Abstract
Phylogenetics is an important component of the systems biology approach. Knowledge about evolution of the genus Leishmania is essential to understand various aspects of basic biology of these parasites, such as parasite–host or parasite–vector relationships, biogeography, or epidemiology. Here, we present a comprehensive guideline for performing phylogenetic studies based on DNA sequence data, but with principles that can be adapted to protein sequences or other molecular markers. It is presented as a compilation of the most commonly used genetic targets for phylogenetic studies of Leishmania, including their respective primers for amplification and references, as well as details of PCR assays. Guidelines are, then, presented to choose the best targets in relation to the types of samples under study. Finally, and importantly, instructions are given to obtain optimal sequences, alignments, and datasets for the subsequent data analysis and phylogenetic inference. Different bioinformatics methods and software for phylogenetic inference are presented and explained. This chapter aims to provide a compilation of methods and generic guidelines to conduct phylogenetics of Leishmania for nonspecialists.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
Similar content being viewed by others
Notes
- 1.
Long branch attraction is a phenomenon in phylogenetics that can alter tree topology. It can occur when the mutation rate is higher along a lineage, or in the presence of a single more distantly related branch. This longer branch tends to be pushed toward the root, or toward shorter branches. It is a problem for most methods, although more for some (Maximum Parsimony, UPGMA) than for others (Maximum Likelihood, Neighbor-Joining), but it is still a problem for those considered as the best methods, such as maximum likelihood, even for long (>100,000 positions) sequences [118]. Reviewed by [119].
References
Dedet J-P, Pratlong F, Lanotte G, Ravel C (1999) The Parasite. Clin Dermatol 17:261–268
Schönian G, Cupolillo E, Mauricio I (2013) Molecular evolution and phylogeny of Leishmania. In: Ponte-Sucre A, Diaz E, Padrón-Nieves M (eds) Drug resistance in Leishmania parasites. Springer, Vienna, pp 15–44. https://doi.org/10.1007/978-3-7091-1125-3_2
Akhoundi M, Kuhls K, Cannet A, Votýpka J, Marty P, Delaunay P, Sereno D (2016) A historical overview of the classification, evolution, and dispersion of Leishmania parasites and sandflies. PLoS Negl Trop Dis 10(3):e0004349
Mauricio I (2018) Leishmania taxonomy. In: Bruschi F, Gradoni L (eds) The leishmaniases: old neglected tropical diseases. Springer, Cham, pp 15–30. https://doi.org/10.1007/978-3-319-72386-0
Lanotte G, Rioux JA, Lepart J, Maazoun R, Pasteur N, Pratlong F (1984) Numerical cladistics of the phylogeny of the genus Leishmania Ross, 1903 (Kinetoplastida-Trypanosomatidae). Use of enzyme characteristics. C R Acad Sci III 299(19):769–772
Rioux JA, Lanotte G, Serres E, Pratlong F, Bastien P, Perieres J (1990) Taxonomy of Leishmania. Use of isoenzymes. Suggestions for a new classification. Ann Parasitol Hum Comp 65(3):111–125
Thomaz-Soccol V, Lanotte G, Rioux JA, Pratlong F, Martini-Dumas A, Serres E (1993) Monophyletic origin of the genus Leishmania Ross, 1903. Ann Parasitol Hum Comp 68(2):107–108
Thomaz-Soccol V, Lanotte G, Rioux JA, Pratlong F, Martini-Dumas A, Serres E (1993) Phylogenetic taxonomy of New World Leishmania. Ann Parasitol Hum Comp 68(2):104–106
Cupolillo E, Grimaldi G Jr, Momen H (1994) A general classification of New World Leishmania using numerical zymotaxonomy. Am J Trop Med Hyg 50(3):296–311
Schönian G, Kuhls K, Mauricio IL (2011) Molecular approaches for a better understanding of the epidemiology and population genetics of Leishmania. Parasitology 138(4):405–425
Van der Auwera G, Dujardin JC (2015) Species typing in dermal leishmaniasis. Clin Microbiol Rev 28(2):265–294. https://doi.org/10.1128/cmr.00104-14
Akhoundi M, Downing T, Votýpka J, Kuhls K, Lukeš J, Cannet A, Ravel C, Marty P, Delaunay P, Kasbari M, Granouillac B, Gradoni L, Sereno D (2017) Leishmania infections: molecular targets and diagnosis. Mol Aspects Med 57:1–29
Espinosa OA, Serrano MG, Camargo EP, Teixeira MM, Shaw JJ (2018) An appraisal of the taxonomy and nomenclature of trypanosomatids presently classified as Leishmania and Endotrypanum. Parasitology 145(4):430–442. https://doi.org/10.1017/s0031182016002092
Maslov DA, Lukeš J, Jirků M, Simpson L (1996) Phylogeny of trypanosomes as inferred from the small and large subunit rRNAs: implications for the evolution of parasitism in the trypanosomatid protozoa. Mol Biochem Parasitol 75(2):197–205
Noyes HA, Camps AP, Chance ML (1996) Leishmania herreri (Kinetoplastida; Trypanosomatidae) is more closely related to Endotrypanum (Kinetoplastida; Trypanosomatidae) than to Leishmania. Mol Biochem Parasitol 80(1):119–123
Noyes HA, Arana BA, Chance ML, Maingon R (1997) The Leishmania hertigi (Kinetoplastida; Trypanosomatidae) complex and the lizard Leishmania: their classification and evidence for a neotropical origin of the Leishmania-Endotrypanum clade. J Eukaryot Microbiol 44(5):511–517
Lukeš J, Jirků M, Dolezel D, Kral'ová I, Hollar L, Maslov DA (1997) Analysis of ribosomal RNA genes suggests that trypanosomes are monophyletic. J Mol Evol 44(5):521–527
Hollar L, Lukeš J, Maslov DA (1998) Monophyly of endosymbiont containing trypanosomatids: phylogeny versus taxonomy. J Eukaryot Microbiol 45(3):293–297
Stevens JR, Noyes HA, Dover GA, Gibson WC (1999) The ancient and divergent origins of the human pathogenic trypanosomes, Trypanosoma brucei and T cruzi. Parasitology 118(Pt 1):107–116
Stevens JR, Noyes HA, Schofield CJ, Gibson W (2001) The molecular evolution of Trypanosomatidae. Adv Parasitol 48:1–56
Maslov DA, Podlipaev SA, Lukeš J (2001) Phylogeny of the kinetoplastida: taxonomic problems and insights into the evolution of parasitism. Mem Inst Oswaldo Cruz 96(3):397–402
Merzlyak E, Yurchenko V, Kolesnikov AA, Alexandrov K, Podlipaev SA, Maslov DA (2001) Diversity and phylogeny of insect trypanosomatids based on small subunit rRNA genes: polyphyly of Leptomonas and Blastocrithidia. J Eukaryot Microbiol 48(2):161–169
Hamilton PB, Stevens JR, Gaunt MW, Gidley J, Gibson WC (2004) Trypanosomes are monophyletic: evidence from genes for glyceraldehyde phosphate dehydrogenase and small subunit ribosomal RNA. Int J Parasitol 34(12):1393–1404. https://doi.org/10.1016/j.ijpara.2004.08.011
Moreira D, Lopez-Garcia P, Vickerman K (2004) An updated view of kinetoplastid phylogeny using environmental sequences and a closer outgroup: proposal for a new classification of the class Kinetoplastea. Int J Syst Evol Microbiol 54(Pt 5):1861–1875. https://doi.org/10.1099/ijs.0.63081-0
Simpson AG, Stevens JR, Lukeš J (2006) The evolution and diversity of kinetoplastid flagellates. Trends Parasitol 22(4):168–174. https://doi.org/10.1016/j.pt.2006.02.006
Guan W, Cao DP, Sun K, Xu JN, Zhang JR, Chen DL, Chen JP (2012) Phylogenic analysis of Chinese Leishmania isolates based on small subunit ribosomal RNA (SSU rRNA) and 7 spliced leader RNA (7SL RNA). Acta Parasitol 57(2):101–113. https://doi.org/10.2478/s11686-012-0022-9
Leelayoova S, Siripattanapipong S, Hitakarun A, Kato H, Tan-ariya P, Siriyasatien P, Osatakul S, Mungthin M (2013) Multilocus characterization and phylogenetic analysis of Leishmania siamensis isolated from autochthonous visceral leishmaniasis cases, southern Thailand. BMC Microbiol 13:60. https://doi.org/10.1186/1471-2180-13-60
Marcili A, Speranca MA, da Costa AP, Madeira Mde F, Soares HS, Sanches Cde O, Acosta Ida C, Girotto A, Minervino AH, Horta MC, Shaw JJ, Gennari SM (2014) Phylogenetic relationships of Leishmania species based on trypanosomatid barcode (SSU rDNA) and gGAPDH genes: Taxonomic revision of Leishmania (L.) infantum chagasi in South America. Infect Genet Evol 25:44–51. https://doi.org/10.1016/j.meegid.2014.04.001
Lukeš J, Skalicky T, Tyc J, Votýpka J, Yurchenko V (2014) Evolution of parasitism in kinetoplastid flagellates. Mol Biochem Parasitol 195(2):115–122. https://doi.org/10.1016/j.molbiopara.2014.05.007
Yurchenko VY, Lukeš J, Jirků M, Zeledon R, Maslov DA (2006) Leptomonas costaricensis sp. n. (Kinetoplastea: Trypanosomatidae), a member of the novel phylogenetic group of insect trypanosomatids closely related to the genus Leishmania. Parasitology 133(Pt 5):537–546. https://doi.org/10.1017/s0031182006000746
Yurchenko V, Lukeš J, Xu X, Maslov DA (2006) An integrated morphological and molecular approach to a new species description in the Trypanosomatidae: the case of Leptomonas podlipaevi n. sp., a parasite of Boisea rubrolineata (Hemiptera: Rhopalidae). J Eukaryot Microbiol 53(2):103–111. https://doi.org/10.1111/j.1550-7408.2005.00078.x
Svobodová M, Zídková L, Čepička I, Oborník M, Lukeš J, Votýpka J (2007) Sergeia podlipaevi gen. nov., sp. nov. (Trypanosomatidae, Kinetoplastida), a parasite of biting midges (Ceratopogonidae, Diptera). Int J Syst Evol Microbiol 57(Pt 2):423–432. https://doi.org/10.1099/ijs.0.64557-0
van Eys GJ, Schoone GJ, Kroon NC, Ebeling SB (1992) Sequence analysis of small subunit ribosomal RNA genes and its use for detection and identification of Leishmania parasites. Mol Biochem Parasitol 51(1):133–142
Noyes H, Pratlong F, Chance M, Ellis J, Lanotte G, Dedet JP (2002) A previously unclassified trypanosomatid responsible for human cutaneous lesions in Martinique (French West Indies) is the most divergent member of the genus Leishmania ss. Parasitology 124(Pt 1):17–24
Croan DG, Morrison DA, Ellis JT (1997) Evolution of the genus Leishmania revealed by comparison of DNA and RNA polymerase gene sequences. Mol Biochem Parasitol 89(2):149–159
Kuhls K, Sinning D, Rauhut F, Köhler K, Litzke LF, Schönian G (2013) Leishmania siamensis as the cause of autochthonous cutaneous leishmaniasis of horses in Germany–a new emerging zoonotic disease? Paper presented at the In: Abstracts book–5th World Congress on Leishmaniasis, 13–17 May, Abstract P694, Porto de Galinhas, Pernambuco, Brazil
Croan D, Ellis J (1996) Phylogenetic relationships between Leishmania, Viannia and Sauroleishmania inferred from comparison of a variable domain within the RNA polymerase II largest subunit gene. Mol Biochem Parasitol 79(1):97–102
Dougall AM, Alexander B, Holt DC, Harris T, Sultan AH, Bates PA, Rose K, Walton SF (2011) Evidence incriminating midges (Diptera: Ceratopogonidae) as potential vectors of Leishmania in Australia. Int J Parasitol 41(5):571–579. https://doi.org/10.1016/j.ijpara.2010.12.008
Pothirat T, Tantiworawit A, Chaiwarith R, Jariyapan N, Wannasan A, Siriyasatien P, Supparatpinyo K, Bates MD, Kwakye-Nuako G, Bates PA (2014) First isolation of Leishmania from Northern Thailand: case report, identification as Leishmania martiniquensis and phylogenetic position within the Leishmania enriettii complex. PLoS Negl Trop Dis 8(12):e3339. https://doi.org/10.1371/journal.pntd.0003339
Kwakye-Nuako G, Mosore MT, Duplessis C, Bates MD, Puplampu N, Mensah-Attipoe I, Desewu K, Afegbe G, Asmah RH, Jamjoom MB, Ayeh-Kumi PF, Boakye DA, Bates PA (2015) First isolation of a new species of Leishmania responsible for human cutaneous leishmaniasis in Ghana and classification in the Leishmania enriettii complex. Int J Parasitol 45(11):679–684. https://doi.org/10.1016/j.ijpara.2015.05.001
Waki K, Dutta S, Ray D, Kolli BK, Akman L, Kawazu S, Lin CP, Chang KP (2007) Transmembrane molecules for phylogenetic analyses of pathogenic protists: Leishmania-specific informative sites in hydrophilic loops of trans- endoplasmic reticulum N-acetylglucosamine-1-phosphate transferase. Eukaryot Cell 6(2):198–210. https://doi.org/10.1128/ec.00282-06
Luyo-Acero GE, Uezato H, Oshiro M, Takei K, Kariya K, Katakura K, Gomez-Landires E, Hashiguchi Y, Nonaka S (2004) Sequence variation of the cytochrome b gene of various human infecting members of the genus Leishmania and their phylogeny. Parasitology 128(Pt 5):483–491
Kato H, Uezato H, Gomez EA, Terayama Y, Calvopina M, Iwata H, Hashiguchi Y (2007) Establishment of a mass screening method of sandfly vectors for Leishmania infection by molecular biological methods. Am J Trop Med Hyg 77(2):324–329
Foulet F, Botterel F, Buffet P, Morizot G, Rivollet D, Deniau M, Pratlong F, Costa JM, Bretagne S (2007) Detection and identification of Leishmania species from clinical specimens by using a real-time PCR assay and sequencing of the cytochrome B gene. J Clin Microbiol 45(7):2110–2115. https://doi.org/10.1128/jcm.02555-06
Asato Y, Oshiro M, Myint CK, Yamamoto Y, Kato H, Marco JD, Mimori T, Gomez EA, Hashiguchi Y, Uezato H (2009) Phylogenic analysis of the genus Leishmania by cytochrome b gene sequencing. Exp Parasitol 121(4):352–361. https://doi.org/10.1016/j.exppara.2008.12.013
Yang BB, Chen DL, Chen JP, Liao L, Hu XS, Xu JN (2013) Analysis of kinetoplast cytochrome b gene of 16 Leishmania isolates from different foci of China: different species of Leishmania in China and their phylogenetic inference. Parasit Vectors 6:32. https://doi.org/10.1186/1756-3305-6-32
Lopes EG, Geraldo Junior CA, Marcili A, Silva RD, Keid LB, Oliveira TM, Soares RM (2016) Performance of conventional PCRs based on primers directed to nuclear and mitochondrial genes for the detection and identification of Leishmania spp. Rev Inst Med Trop Sao Paulo 58:41. https://doi.org/10.1590/s1678-9946201658041
Leelayoova S, Siripattanapipong S, Manomat J, Piyaraj P, Tan-Ariya P, Bualert L, Mungthin M (2017) Leishmaniasis in Thailand: a review of causative agents and situations. Am J Trop Med Hyg 96(3):534–542. https://doi.org/10.4269/ajtmh.16-0604
Ibrahim ME, Barker DC (2001) The origin and evolution of the Leishmania donovani complex as inferred from a mitochondrial cytochrome oxidase II gene sequence. Infect Genet Evol 1(1):61–68
Cao DP, Guo XG, Chen DL, Chen JP (2011) Species delimitation and phylogenetic relationships of Chinese Leishmania isolates reexamined using kinetoplast cytochrome oxidase II gene sequences. Parasitol Res 109(1):163–173. https://doi.org/10.1007/s00436-010-2239-6
Zelazny AM, Fedorko DP, Li L, Neva FA, Fischer SH (2005) Evaluation of 7SL RNA gene sequences for the identification of Leishmania spp. Am J Trop Med Hyg 72(4):415–420
Stevenson LG, Fedorko DP, Zelazny AM (2010) An enhanced method for the identification of Leishmania spp. using real-time polymerase chain reaction and sequence analysis of the 7SL RNA gene region. Diagn Microbiol Infect Dis 66(4):432–435. https://doi.org/10.1016/j.diagmicrobio.2009.11.005
Van der Auwera G, Ravel C, Verweij JJ, Bart A, Schönian G, Felger I (2014) Evaluation of four single-locus markers for Leishmania species discrimination by sequencing. J Clin Microbiol 52(4):1098–1104. https://doi.org/10.1128/jcm.02936-13
Podlipaev SA, Sturm NR, Fiala I, Fernandes O, Westenberger SJ, Dollet M, Campbell DA, Lukeš J (2004) Diversity of insect trypanosomatids assessed from the spliced leader RNA and 5S rRNA genes and intergenic regions. J Eukaryot Microbiol 51(3):283–290
Marfurt J, Nasereddin A, Niederwieser I, Jaffe CL, Beck HP, Felger I (2003) Identification and differentiation of Leishmania species in clinical samples by PCR amplification of the miniexon sequence and subsequent restriction fragment length polymorphism analysis. J Clin Microbiol 41(7):3147–3153
Mauricio IL, Stothard JR, Miles MA (2004) Leishmania donovani complex: genotyping with the ribosomal internal transcribed spacer and the mini-exon. Parasitology 128(Pt 3):263–267
Votýpka J, Maslov DA, Yurchenko V, Jirků M, Kment P, Lun ZR, Lukeš J (2010) Probing into the diversity of trypanosomatid flagellates parasitizing insect hosts in South-West China reveals both endemism and global dispersal. Mol Phylogenet Evol 54(1):243–253. https://doi.org/10.1016/j.ympev.2009.10.014
Roelfsema JH, Nozari N, Herremans T, Kortbeek LM, Pinelli E (2011) Evaluation and improvement of two PCR targets in molecular typing of clinical samples of Leishmania patients. Exp Parasitol 127(1):36–41. https://doi.org/10.1016/j.exppara.2010.06.024
Fraga J, Montalvo AM, Van der Auwera G, Maes I, Dujardin JC, Requena JM (2013) Evolution and species discrimination according to the Leishmania heat-shock protein 20 gene. Infect Genet Evol 18:229–237. https://doi.org/10.1016/j.meegid.2013.05.020
Garcia L, Kindt A, Bermudez H, Llanos-Cuentas A, De Doncker S, Arevalo J, Wilber Quispe Tintaya K, Dujardin JC (2004) Culture-independent species typing of neotropical Leishmania for clinical validation of a PCR-based assay targeting heat shock protein 70 genes. J Clin Microbiol 42(5):2294–2297
Fraga J, Montalvo AM, De Doncker S, Dujardin JC, Van der Auwera G (2010) Phylogeny of Leishmania species based on the heat-shock protein 70 gene. Infect Genet Evol 10(2):238–245. https://doi.org/10.1016/j.meegid.2009.11.007
da Silva LA, de Sousa Cdos S, da Graca GC, Porrozzi R, Cupolillo E (2010) Sequence analysis and PCR-RFLP profiling of the hsp70 gene as a valuable tool for identifying Leishmania species associated with human leishmaniasis in Brazil. Infect Genet Evol 10(1):77–83. https://doi.org/10.1016/j.meegid.2009.11.001
Montalvo AM, Fraga J, Monzote L, Montano I, De Doncker S, Dujardin JC, Van der Auwera G (2010) Heat-shock protein 70 PCR-RFLP: a universal simple tool for Leishmania species discrimination in the New and Old World. Parasitology 137(8):1159–1168. https://doi.org/10.1017/s0031182010000089
Odiwuor S, Veland N, Maes I, Arevalo J, Dujardin JC, Van der Auwera G (2012) Evolution of the Leishmania braziliensis species complex from amplified fragment length polymorphisms, and clinical implications. Infect Genet Evol 12(8):1994–2002. https://doi.org/10.1016/j.meegid.2012.03.028
Montalvo AM, Fraga J, Maes I, Dujardin JC, Van der Auwera G (2012) Three new sensitive and specific heat-shock protein 70 PCRs for global Leishmania species identification. Eur J Clin Microbiol Infect Dis 31(7):1453–1461. https://doi.org/10.1007/s10096-011-1463-z
Van der Auwera G, Maes I, De Doncker S, Ravel C, Cnops L, Van Esbroeck M, Van Gompel A, Clerinx J, Dujardin JC (2013) Heat-shock protein 70 gene sequencing for Leishmania species typing in European tropical infectious disease clinics. Euro Surveill 18(30):20543
Cupolillo E, Grimaldi Jr G, Momen H, Beverly S (1995) Intergenic region typing (IRT): A rapid molecular approach to the characterization and evolution of Leishmania. Mol Biochem Parasitol 73:145–155
Mauricio IL, Gaunt MW, Stothard JR, Miles MA (2007) Glycoprotein 63 (gp63) genes show gene conversion and reveal the evolution of Old World Leishmania. Int J Parasitol 37(5):565–576
Guerbouj S, Victoir K, Guizani I, Seridi N, Nuwayri-Salti N, Belkaid M, Ben Ismail R, Le Ray D, Dujardin JC (2001) Gp63 gene polymorphism and population structure of Leishmania donovani complex: influence of the host selection pressure? Parasitology 122:25–35
Victoir K, De Doncker S, Cabrera L, Alvarez E, Arevalo J, Llanos-Cuentas A, Le Ray D, Dujardin JC (2003) Direct identification of Leishmania species in biopsies from patients with American tegumentary leishmaniasis. Trans R Soc Trop Med Hyg 97:80–87
Victoir K, Bañuls AL, Arevalo J, Lllanos-Cuentas A, Hamers R, Noël S, de Doncker S, Le Ray D, Tibayrenc M, Dujardin JC (1998) The gp63 gene locus, a target for genetic characterization of Leishmania belonging to the subgenus Viannia. Parasitology 117:1–113
Garcia AL, Kindt A, Quispe-Tintaya KW, Bermudez H, Llanos A, Arevalo J, Bañuls AL, De Doncker S, Le Ray D, Dujardin JC (2005) American tegumentary leishmanisis: antigene polymorphism, taxonomy and clinical pleomorphism. Inf Gen Evol 5:109–111
Quispe-Tintaya KW, Ying X, Dedet JP, Rijal S, De Bolle X, Dujardin JC (2004) Antigen genes for molecular epidemiology of leishmaniasis: polymorphism of cystein protease b and surface metalloprotease glycoprotein 63 in the Leishmania donovani complex. J Inf Dis 189:1035–1043
Spanakos G, Patsoula E, Kremastinou T, Saroglou G, Vakalis N (2002) Development of a PCR-based method for diagnosis of Leishmania in blood samples. Molecular and Cellular Probes 16: 415–420 https://doi.org/10.1006/mcpr.2002.0436
Fernandes O, Temeira MMG, Sturm NR, Sousa MA, Camargo EP, Degrave WM, Campbell DA (1997) Miniexon gene sequences define six groups within the genus Crithidia. J Euk Microbiol 44(6):535–539
Fernandes O, Murthy VK, Kurath U, Degrave WM, Campbell DA (1994) Mini-exon gene variation in human pathogenic Leishmania species. Mol Biochem Parasitol 66: 261–271
Akman L, Aksu HSZ, Wang RQ, Ozensoy S, Ozbel Y, Alkan Z, Ozcel MA, Culha G, Ozcan K, Uzun S, Memisoglu HR, Chang KP (2000) Multi-site DNA polymorphism analyses of Leishmania isolates define their genotypes predicting clinical epidemiology of Leishmaniasis in a specific region. J Eukaryot Microbiol 47(6):545–554
Gonzalez-Aseguinolaza G, Taladriz S, Marquet A, Larraga V (1999) Molecular cloning, cell localization and binding affinity to DNA replication proteins of the p36/LACK protective antigen from Leishmania infantum. Eur J Biochem 259:909–916.
Davila AM, Momen H (2000) Internal-transcribed-spacer (ITS) sequences used to explore phylogenetic relationships within Leishmania. Ann Trop Med Parasitol 94(6):651–654
El Tai NO, El Fari M, Mauricio I, Miles MA, Oskam L, El Safi SH, Presber WH, Schönian G (2001) Leishmania donovani: intraspecific polymorphisms of Sudanese isolates revealed by PCR-based analyses and DNA sequencing. Exp Parasitol 97(1):35–44. https://doi.org/10.1006/expr.2001.4592
Berzunza-Cruz M, Cabrera N, Crippa-Rossi M, Sosa Cabrera T, Perez-Montfort R, Becker I (2002) Polymorphism analysis of the internal transcribed spacer and small subunit of ribosomal RNA genes of Leishmania mexicana. Parasitol Res 88(10):918–925. https://doi.org/10.1007/s00436-002-0672-x
Kuhls K, Mauricio IL, Pratlong F, Presber W, Schönian G (2005) Analysis of ribosomal DNA internal transcribed spacer sequences of the Leishmania donovani complex. Microbes Infect 7(11-12):1224–1234. https://doi.org/10.1016/j.micinf.2005.04.009
Spanakos G, Patsoula E, Kremastinou T, Saroglou G, Vakalis N (2002) Development of a PCR-based method for diagnosis of Leishmania in blood samples. Molecular and Cellular Probes 16: 415–420 https://doi.org/10.1006/mcpr.2002.0436
Spanakos G, Piperaki ET, Menounos PG, Tegos N, Flemetakis A, Vakalis NC (2008) Detection and species identification of Old World Leishmania in clinical samples using a PCR-based method. Trans R Soc Trop Med Hyg 102(1):46–53. https://doi.org/10.1016/j.trstmh.2007.05.019
Parvizi P, Ready PD (2008) Nested PCRs and sequencing of nuclear ITS-rDNA fragments detect three Leishmania species of gerbils in sandflies from Iranian foci of zoonotic cutaneous leishmaniasis. Trop Med Int Health 13(9):1159–1171. https://doi.org/10.1111/j.1365-3156.2008.02121.x
de Almeida ME, Steurer FJ, Koru O, Herwaldt BL, Pieniazek NJ, da Silva AJ (2011) Identification of Leishmania spp. by molecular amplification and DNA sequencing analysis of a fragment of rRNA internal transcribed spacer 2. J Clin Microbiol 49(9):3143–3149. https://doi.org/10.1128/jcm.01177-11
Uliana SR, Nelson K, Beverley SM, Camargo EP, Floeter-Winter LM (1994) Discrimination amongst Leishmania by polymerase chain reaction and hybridization with small subunit ribosomal DNA derived oligonucleotides. J Eukaryot Microbiol 41(4):324–330
Bualert L, Charungkiattikul W, Thongsuksai P, Mungthin M, Siripattanapipong S, Khositnithikul R, Naaglor T, Ravel C, El Baidouri F, Leelayoova S (2012) Autochthonous disseminated dermal and visceral leishmaniasis in an AIDS patient, southern Thailand, caused by Leishmania siamensis. Am J Trop Med Hyg 86(5):821–824. https://doi.org/10.4269/ajtmh.2012.11-0707
Meredith SE, Zijlstra EE, Schoone GJ, Kroon CC, van Eys GJ, Schaeffer KU, el-Hassan AM, Lawyer PG (1993) Development and application of the polymerase chain reaction for the detection and identification of Leishmania parasites in clinical material. Arch Inst Pasteur Tunis 70(3-4):419–431
Schönian G, Nasereddin A, Dinse N, Schweynoch C, Schallig HD, Presber W, Jaffe CL (2003) PCR diagnosis and characterization of Leishmania in local and imported clinical samples. Diagn Microbiol Infect Dis 47(1):349–358
Da Silva FM, Noyes H, Campaner M, Junqueira AC, Coura JR, Anez N, Shaw JJ, Stevens JR, Teixeira MM (2004) Phylogeny, taxonomy and grouping of Trypanosoma rangeli isolates from man, triatomines and sylvatic mammals from widespread geographical origin based on SSU and ITS ribosomal sequences. Parasitology 129(Pt 5):549–561
El Tai NO, Osman OF, el Fari M, Presber W, Schönian G (2000) Genetic heterogeneity of ribosomal internal transcribed spacer in clinical samples of Leishmania donovani spotted on filter paper as revealed by single-strand conformation polymorphisms and sequencing. Trans R Soc Trop Med Hyg 94(5):575–579
Croan D, Ellis J (1997) Monophyletic origin of the genus Sauroleishmania. Arch Protistenkd 148:269–275
Hannaert V, Opperdoes FR, Michels PA (1998) Comparison and evolutionary analysis of the glycosomal glyceraldehyde-3-phosphate dehydrogenase from different Kinetoplastida. J Mol Evol 47(6):728–738
Looker D, Miller LA, Elwood HJ, Stickel S, Sogin ML (1988) Primary structure of the Leishmania donovani small subunit ribosomal RNA coding region. Nucleic Acids Res 16(14b):7198
Mauricio IL, Yeo M, Baghaei M, Doto D, Pratlong F, Zemanová E, Dedet JP, Lukeš J, Miles MA (2006) Towards multilocus sequence typing of the Leishmania donovani complex: resolving genotypes and haplotypes for five polymorphic metabolic enzymes (ASAT, GPI, NH1, NH2, PGD). Int J Parasitol 36(7):757–769. https://doi.org/10.1016/j.ijpara.2006.03.006
Herrera G, Hernandez C, Ayala MS, Florez C, Teheran AA, Ramirez JD (2017) Evaluation of a multilocus sequence typing (MLST) scheme for Leishmania (Viannia) braziliensis and Leishmania (Viannia) panamensis in Colombia. Parasit Vectors 10(1):236. https://doi.org/10.1186/s13071-017-2175-8
Tsukayama P, Lucas C, Bacon DJ (2009) Typing of four genetic loci discriminates among closely related species of New World Leishmania. Int J Parasitol 39(3):355–362. https://doi.org/10.1016/j.ijpara.2008.08.004
Zhang CY, Lu XJ, Du XQ, Jian J, Shu L, Ma Y (2013) Phylogenetic and evolutionary analysis of Chinese Leishmania isolates based on multilocus sequence typing. PLoS One 8(4):e63124. https://doi.org/10.1371/journal.pone.0063124
Boité MC, Mauricio IL, Miles MA, Cupolillo E (2012) New insights on taxonomy, phylogeny and population genetics of Leishmania (Viannia) parasites based on multilocus sequence analysis. PLoS Negl Trop Dis 6(11):e1888. https://doi.org/10.1371/journal.pntd.0001888
Marlow MA, Boité MC, Ferreira GE, Steindel M, Cupolillo E (2014) Multilocus sequence analysis for Leishmania braziliensis outbreak investigation. PLoS Negl Trop Dis 8(2):e2695. https://doi.org/10.1371/journal.pntd.0002695
Zemanová E, Jirků M, Mauricio IL, Horák A, Miles MA, Lukeš J (2007) The Leishmania donovani complex: genotypes of five metabolic enzymes (ICD, ME, MPI, G6PDH, and FH), new targets for multilocus sequence typing. Int J Parasitol 37(2):149–160. https://doi.org/10.1016/j.ijpara.2006.08.008
Marco JD, Barroso PA, Locatelli FM, Cajal SP, Hoyos CL, Nevot MC, Lauthier JJ, Tomasini N, Juarez M, Estevez JO, Korenaga M, Nasser JR, Hashiguchi Y, Ruybal P (2015) Multilocus sequence typing approach for a broader range of species of Leishmania genus: describing parasite diversity in Argentina. Infect Genet Evol 30:308–317. https://doi.org/10.1016/j.meegid.2014.12.031
El Baidouri F, Diancourt L, Berry V, Chevenet F, Pratlong F, Marty P, Ravel C (2013) Genetic structure and evolution of the Leishmania genus in Africa and Eurasia: what does MLSA tell us. PLoS Negl Trop Dis 7(6):e2255. https://doi.org/10.1371/journal.pntd.0002255
Chaara D, Ravel C, Bañuls A, Haouas N, Lami P, Talignani L, El Baidouri F, Jaouadi K, Harrat Z, Dedet JP, Babba H, Pratlong F (2015) Evolutionary history of Leishmania killicki (synonymous Leishmania tropica) and taxonomic implications. Parasit Vectors 8:198. https://doi.org/10.1186/s13071-015-0821-6
Shaw J, Pratlong F, Floeter-Winter L, Ishikawa E, El Baidouri F, Ravel C, Dedet JP (2015) Characterization of Leishmania (Leishmania) waltoni n.sp. (Kinetoplastida: Trypanosomatidae), the parasite responsible for diffuse cutaneous leishmaniasis in the Dominican Republic. Am J Trop Med Hyg 93(3):552–558. https://doi.org/10.4269/ajtmh.14-0774
Lukeš J, Mauricio IL, Schönian G, Dujardin JC, Soteriadou K, Dedet JP, Kuhls K, Tintaya KW, Jirků M, Chocholová E, Haralambous C, Pratlong F, Oborník M, Horák A, Ayala FJ, Miles MA (2007) Evolutionary and geographical history of the Leishmania donovani complex with a revision of current taxonomy. Proc Natl Acad Sci U S A 104(22):9375–9380
Miles MA, Llewellyn MS, Lewis MD, Yeo M, Baleela R, Fitzpatrick S, Gaunt MW, Mauricio IL (2009) The molecular epidemiology and phylogeography of Trypanosoma cruzi and parallel research on Leishmania: looking back and to the future. Parasitology 136(12):1509–1528. https://doi.org/10.1017/s0031182009990977
Downing T, Stark O, Vanaerschot M, Imamura H, Sanders M, Decuypere S, de Doncker S, Maes I, Rijal S, Sundar S, Dujardin JC, Berriman M, Schönian G (2012) Genome-wide SNP and microsatellite variation illuminate population-level epidemiology in the Leishmania donovani species complex. Infect Genet Evol 12(1):149–159. https://doi.org/10.1016/j.meegid.2011.11.005
Imamura H, Downing T, Van den Broeck F, Sanders MJ, Rijal S, Sundar S, Mannaert A, Vanaerschot M, Berg M, De Muylder G, Dumetz F, Cuypers B, Maes I, Domagalska M, Decuypere S, Rai K, Uranw S, Bhattarai NR, Khanal B, Prajapati VK, Sharma S, Stark O, Schönian G, De Koning HP, Settimo L, Vanhollebeke B, Roy S, Ostyn B, Boelaert M, Maes L, Berriman M, Dujardin JC, Cotton JA (2016) Evolutionary genomics of epidemic visceral leishmaniasis in the Indian subcontinent. eLife 5. https://doi.org/10.7554/eLife.12613
Harkins KM, Schwartz RS, Cartwright RA, Stone AC (2016) Phylogenomic reconstruction supports supercontinent origins for Leishmania. Infect Genet Evol 38:101–109. https://doi.org/10.1016/j.meegid.2015.11.030
Lukeš J, Butenko A, Hashimi H, Maslov DA, Votýpka J, Yurchenko V (2018) Trypanosomatids are much more than just trypanosomes: clues from the expanded family tree. Trends Parasitol. https://doi.org/10.1016/j.pt.2018.03.002
Villinski JT, Klena JD, Abbassy M, Hoel DF, Puplampu N, Mechta S, Boakye D, Raczniak G (2008) Evidence for a new species of Leishmania associated with a focal disease outbreak in Ghana. Diagn Microbiol Infect Dis 60(3):323–327. https://doi.org/10.1016/j.diagmicrobio.2007.09.013
Stevens JR, Gibson WC (1999) The evolution of pathogenic trypanosomes. Cad Saude Publica 15(4):673–684
Kaufer A, Ellis J, Stark D, Barratt J (2017) The evolution of trypanosomatid taxonomy. Parasit Vectors 10(1):287. https://doi.org/10.1186/s13071-017-2204-7
Rahbarian N, Mesgarian A, Mahmoudi Rad M, Hajaran H, Shahbazi F, Mesgarian Z, Taghipour N (2009) Identification of Leishmania species isolated from human cutaneous leishmaniasis using PCR method. J Res Health Sci 9(2):48–51
Kostygov AY, Yurchenko V (2017) Revised classification of the subfamily Leishmaniinae (Trypanosomatidae). Folia Parasitol 64. https://doi.org/10.14411/fp.2017.020
Nascimento FF, dos Reis M, Yang Z (2017) A biologist’s guide to Bayesian phylogenetic analysis. Nat Ecol Evol 1(10):1446–1454. https://doi.org/10.1038/s41559-017-0280-x
Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35(6):1547–1549. https://doi.org/10.1093/molbev/msy096
Hamarsheh O, Presber W, Abdeen Z, Sawalha S, Al-Lahem A, Schönian G (2007) Genetic structure of Mediterranean populations of the sandfly Phlebotomus papatasi by mitochondrial cytochrome b haplotype analysis. Med Vet Entomol 21(3):270–277. https://doi.org/10.1111/j.1365-2915.2007.00695.x
Savani ES, Nunes VL, Galati EA, Castilho TM, Araujo FS, Ilha IM, Camargo MC, D'Auria SR, Floeter-Winter LM (2005) Occurrence of co-infection by Leishmania (Leishmania) chagasi and Trypanosoma (Trypanozoon) evansi in a dog in the state of Mato Grosso do Sul, Brazil. Mem Inst Oswaldo Cruz 100(7):739–741. doi:/s0074-02762005000700011
Thompson JD, Higgins DG, Gibson TJ (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(22):4673–4680
Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32(5):1792–1797. https://doi.org/10.1093/nar/gkh340
Katoh K, Misawa K, Kuma K-i, Miyata T (2002) MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res 30(14):3059–3066
Notredame C, Higgins DG, Heringa J (2000) T-coffee: a novel method for fast and accurate multiple sequence alignment. J Mol Biol 302(1):205–217. https://doi.org/10.1006/jmbi.2000.4042
Löytynoja A, Goldman N (2010) webPRANK: a phylogeny-aware multiple sequence aligner with interactive alignment browser. BMC Bioinformatics 11(1):579. https://doi.org/10.1186/1471-2105-11-579
Gouveia-Oliveira R, Sackett PW, Pedersen AG (2007) MaxAlign: maximizing usable data in an alignment. BMC Bioinformatics 8(1):312. https://doi.org/10.1186/1471-2105-8-312
Hall TA (1999) {BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT}. In: Nucleic acids symposium series. pp. 95–98. doi:citeulike-article-id:6807604
Huson DH, Bryant D (2006) Application of phylogenetic networks in evolutionary studies. Mol Biol Evol 23(2):254–267. https://doi.org/10.1093/molbev/msj030
Kück P, Mayer C, Wägele J-W, Misof B (2012) Long branch effects distort maximum likelihood phylogenies in simulations despite selection of the correct model. PLoS One 7(5):e36593. https://doi.org/10.1371/journal.pone.0036593
Bergsten J (2005) A review of long-branch attraction. Cladistics 21(2):163–163-193. https://doi.org/10.1111/j.1096-0031.2005.00059.x
Felsenstein J (2005) PHYLIP (Phylogeny Inference Package) version 3.6. Distributed by the author. Department of Genome Sciences, University of Washington, Seattle
Swofford DL (1998) PAUP*. Phylogenetic Analysis Using Parsimony (*and Other Methods). Version 4. Sinauer Associates, Sunderland, Massachusetts
Drummond AJ, Suchard MA, Xie D, Rambaut A (2012) Bayesian Phylogenetics with BEAUti and the BEAST 1.7. Mol Biol Evol 29(8):1969–1973. https://doi.org/10.1093/molbev/mss075
Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP (2012) MrBayes 3.2: efficient bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61(3):539–542. https://doi.org/10.1093/sysbio/sys029
Tajima F (1993) Simple methods for testing the molecular evolutionary clock hypothesis. Genetics 135(2):599–607
Bandelt H-J, Dress AWM (1992) Split decomposition: a new and useful approach to phylogenetic analysis of distance data. Mol Phylogenet Evol 1(3):242–252. https://doi.org/10.1016/1055-7903(92)90021-8
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2019 Springer Science+Business Media, LLC, part of Springer Nature
About this protocol
Cite this protocol
Kuhls, K., Mauricio, I. (2019). Phylogenetic Studies. In: Clos, J. (eds) Leishmania. Methods in Molecular Biology, vol 1971. Humana Press, New York, NY. https://doi.org/10.1007/978-1-4939-9210-2_2
Download citation
DOI: https://doi.org/10.1007/978-1-4939-9210-2_2
Published:
Publisher Name: Humana Press, New York, NY
Print ISBN: 978-1-4939-9209-6
Online ISBN: 978-1-4939-9210-2
eBook Packages: Springer Protocols