEQUENCE; DRUG EFFECTS; GENETICS; GENOTYPE; ISOLATION AND PURIFICATION; MICROBIAL SENSITIVITY TEST; MICROBIOLOGY; MULTIDRUG RESISTANCE; NEW YORK; SALMONELLA ENTERICA; SALMONELLOSIS; WASHINGTON;

ANIMALS; ANTI-BACTERIAL AGENTS; CATTLE; CATTLE DISEASES; DRUG RESISTANCE, MULTIPLE, BACTERIAL; GENOME, BACTERIAL; GENOTYPE; MICROBIAL SENSITIVITY TESTS; NEW YORK; SALMONELLA ENTERICA; SALMONELLA INFECTIONS; SALMONELLA INFECTIONS, ANIMAL; SEQUENCE ANALYSIS, DNA; WASHINGTON;

EID: 85020009023     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.00140-17     Document Type: Article

References (81)

1. Scallan E, Hoekstra RM, Angulo FJ, Tauxe RV, Widdowson MA, Roy SL, Jones JL, Griffin PM. 2011. Foodborne illness acquired in the United States-major pathogens. Emerg Infect Dis 17:7-15. https://doi.org/10.3201/eid1701.P11101
2. CDC. 2013. Antibiotic resistance threats in the United States, 2013. CDC, Atlanta, GA
3. WHO. 2014. Antimicrobial resistance: global report on surveillance. WHO, Geneva, Switzerland
4. Van Boeckel TP, Brower C, Gilbert M, Grenfell BT, Levin SA, Robinson TP, Teillant A, Laxminarayan R. 2015. Global trends in antimicrobial use in food animals. Proc Natl Acad Sci U S A 112:5649-5654. https://doi.org/10.1073/pnas.1503141112
5. Silbergeld EK, Graham J, Price LB. 2008. Industrial food animal production, antimicrobial resistance, and human health. Annu Rev Public Health 29:151-169. https://doi.org/10.1146/annurev.publhealth.29.020907.090904
6. Hendriksen SW, Orsel K, Wagenaar JA, Miko A, van Duijkeren E. 2004. Animal-to-human transmission of Salmonella Typhimurium DT104A variant. Emerg Infect Dis 10:2225-2227. https://doi.org/10.3201/eid1012.040286
7. Fey PD, Safranek TJ, Rupp ME, Dunne EF, Ribot E, Iwen PC, Bradford PA, Angulo FJ, Hinrichs SH. 2000. Ceftriaxone-resistant Salmonella infection acquired by a child from cattle. N Engl J Med 342:1242-1249. https://doi.org/10.1056/NEJM200004273421703
8. Hoelzer K, Moreno Switt AI, Wiedmann M. 2011. Animal contact as a source of human non-typhoidal salmonellosis. Vet Res 42:34. https://doi.org/10.1186/1297-9716-42-34
9. White DG, Zhao S, Sudler R, Ayers S, Friedman S, Chen S, McDermott PF, McDermott S, Wagner DD, Meng J. 2001. The isolation of antibioticresistant Salmonella from retail ground meats. N Engl J Med 345: 1147-1154. https://doi.org/10.1056/NEJMoa010315
10. Cody SH, Abbott SL, Marfin AA, Schulz B, Wagner P, Robbins K, Mohle-Boetani JC, Vugia DJ. 1999. Two outbreaks of multidrug-resistant Salmonella serotype Typhimurium DT104 infections linked to raw-milk cheese in Northern California. JAMA 281:1805-1810. https://doi.org/10.1001/jama.281.19.1805
11. Hald T, Aspinall W, Devleesschauwer B, Cooke R, Corrigan T, Havelaar AH, Gibb HJ, Torgerson PR, Kirk MD, Angulo FJ, Lake RJ, Speybroeck N, Hoffmann S. 2016. World Health Organization estimates of the relative contributions of food to the burden of disease due to selected foodborne hazards: a structured expert elicitation. PLoS One 11:e0145839. https://doi.org/10.1371/journal.pone.0145839
12. Johnson JR, Sannes MR, Croy C, Johnston B, Clabots C, Kuskowski MA, Bender J, Smith KE, Winokur PL, Belongia EA. 2007. Antimicrobial drugresistant Escherichia coli from humans and poultry products, Minnesota and Wisconsin, 2002-2004. Emerg Infect Dis 13:838-846. https://doi.org/10.3201/eid1306.061576
13. Price LB, Stegger M, Hasman H, Aziz M, Larsen J, Andersen PS, Pearson T, Waters AE, Foster JT, Schupp J, Gillece J, Driebe E, Liu CM, Springer B, Zdovc I, Battisti A, Franco A, Zmudzki J, Schwarz S, Butaye P, Jouy E, Pomba C, Porrero MC, Ruimy R, Smith TC, Robinson DA, Weese JS, Arriola CS, Yu F, Laurent F, Keim P, Skov R, Aarestrup FM. 2012. Staphylococcus aureus CC398: host adaptation and emergence of methicillin resistance in livestock. mBio 3(1):e00305-11. https://doi.org/10.1128/mBio.00305-11
14. Mather AE, Reid SW, Maskell DJ, Parkhill J, Fookes MC, Harris SR, Brown DJ, Coia JE, Mulvey MR, Gilmour MW, Petrovska L, de Pinna E, Kuroda M, Akiba M, Izumiya H, Connor TR, Suchard MA, Lemey P, Mellor DJ, Haydon DT, Thomson NR. 2013. Distinguishable epidemics of multidrug-resistant Salmonella Typhimurium DT104 in different hosts. Science 341: 1514-1517. https://doi.org/10.1126/science.1240578
15. Mather AE, Matthews L, Mellor DJ, Reeve R, Denwood MJ, Boerlin P, Reid-Smith RJ, Brown DJ, Coia JE, Browning LM, Haydon DT, Reid SW. 2012. An ecological approach to assessing the epidemiology of antimicrobial resistance in animal and human populations. Proc Biol Sci 279: 1630-1639. https://doi.org/10.1098/rspb.2011.1975
16. Kwong JC, Mercoulia K, Tomita T, Easton M, Li HY, Bulach DM, Stinear TP, Seemann T, Howden BP. 2016. Prospective whole-genome sequencing enhances national surveillance of Listeria monocytogenes. J Clin Microbiol 54:333-342. https://doi.org/10.1128/JCM.02344-15
17. Holmes A, Allison L, Ward M, Dallman TJ, Clark R, Fawkes A, Murphy L, Hanson M. 2015. Utility of whole-genome sequencing of Escherichia coli O157 for outbreak detection and epidemiological surveillance. J Clin Microbiol 53:3565-3573. https://doi.org/10.1128/JCM.01066-15
18. Taylor AJ, Lappi V, Wolfgang WJ, Lapierre P, Palumbo MJ, Medus C, Boxrud D. 2015. Characterization of foodborne outbreaks of Salmonella enterica serovar Enteritidis with whole-genome sequencing single nucleotide polymorphism-based analysis for surveillance and outbreak detection. J Clin Microbiol 53:3334-3340. https://doi.org/10.1128/JCM.01280-15
19. Fricke WF, Welch TJ, McDermott PF, Mammel MK, LeClerc JE, White DG, Cebula TA, Ravel J. 2009. Comparative genomics of the IncA/C multidrug resistance plasmid family. J Bacteriol 191:4750-4757. https://doi.org/10.1128/JB.00189-09
20. Cloeckaert A, Chaslus-Dancla E. 2001. Mechanisms of quinolone resistance in Salmonella. Vet Res 32:291-300. https://doi.org/10.1051/vetres:2001105
21. Andres P, Lucero C, Soler-Bistue A, Guerriero L, Albornoz E, Tran T, Zorreguieta A, PMQR Group, Galas M, Corso A, Tolmasky ME, Petroni A. 2013. Differential distribution of plasmid-mediated quinolone resistance genes in clinical enterobacteria with unusual phenotypes of quinolone susceptibility from Argentina. Antimicrob Agents Chemother 57: 2467-2475. https://doi.org/10.1128/AAC.01615-12
22. Hansen LH, Jensen LB, Sorensen HI, Sorensen SJ. 2007. Substrate specificity of the OqxAB multidrug resistance pump in Escherichia coli and selected enteric bacteria. J Antimicrob Chemother 60:145-147. https://doi.org/10.1093/jac/dkm167
23. WHO. 2015. WHO estimates of the global burden of foodborne diseases, 2007-2015. WHO, Geneva, Switzerland
24. Helms M, Ethelberg S, Molbak K, DT104 Study Group. 2005. International Salmonella Typhimurium DT104 infections, 1992-2001. Emerg Infect Dis 11:859-867. https://doi.org/10.3201/eid1106.041017
25. Leekitcharoenphon P, Hendriksen RS, Le Hello S, Weill FX, Baggesen DL, Jun SR, Ussery DW, Lund O, Crook DW, Wilson DJ, Aarestrup FM. 2016. Global genomic epidemiology of Salmonella enterica serovar Typhimurium DT104. Appl Environ Microbiol 82:2516-2526. https://doi.org/10.1128/AEM.03821-15
26. Ribot EM, Wierzba RK, Angulo FJ, Barrett TJ. 2002. Salmonella enterica serotype Typhimurium DT104 isolated from humans, United States, 1985, 1990, and 1995. Emerg Infect Dis 8:387-391. https://doi.org/10.3201/eid0804.010202
27. McDermott PF, Tyson GH, Kabera C, Chen Y, Li C, Folster JP, Ayers SL, Lam C, Tate HP, Zhao S. 2016. Whole-genome sequencing for detecting antimicrobial resistance in nontyphoidal Salmonella. Antimicrob Agents Chemother 60:5515-5520. https://doi.org/10.1128/AAC.01030-16
28. Zankari E, Hasman H, Kaas RS, Seyfarth AM, Agerso Y, Lund O, Larsen MV, Aarestrup FM. 2013. Genotyping using whole-genome sequencing is a realistic alternative to surveillance based on phenotypic antimicrobial susceptibility testing. J Antimicrob Chemother 68:771-777. https://doi.org/10.1093/jac/dks496
29. Gordon NC, Price JR, Cole K, Everitt R, Morgan M, Finney J, Kearns AM, Pichon B, Young B, Wilson DJ, Llewelyn MJ, Paul J, Peto TE, Crook DW, Walker AS, Golubchik T. 2014. Prediction of Staphylococcus aureus antimicrobial resistance by whole-genome sequencing. J Clin Microbiol 52:1182-1191. https://doi.org/10.1128/JCM.03117-13
30. Bradley P, Gordon NC, Walker TM, Dunn L, Heys S, Huang B, Earle S, Pankhurst LJ, Anson L, de Cesare M, Piazza P, Votintseva AA, Golubchik T, Wilson DJ, Wyllie DH, Diel R, Niemann S, Feuerriegel S, Kohl TA, Ismail N, Omar SV, Smith EG, Buck D, McVean G, Walker AS, Peto TE, Crook DW, Iqbal Z. 2015. Rapid antibiotic-resistance predictions from genome sequence data for Staphylococcus aureus and Mycobacterium tuberculosis. Nat Commun 6:10063. https://doi.org/10.1038/ncomms10063
31. Zhao S, Tyson GH, Chen Y, Li C, Mukherjee S, Young S, Lam C, Folster JP, Whichard JM, McDermott PF. 2016. Whole-genome sequencing analysis accurately predicts antimicrobial resistance phenotypes in Campylobacter spp. Appl Environ Microbiol 82:459-466. https://doi.org/10.1128/AEM.02873-15
32. Hooper DC, Jacoby GA. 2015. Mechanisms of drug resistance: quinolone resistance. Ann N Y Acad Sci 1354:12-31. https://doi.org/10.1111/nyas.12830
33. Gupta SK, Padmanabhan BR, Diene SM, Lopez-Rojas R, Kempf M, Landraud L, Rolain JM. 2014. ARG-ANNOT, a new bioinformatic tool to discover antibiotic resistance genes in bacterial genomes. Antimicrob Agents Chemother 58:212-220. https://doi.org/10.1128/AAC.01310-13
34. Jia B, Raphenya AR, Alcock B, Waglechner N, Guo P, Tsang KK, Lago BA, Dave BM, Pereira S, Sharma AN, Doshi S, Courtot M, Lo R, Williams LE, Frye JG, Elsayegh T, Sardar D, Westman EL, Pawlowski AC, Johnson TA, Brinkman FS, Wright GD, McArthur AG. 2017. CARD 2017: expansion and model-centric curation of the comprehensive antibiotic resistance database. Nucleic Acids Res 45(D1):D566-D573. https://doi.org/10.1093/nar/gkw1004
35. Davis MA, Besser TE, Orfe LH, Baker KN, Lanier AS, Broschat SL, New D, Call DR. 2011. Genotypic-phenotypic discrepancies between antibiotic resistance characteristics of Escherichia coli isolates from calves in management settings with high and low antibiotic use. Appl Environ Microbiol 77:3293-3299. https://doi.org/10.1128/AEM.02588-10
36. Folster JP, Tolar B, Pecic G, Sheehan D, Rickert R, Hise K, Zhao S, Fedorka-Cray PJ, McDermott P, Whichard JM. 2014. Characterization of blaCMY plasmids and their possible role in source attribution of Salmonella enterica serotype Typhimurium infections. Foodborne Pathog Dis 11:301-306. https://doi.org/10.1089/fpd.2013.1670
37. Madec JY, Doublet B, Ponsin C, Cloeckaert A, Haenni M. 2011. Extendedspectrum beta-lactamase blaCTX-M-1 gene carried on an IncI1 plasmid in multidrug-resistant Salmonella enterica serovar Typhimurium DT104 in cattle in France. J Antimicrob Chemother 66:942-944. https://doi.org/10.1093/jac/dkr014
38. Carattoli A, Zankari E, Garcia-Fernandez A, Voldby Larsen M, Lund O, Villa L, Moller Aarestrup F, Hasman H. 2014. In silico detection and typing of plasmids using PlasmidFinder and plasmid multilocus sequence typing. Antimicrob Agents Chemother 58:3895-3903. https://doi.org/10.1128/AAC.02412-14
39. Chu C, Feng Y, Chien AC, Hu S, Chu CH, Chiu CH. 2008. Evolution of genes on the Salmonella Virulence plasmid phylogeny revealed from sequencing of the virulence plasmids of S. enterica serotype Dublin and comparative analysis. Genomics 92:339-343. https://doi.org/10.1016/j.ygeno.2008.07.010
40. Davis MA, Besser TE, Eckmann K, MacDonald K, Green D, Hancock DD, Baker KN, Warnick LD, Soyer Y, Wiedmann M, Call DR. 2007. Multidrugresistant Salmonella Typhimurium, Pacific Northwest, United States. Emerg Infect Dis 13:1583-1586. https://doi.org/10.3201/eid1310.070536
41. Wong VK, Baker S, Pickard DJ, Parkhill J, Page AJ, Feasey NA, Kingsley RA, Thomson NR, Keane JA, Weill FX, Edwards DJ, Hawkey J, Harris SR, Mather AE, Cain AK, Hadfield J, Hart PJ, Thieu NT, Klemm EJ, Glinos DA, Breiman RF, Watson CH, Kariuki S, Gordon MA, Heyderman RS, Okoro C, Jacobs J, Lunguya O, Edmunds WJ, Msefula C, Chabalgoity JA, Kama M, Jenkins K, Dutta S, Marks F, Campos J, Thompson C, Obaro S, MacLennan CA, Dolecek C, Keddy KH, Smith AM, Parry CM, Karkey A, Mulholland EK, Campbell JI, Dongol S, Basnyat B, Dufour M, Bandaranayake D, Naseri TT, Singh SP, Hatta M, Newton P, Onsare RS, Isaia L, Dance D, Davong V, Thwaites G, Wijedoru L, Crump JA, De Pinna E, Nair S, Nilles EJ, Thanh DP, Turner P, Soeng S, Valcanis M, Powling J, Dimovski K, Hogg G, Farrar J, Holt KE, Dougan G. 2015. Phylogeographical analysis of the dominant multidrug-resistant H58 clade of Salmonella Typhi identifies inter-and intracontinental transmission events. Nat Genet 47:632-639. https://doi.org/10.1038/ng.3281
42. Strachan NJ, Rotariu O, Lopes B, MacRae M, Fairley S, Laing C, Gannon V, Allison LJ, Hanson MF, Dallman T, Ashton P, Franz E, van Hoek AH, French NP, George T, Biggs PJ, Forbes KJ. 2015. Whole genome sequencing demonstrates that geographic variation of Escherichia coli O157 genotypes dominates host association. Sci Rep 5:14145. https://doi.org/10.1038/srep14145
43. Spoor LE, McAdam PR, Weinert LA, Rambaut A, Hasman H, Aarestrup FM, Kearns AM, Larsen AR, Skov RL, Fitzgerald JR. 2013. Livestock origin for a human pandemic clone of community-associated methicillin-resistant Staphylococcus aureus. mBio 4(4):e00356-13. https://doi.org/10.1128/mBio.00356-13
44. Ward MJ, Gibbons CL, McAdam PR, van Bunnik BA, Girvan EK, Edwards GF, Fitzgerald JR, Woolhouse ME. 2014. Time-scaled evolutionary analysis of the transmission and antibiotic resistance dynamics of Staphylococcus aureus clonal complex 398. Appl Environ Microbiol 80:7275-7282. https://doi.org/10.1128/AEM.01777-14
45. Madec JY, Haenni M, Nordmann P, Poirel L. 2017. ESBL/AmpC-and carbapenemase-producing Enterobacteriaceae in animals: a threat for humans? Clin Microbiol Infect https://doi.org/10.1016/j.cmi.2017.01.013
46. CLSI. 2012. Performance standards for antimicrobial susceptibility testing; twenty-second informational supplement. M100-D22, 22nd ed. Clinical Laboratory Standard Institute, Wayne, PA
47. CLSI. 2013. Performance standards for antimicrobial disk and dilution susceptibility tests for bacteria isolated from animals approved standard- fourth edition. VET01-A4, 3rd ed. Clinical and Laboratory Standards Institute, Wayne, PA
48. Bolger AM, Lohse M, Usadel B. 2014. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30:2114-2120. https://doi.org/10.1093/bioinformatics/btu170
49. Babraham Bioinformatics. 2014. FastQC v. 0.11.2. http://www.bioinformatics.babraham.ac.uk/projects/fastqc/
50. Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, Kulikov AS, Lesin VM, Nikolenko SI, Pham S, Prjibelski AD, Pyshkin AV, Sirotkin AV, Vyahhi N, Tesler G, Alekseyev MA, Pevzner PA. 2012. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 19:455-477. https://doi.org/10.1089/cmb.2012.0021
51. Bushnell B. 2015. BBMap v. 35.49, https://sourceforge.net/projects/bbmap/
52. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R, 1000 Genome Project Data Processing Subgroup. 2009. The sequence alignment/map format and SAMtools. Bioinformatics 25:2078-2079. https://doi.org/10.1093/bioinformatics/btp352
53. Zhang S, Yin Y, Jones MB, Zhang Z, Deatherage Kaiser BL, Dinsmore BA, Fitzgerald C, Fields PI, Deng X. 2015. Salmonella serotype determination utilizing high-throughput genome sequencing data. J Clin Microbiol 53:1685-1692. https://doi.org/10.1128/JCM.00323-15
54. Inouye M, Dashnow H, Raven LA, Schultz MB, Pope BJ, Tomita T, Zobel J, Holt KE. 2014. SRST2: rapid genomic surveillance for public health and hospital microbiology labs. Genome Med 6:90. https://doi.org/10.1186/s13073-014-0090-6
55. University of Warwick. 2015. Salmonella enterica MLST database. University of Warwick, Coventry, England
56. Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J, Bealer K, Madden TL. 2009. BLAST+: architecture and applications. BMC Bioinformatics 10:421. https://doi.org/10.1186/1471-2105-10-421
57. Gardner SN, Hall BG. 2013. When whole-genome alignments just won't work: kSNP v2 software for alignment-free SNP discovery and phylogenetics of hundreds of microbial genomes. PLoS One 8:e81760. https://doi.org/10.1371/journal.pone.0081760
58. Iqbal Z, Caccamo M, Turner I, Flicek P, McVean G. 2012. De novo assembly and genotyping of variants using colored de Bruijn graphs. Nat Genet 44:226-232. https://doi.org/10.1038/ng.1028
59. Sangal V, Harbottle H, Mazzoni CJ, Helmuth R, Guerra B, Didelot X, Paglietti B, Rabsch W, Brisse S, Weill FX, Roumagnac P, Achtman M. 2010. Evolution and population structure of Salmonella enterica serovar Newport. J Bacteriol 192:6465-6476. https://doi.org/10.1128/JB.00969-10
60. PLINK/Seq.2014. PLINK/Seq v. 0.10. https://atgu.mgh.harvard.edu/plinkseq/
61. Croucher NJ, Page AJ, Connor TR, Delaney AJ, Keane JA, Bentley SD, Parkhill J, Harris SR. 2015. Rapid phylogenetic analysis of large samples of recombinant bacterial whole genome sequences using Gubbins. Nucleic Acids Res 43:e15. https://doi.org/10.1093/nar/gku1196
62. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. 2013. MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol Biol Evol 30:2725-2729. https://doi.org/10.1093/molbev/mst197
63. Tavare S. 1986. Some probabilistic and statistical problems in the analysis of DNA sequences, p 57-86. In Miura RM (ed), Lectures on mathematics in the life sciences, vol 17. American Mathematical Society, Providence, RI
64. Kimura M. 1980. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111-120. https://doi.org/10.1007/BF01731581
65. Drummond AJ, Suchard MA, Xie D, Rambaut A. 2012. Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol Biol Evol 29:1969-1973. https://doi.org/10.1093/molbev/mss075
66. Rambaut A. 2013. Analysis of variable sites only in BEAST or MrBayes. https://groups.google.com/forum/#!topic/beast-users/V5vRghILMfw
67. Rambaut A, Lam TT, Max Carvalho L, Pybus OG. 2016. Exploring the temporal structure of heterochronous sequences using TempEst (formerly Path-O-Gen). Virus Evol 2(1):vew007. https://doi.org/10.1093/ve/vew007
68. Drummond AJ, Ho SY, Phillips MJ, Rambaut A. 2006. Relaxed phylogenetics and dating with confidence. PLoS Biol 4:e88. https://doi.org/10.1371/journal.pbio.0040088
69. Drummond AJ, Rambaut A, Shapiro B, Pybus OG. 2005. Bayesian coalescent inference of past population dynamics from molecular sequences. Mol Biol Evol 22:1185-1192. https://doi.org/10.1093/molbev/msi103
70. Baele G, Li WL, Drummond AJ, Suchard MA, Lemey P. 2013. Accurate model selection of relaxed molecular clocks in Bayesian phylogenetics. Mol Biol Evol 30:239-243. https://doi.org/10.1093/molbev/mss243
71. Baele G, Lemey P, Bedford T, Rambaut A, Suchard MA, Alekseyenko AV. 2012. Improving the accuracy of demographic and molecular clock model comparison while accommodating phylogenetic uncertainty. Mol Biol Evol 29:2157-2167. https://doi.org/10.1093/molbev/mss084
72. R Core Team. 2016. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/
73. Holm S. 1979. A simple sequentially rejective multiple test procedure. Scand J Statistics 6:65-70
74. Clarke KR. 1993. Non-parametric multivariate analyses of changes in community structure. Austral J Ecol 18:117-143. https://doi.org/10.1111/j.1442-9993.1993.tb00438.x
75. Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PR, O'Hara RB, Simpson GL, Solymos P, Stevens MHH, Szoecs E, Helene Wagner H. 2016. vegan: community ecology package, v2.4-0. https://CRAN.R-project.org/package=vegan
76. Anderson MJ, Walsh DCI. 2013. PERMANOVA, ANOSIM, and the Mantel test in the face of heterogeneous dispersions: what null hypothesis are you testing? Ecol Monographs 83:557-574. https://doi.org/10.1890/12-2010.1
77. Lozupone C, Knight R. 2005. UniFrac: a new phylogenetic method for comparing microbial communities. Appl Environ Microbiol 71: 8228-8235. https://doi.org/10.1128/AEM.71.12.8228-8235.2005
78. Chase JM, Kraft NJB, Smith KG, Vellend M, Inouye BD. 2011. Using null models to disentangle variation in community dissimilarity from variation in α-diversity. Ecosphere 2:1-11. https://doi.org/10.1890/ES10-00117.1
79. Anderson MJ. 2001. A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:32-46
80. Kruskal JB. 1964. Multidimensional scaling by optimizing goodness of fit to a nonmetric hypothesis. Psychometrika 29:1-27. https://doi.org/10.1007/BF02289565
81. Kruskal JB. 1964. Nonmetric multidimensional scaling: a numerical method. Psychometrika 29:115-129. https://doi.org/10.1007/BF02289694