What can pathogen phylogenetics tell us about cross-species transmission?
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- Delilah Norton
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1 The Boyd Orr Centre for Population and Ecosystem Health What can pathogen phylogenetics tell us about cross-species transmission? Roman Biek! Bovine TB workshop 3 Sep 2015
2 Talk outline Genetic tracking of pathogen transmission Host species as discrete character states Analytical challenges Case studies: CSF and btb 1
3 Two-host transmission tree Cattle Badgers Time
4 Two-host transmission tree Cattle Host switches: How often? Which direction? Badgers Time
5 Actual transmission tree is unknown Cattle Badgers Time
6 Actual transmission tree is unknown Most hosts are not sampled Cattle Badgers Time
7 Actual transmission tree is unknown Most hosts are not sampled Cattle Badgers Time Host switch missed
8 Actual transmission tree is unknown Mutations make tree visible Cattle Badgers Time
9 Rare switches are easy to detect 8
10 Only applies to few reservoir systems Host switches only rare in this zone! Viana et al. 2014, Trends Ecol & Evol 9
11 Frequent switches create ambiguous signal Multiple switches or continuous transmission?! 10
12 Quantifying cross-species transmission What is the minimum number of host switches needed to explain phylogenetic patterns? => parsimony principle Alternative: model host switches over time using Markovian rate matrix (Pagel 1994, Proc Royal Soc B) allows for undetected changes probabilistic model => can be fit using likelihood general method for discrete character evolution 11
13 Example: classical swine fever virus (CSF) Cross species transmission parameters dp1 Symmetrical Asymmetrical β βi,j wb1 dp1 βj,i wb1
14 Inferring host state probabilities for internal tree nodes Host state probabilities for each node Czech Republic Austria Slovakia!! wild boar domestic pig 1! CSF0120/AT/unknown/wb/1994 CSF0119/AT/unknown/dp/1992 CSF0077/CZ/Trebic/dp/1992! CSF0733/AT/NOE/wb/2000! CSF0728/SK/NoveZamky/wb/2000! CSF0727/SK/RimavskaS/wb/2000! CSF0374/CZ/Vyskov/wb/1996! CSF0737/AT/NOE/wb/2000! CSF0829/CZ/unknown/dp/1995! CSF0825/CZ/unknown/dp/1995! CSF0827/CZ/unknown/dp/1995! CSF0823/CZ/unknown/dp/1995! CSF0115/AT/unknown/dp/1992! CSF0126/AT/Kaernten/dp/1995! CSF0370/CZ/Vyskov/wb/1997! CSF0122/AT/unknown/dp/1994! CSF0121/AT/unknown/dp/1994! CSF0150/AT/unknown/wb/1993! CSF0152/AT/unknown/wb/1996! CSF0151/AT/NOE/wb/1996! CSF0369/CZ/Kromeriz/dp/1997! CSF0368/CZ/Hodonin/wb/1997! CSF0373/CZ/Breclav/wb/1996! CSF0371/CZ/UhHradiste/wb/1997! CSF0372/CZ/Hodonin/wb/1996! CSF0117/AT/unknown/dp/1992! CSF0118/AT/unknown/dp/1992! CSF0116/AT/unknown/dp/1992! CSF0376/CZ/Znojmo/wb/1996! CSF0377/CZ/unknown/dp/1996! CSF0711/SK/Snina/wb/1995! CSF0715/SK/Lucenec/wb/1996! CSF0716/SK/Senica/dp/1996! CSF0714/SK/Lucenec/dp/1996! CSF0713/SK/NoveZamky/wb/1996! CSF0712/SK/NoveZamky/wb/1996! CSF0584/CZ/unknown/wb/1998! CSF0585/CZ/unknown/wb/1998! CSF0583/CZ/Zlin/wb/1998! CSF0581/CZ/UhHradiste/wb/1998! CSF0580/CZ/unknown/wb/1998! CSF0582/CZ/unknown/wb/1997! CSF0528/SK/Revuca/wb/1998! CSF0527/SK/Namestovo/wb/1998! CSF0710/SK/ZlateMor/wb/2000! CSF0378/CZ/Tabor/dp/1994! CSF0380/CZ/Jihlava/wb/1993! CSF0381/CZ/unknown/wb/1993! CSF0719/SK/BanskaSti/wb/1997! CSF0720/SK/Levice/wb/1997! CSF0722/SK/Levice/wb/1998! CSF0726/SK/ZiarnadH/wb/1999! CSF0725/SK/Poltar/dp/1998! CSF0723/SK/NoveZamky/wb/1999! CSF0721/SK/Nitra/dp/1997! CSF0718/SK/RimavskaS/dp/2000!! Wild boar Domestic pig
15 CSF0107/DE/wb1/1994 CSF0573/IT/dp1/1998 CSF0480/DE/wb1/ Spatial population structure Three spatially distinct clades of CSF CSF0811/DE/dp1/2002 CSF0337/ES/dp1/1997 CSF0264/DE/wb1/1996 CSF0247/DE/dp1/1994 CSF0365/DE/dp1/1997 CSF0277/DE/dp1/1997 CSF0360/ES/dp1/1997 CSF0265/DE/wb1/1997 CSF0270/DE/dp1/1994 CSF0329/DE/dp1/1997 CSF0243/DE/dp1/1994 CSF0326/DE/wb1/1996 CSF0354/DE/dp1/1997 CSF0349/DE/dp1/1997 CSF0366/DE/dp1/1997 CSF0268/DE/wb1/1992 CSF0295/PL/dp1/1995 CSF0359/DE/dp1/1997 CSF0356/DE/dp1/1997 CSF0320/PL/dp1/1996 CSF0292/PL/dp1/1995 CSF0624/DE/wb1/1999 CSF0798/DE/dp1/2002 CSF0378/CZ/dp1/1994 CSF0384/DE/wb1/1993 CSF0713/SK/wb1/1996 CSF0785/IT/dp1/2001 CSF0393/DE/dp1/1997 CSF0376/CZ/wb1/1996 CSF0716/SK/dp1/1996 CSF0633/DE/dp1/1999 CSF0622/DE/wb1/1999 CSF0778/DE/dp1/2001 CSF0729/DE/wb1/2000 CSF0617/YU/dp1/1999 CSF0616/RS/dp1/1999 CSF0387/DE/dp1/1994 CSF0097/DE/dp1/1993 CSF0331/DE/wb1/1997 CSF0599/CH/wb1/1998 CSF0273/DE/dp1/1997 CSF0272/DE/dp1/1997 CSF0260/DE/dp1/1993 CSF0327/DE/dp1/1997 CSF0258/DE/dp1/1994 CSF0259/DE/dp1/1995 CSF0283/NL/dp1/1997 CSF0371/CZ/wb1/1997 CSF0219/DE/dp1/1994 CSF0352/DE/dp1/1997 CSF0353/DE/dp1/1997 CSF0363/ES/dp1/1997 CSF0323/DE/wb1/1996 CSF0297/PL/dp1/1992 CSF0289/DE/wb1/1996 CSF0291/PL/dp1/1995 CSF0294/PL/dp1/1995 CSF0299/PL/dp1/1992 CSF0635/DE/dp1/1993 CSF0714/SK/dp1/1996 CSF0718/SK/dp1/2000 CSF0784/IT/dp1/2001 CSF0783/IT/dp1/2001 CSF0719/SK/wb1/1997 CSF0795/DE/dp1/2002 CSF0722/SK/wb1/1998 CSF0712/SK/wb1/1996 CSF0810/DE/dp1/2002 CSF0731/DE/wb1/2000 CSF0750/ES/dp1/2001 CSF0388/DE/dp1/1995 CSF0715/SK/wb1/1996 CSF0634/DE/dp1/1999 CSF0619/DE/wb1/1999 CSF0720/SK/wb1/1997 CSF0799/DE/wb1/2002 CSF0386/DE/dp1/1994 CSF0737/AT/wb1/2000 CSF0727/SK/wb1/2000 CSF0710/SK/wb1/2000 CSF0186/DE/dp1/1993 CSF0185/DE/dp1/1993 CSF0281/DE/dp1/1997CSF0146/DE/dp1/1995 CSF0364/ES/dp1/1997 CSF0257/DE/dp1/1995 CSF0839/RO/dp1/2004 CSF0335/DE/dp1/1997 CSF0333/DE/dp1/1997 CSF0334/DE/dp1/1997 CSF0339/DE/dp1/1997 CSF0251/DE/dp1/1994 CSF0324/DE/wb1/1996 CSF0282/DE/dp1/1997 CSF0286/DE/dp1/1994 CSF0263/DE/wb1/1996 CSF0218/DE/dp1/1994 CSF0328/DE/dp1/1997 CSF0271/DE/dp1/1994 CSF0245/DE/dp1/1994 CSF0262/DE/wb1/1996 CSF0330/DE/dp1/1997 CSF0325/DE/wb1/1996 CSF0351/DE/dp1/1997 CSF0350/DE/dp1/1997 CSF0361/ES/dp1/1997 CSF0348/DE/dp1/1997 CSF0347/DE/dp1/1997 CSF0341/DE/wb1/1997 CSF0340/DE/dp1/1997 CSF0345/DE/dp1/1997 CSF0369/CZ/dp1/1997 CSF0370/CZ/wb1/1997 CSF0368/CZ/wb1/1997 CSF0304/DE/dp1/1997 CSF0319/PL/dp1/1993 CSF0290/PL/dp1/1995 CSF0355/DE/dp1/1997 CSF0357/DE/dp1/1997 CSF0358/DE/dp1/1997 CSF0288/DE/dp1/1997 CSF0287/DE/dp1/1997 CSF0301/DE/dp1/1997 CSF0318/PL/dp1/1994 CSF0296/PL/dp1/1992 CSF0298/PL/dp1/1992 CSF0790/DE/dp1/2002 CSF0791/DE/dp1/2002 CSF0793/DE/dp1/2002 CSF0789/DE/dp1/2002 CSF0809/DE/dp1/2002 CSF0391/DE/dp1/1997 CSF0390/DE/dp1/1997 CSF0389/DE/dp1/1995 CSF0098/DE/dp1/1993 CSF0621/DE/wb1/1999 CSF0618/DE/wb1/1999 CSF0623/DE/wb1/1999 CSF0374/CZ/wb1/1996 CSF0385/DE/dp1/1994 CSF0721/SK/dp1/1997 CSF0725/SK/dp1/1998 CSF0777/DE/dp1/2001 CSF0638/DE/wb1/1998 CSF0728/SK/wb1/2000 CSF0658/DE/dp1/1999 CSF0781/DE/wb1/2001 CSF0093/DE/dp1/1993 CSF0636/DE/wb1/1993 CSF0723/SK/wb1/1999 CSF0752/DE/dp1/2001 CSF0779/DE/wb1/2001 CSF0733/AT/wb1/2000 CSF0748/DE/dp1/2001 CSF0782/DE/wb1/2001 CSF0780/DE/wb1/2001 CSF0092/DE/wb1/1992 CSF0380/CZ/wb1/1993 CSF0726/SK/wb1/1999 CSF0711/SK/wb1/1995 CSF0794/DE/dp1/2002 CSF0109/DE/wb1/1994 CSF0096/DE/wb1/1993 CSF0095/DE/dp1/1993 CSF0210/DE/dp1/1994 CSF0078/DE/dp1/1992 CSF0084/DE/dp1/1992 CSF0077/CZ/dp1/1992 CSF0105/DE/dp1/1994 CSF0104/DE/dp1/1994 CSF0106/DE/dp1/1994 CSF0103/DE/dp1/1993 CSF0083/DE/dp1/1992 CSF0079/DE/dp1/1992 CSF0089/DE/dp1/1992 CSF0574/DE/wb1/1998 CSF0570/DE/wb1/1998 CSF0571/ES/dp1/1998 CSF0527/SK/wb1/1998 CSF0838/RO/dp1/2004 CSF0401/IT/wb1/1997 CSF0407/IT/wb1/1997 CSF0485/DE/wb1/1997 CSF0495/DE/wb1/1997 CSF0605/BG/dp1/1998 CSF0600/DE/wb1/1998 CSF0587/DE/dp1/1998 CSF0588/DE/wb1/1998 CSF0589/DE/wb1/1998 CSF0822/FR/wb1/2003 CSF0837/RO/dp1/2004 CSF0576/FR/wb1/1992 CSF0606/BG/dp1/1998 CSF0090/DE/wb1/1992 CSF0437/DE/dp1/1995 CSF0400/IT/wb1/1997 CSF0404/IT/wb1/1997 CSF0577/FR/wb1/1997 CSF0406/IT/dp1/1997 CSF0422/ES/dp1/1997 CSF0373/CZ/wb1/1996 CSF0372/CZ/wb1/1996 CSF0184/DE/wb1/1993 CSF0405/IT/wb1/1997 CSF0126/AT/dp1/1995 CSF0138/DE/dp1/1995 CSF0598/CH/wb1/1998 CSF0593/DE/wb1/1998 CSF0484/DE/dp1/1998 CSF0581/CZ/wb1/1998 CSF0583/CZ/wb1/1998 CSF0578/DE/wb1/1998 CSF0608/BG/wb1/1999 CSF0615/YU/dp1/1999 CSF0100/DE/dp1/1993 CSF0572/ES/dp1/1998CSF0101/DE/dp1/1993 CSF0590/DE/wb1/1998 CSF0607/BG/dp1/1999 CSF0528/SK/wb1/1998 CSF0113/DE/dp1/1994 CSF0114/DE/dp1/1994 CSF0123/DE/dp1/1995 CSF0148/DE/dp1/1994 CSF0131/DE/dp1/1994 CSF0136/DE/dp1/1994 CSF0171/DE/wb1/1996 CSF0132/DE/dp1/1994 CSF0575/FR/wb1/1992 CSF0436/DE/dp1/1995 CSF0402/IT/dp1/1997 CSF0609/BG/dp1/1997 CSF0102/DE/dp1/1993 CSF0483/DE/wb1/1995 CSF0463/DE/wb1/1995 CSF0411/DE/wb1/1997 CSF0167/DE/wb1/1996 CSF0141/DE/dp1/1995 CSF0142/DE/dp1/1995 CSF0145/DE/dp1/1995 CSF0591/DE/wb1/1998 CSF0124/DE/dp1/1995 CSF0183/DE/wb1/1993 CSF0125/DE/dp1/1995 CSF0147/DE/dp1/1995 CSF0134/DE/dp1/1995 CSF0166/DE/wb1/1996 CSF0144/DE/dp1/1995 CSF0399/IT/dp1/1997 CSF0424/ES/dp1/1998 CSF0579/DE/dp1/1998 CSF0423/ES/dp1/1998 CSF0614/YU/dp1/1999 CSF0112/DE/dp1/1994 CSF0140/DE/dp1/1995 CSF0143/DE/dp1/1995 CSF0151/AT/wb1/1996 CSF0139/DE/dp1/1995 CSF0812/DE/dp1/2002 CSF0865/BG/dp2/2007 CSF0861/BG/dp2/2007 CSF0864/BG/dp2/2007 CSF0862/BG/dp2/2007 CSF0852/BG/dp2/2006 CSF0853/BG/dp2/2006 CSF0857/DE/dp2/2006 CSF0868/HR/dp2/2006 CSF0860/BG/dp2/2006 CSF0859/BG/dp2/2006 CSF0894/RO/dp2/2007 CSF0895/RO/dp2/2006 CSF0896/RO/dp2/2006 CSF0897/RO/dp2/2006 CSF0893/RO/dp2/2006 CSF0882/RO/dp2/2006 CSF0886/RO/dp2/2006 CSF0841/RO/dp2/2004 CSF0848/RO/dp2/2004 CSF0846/RO/dp2/2004 CSF0858/BG/wb2/2004 CSF0871/HR/dp2/2007 CSF0880/RO/dp2/2007 CSF0877/RO/dp2/2007 CSF0890/RO/wb2/2007 CSF0892/RO/dp2/2006 CSF0847/RO/dp2/2004 CSF0879/RO/dp2/2006 CSF0881/RO/dp2/2006 CSF0883/RO/dp2/2006 CSF0891/RO/dp2/2006 CSF0885/RO/dp2/2006 CSF0888/RO/dp2/2006 CSF0887/RO/dp2/2006 CSF0889/RO/dp2/2006 CSF0840/RO/dp2/2004 XXX0288/FR/dp2/2002 XXX0287/FR/wb2/2002 XXX0289/FR/wb2/2002 XXX0498/IT/dp2/1998 XXX0315/NL/dp2/1997 XXX0372/IT/dp2/1997 XXX0499/IT/dp2/1997 XXX0500/IT/wb2/1997 XXX0167/IT/dp2/1992 CSF1045/DE/wb2/2009 XXX0252/HU/wb2/2007 CSF1023/RO/dp2/2007 XXX0250/HR/dp2/2007 CSF1020/RO/dp2/2007 CSF1021/RO/dp2/2007 CSF1025/RO/dp2/2007 XXX0281/FR/dp2/2002 CSF1011/RO/dp2/2006 CSF1008/RO/dp2/2006 CSF1012/RO/dp2/2006 CSF1013/RO/dp2/2006 XXX0284/FR/wb2/2002 CSF1018/RO/dp2/2007 CSF1005/RO/dp2/2005 XXX0501/IT/wb2/1998 XXX0286/FR/wb2/2002 XXX0168/IT/dp2/1992 CSF1053/RS/dp2/2010 CSF1049/BG/wb2/2009 CSF1026/RO/dp2/2007 CSF1027/HU/wb2/2007 CSF1024/RO/dp2/2007 CSF1022/RO/dp2/2007 XXX0277/FR/wb2/2002 XXX0278/FR/dp2/2002 XXX0280/FR/dp2/2002 CSF1009/RO/dp2/2006 CSF1019/RO/dp2/2007 CSF1010/RO/dp2/2006 XXX0282/FR/dp2/2002 XXX0283/FR/wb2/2002 CSF1003/RO/dp2/2005 CSF1004/RO/wb2/2005 CSF1001/RO/dp2/2006 CSF0898/RO/dp2/2006 XXX0520/IT/wb3/1995 XXX0506/IT/dp3/1997 XXX0507/IT/dp3/1997 XXX0511/IT/dp3/1997 XXX0505/IT/dp3/1997 XXX0502/IT/dp3/1997 XXX0503/IT/wb3/1997 XXX0504/IT/wb3/1998 XXX0610/RS/wb3/2005 XXX0559/IT/dp3/1997 XXX0526/IT/dp3/1998 XXX0612/RS/wb3/2006 XXX0512/IT/dp3/1998 XXX0561/IT/wb3/1998 XXX0521/IT/wb3/1995 XXX0522/IT/dp3/1997 XXX0558/IT/dp3/1996 XXX0611/RS/wb3/2004 XXX0519/IT/wb3/1995 XXX0560/IT/wb3/1997 XXX0562/IT/wb3/1997 XXX0564/IT/wb3/1997 XXX0531/IT/dp3/1997 XXX0563/IT/wb3/1998 XXX0542/IT/dp3/1999 XXX0565/IT/wb3/1998 XXX0557/IT/wb3/2000 XXX0541/IT/dp3/1999 XXX0540/IT/dp3/1999 XXX0539/IT/dp3/2000 XXX0569/IT/dp3/1999 XXX0608/DE/wb3/2005 Central Europe SE Europe Italy How do patterns of cross-species transmission compare between different parts of Europe? => Potential for sampling bias: Has relative sampling effort with respect to pigs and boar been the same across these areas?
16 Estimated rates of cross species transmission Annual transmission probability Central Europe SE Europe SE Europe Italy
17 Effects of sampling bias? More virus samples available from domestic pigs Central Europe SE Europe Italy
18 Reduce sampling bias by down-sampling Randomly remove taxa from tree => repeat 40x ΔAIC Delta AIC Original model still receives highest support!!!!!!! Central Europe SE Europe Italy mod1 mod2 mod3 mod4 mod5 mod6 Models Models
19 Assessing the effect of biased sampling using simulations Empirical ratio in CSF study Inferred transmission probability 0 1 boar/pig ra.o 0 1 Domestic pig to wild boar Wild boar to domestic pig Qualitatively robust but quantitatively highly susceptible to sampling bias!
20 Lessons from M bovis genome data Trewby et al., in review 1 SNP VNTR-10 Clade 1 cattle sample VNTR-10 Clade 2 cattle sample VNTR-10 badger sample VNTR-1 cattle sample 1 SNP VNTR-1 badger sample VNTR-10 lineage VNTR-1 lineage Limited phylogenetic resolution No badger-associated clades Group&1& VNTR-type switching 89/96 95/99 90/99 65/90 87/99 95/100 2 A 75/99 3 D 1 B C Group&2& Evolution measurable but slow: on average one mutation every 4-5 years 19
21 Evolution & epidemiology: relative time scales Biek et al. 2015, Trends Ecol Evol 20
22 Conclusions Cross-species transmission can be inferred using discrete character state approach Inference rarely straight forward, especially with respect to quantitative answers Sampling biases may drive results - difficult to avoid but important to assess Additional challenges in the case of M. bovis => sequence data alone will be insufficient to reveal transmission patterns 21
23 Acknowledgements btb - Rowland Kao, Hannah Trewby, Robin Skuce and team at AFBI CSF Thibaud Boutin Research and Policy in Infectious Disease Dynamics (RAPIDD)
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