Absence of genetic structure in Baylisascaris schroederi populations, a giant panda parasite, determined by mitochondrial sequencing

Particle and Fibre Toxicology

Guangyou Yang¹  Xuerong Peng⁴  Tao Wang¹  Xiaobin Gu¹  Tianyu Liu¹  Yun Sun¹  Chengdong Wang³  Zhihe Zhang³  Xuan Zhou²  Yue Xie¹ 

[1]Department of Parasitology, College of Veterinary Medicine, Sichuan Agricultural University, Ya’an 625014, China

[2]Centre for Animal Diseases Control and Prevention, Dachuan Animal Husbandry Bureau, Dazhou 623000, China

[3]Chengdu Research Base of Giant Panda Breeding, Chengdu 610081, China

[4]Department of Chemistry, College of Life and Basic Science, Sichuan Agricultural University, Ya’an 625014, China

关键词: Mitochondrial cox1;    Mitochondrial atp6;    Genetic diversity;    Roundworm;    Ailuropoda melanoleuca;   

Others  :  1148188
DOI  :  10.1186/s13071-014-0606-3

 received in 2014-11-11, accepted in 2014-12-16,  发布年份 2014

【 摘 要 】

Background

Infection with the parasitic nematode, Baylisascaris schroederi (Ascaridida: Nematoda), is one of the most important causes of death in giant pandas, and was responsible for half of deaths between 2001 and 2005. Mitochondrial (mt) DNA sequences of parasites can unveil their genetic diversity and depict their likely dynamic evolution and therefore may provide insights into parasite survival and responses to host changes, as well as parasite control.

Methods

Based on previous studies, the present study further annotated the genetic variability and structure of B. schroederi populations by combining two different mtDNA markers, ATPase subunit 6 (atp6) and cytochrome c oxidase subunit I (cox1). Both sequences were completely amplified and genetically analyzed among 57 B. schroederi isolates, which were individually collected from ten geographical regions located in three important giant panda habitats in China (Minshan, Qionglai and Qinling mountain ranges).

Results

For the DNA dataset, we identified 20 haplotypes of atp6, 24 haplotypes of cox1, and 39 haplotypes of atp6 + cox1. Further haplotype network and phylogenetic analyses demonstrated that B. schroederi populations were predominantly driven by three common haplotypes, atp6 A1, cox1 C10, and atp6 + cox1 H11. However, due to low rates of gene differentiation between the three populations, both the atp6 and cox1 genes appeared not to be significantly associated with geographical divisions. In addition, high gene flow was detected among the B. schroederi populations, consistent with previous studies, suggesting that this parasite may be essentially homogenous across endemic areas. Finally, neutrality tests and mismatch analysis indicated that B. schroederi had undergone earlier demographic expansion.

Conclusions

These results confirmed that B. schroederi populations do not follow a pattern of isolation by distance, further revealing the possible existence of physical connections before geographic separation. This study should also contribute to an improved understanding of the population genetics and evolutionary biology of B. schroederi and assist in the control of baylisascariasis in giant pandas.

【 授权许可】

   
2014 Xie et al.; licensee BioMed Central.

【 图 表 】

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【 参考文献 】

• [1]Ling DI, Zwerling AA, Pai M: GenoType MTBDR assays for the diagnosis of multidrug-resistant tuberculosis: a meta-analysis. Eur Respir J 2008, 32:1165-1174.
• [2]Small PM, Hopewell PC, Singh SP, Paz A, Parsonnet J, Ruston DC, Schecter GF, Daley CL, Schoolnik GK: The epidemiology of tuberculosis in San Francisco–a population-based study using conventional and molecular methods. N Engl J Med 1994, 330:1703-1709.
• [3]Brudey K, Driscoll JR, Rigouts L, Prodinger WM, Gori A, Al-Hajoj SA, Allix C, Aristimuño L, Arora J, Baumanis V, Binder L, Cafrune P, Cataldi A, Cheong S, Diel R, Ellermeier C, Evans JT, Fauville-Dufaux M, Ferdinand S, Garcia de Viedma D, Garzelli C, Gazzola L, Gomes HM, Guttierez MC, Hawkey PM, van Helden PD, Kadival GV, Kreiswirth BN, Kremer K, Kubin M, et al: Mycobacterium tuberculosis complex genetic diversity: mining the fourth international spoligotyping database (SpolDB4) for classification, population genetics and epidemiology.BMC Microbiol 2006, 6:23.
• [4]Gasser RB, Jabbar A, Mohandas N, Schnyder M, Deplazes P, Littlewood DTJ, Jex AR: Mitochondrial genome of Angiostrongylus vasorum: Comparison with congeners and implications for studying the population genetics and epidemiology of this parasite. Infect Genet Evol 2012, 12:1884-1891.
• [5]Mas-Coma S, Valero MA, Bargues MD: Fasciola, lymnaeids and human fascioliasis, with a global overview on disease transmission, epidemiology, evolutionary genetics, molecular epidemiology and control. Adv Parasitol 2009, 69:41-146.
• [6]Betson M, Nejsum P, Bendall RP, Deb RM, Stothard JR: Molecular epidemiology of ascariasis: a global perspective on the transmission dynamics of Ascaris in people and pigs. J Infect Dis 2014, 210:932-941.
• [7]Barrett LG, Thrall PH, Burdon JJ, Linde CC: Life history determines genetic structure and evolutionary potential of host-parasite interactions. Trends Ecol Evol 2008, 23:678-685.
• [8]Blouin MS, Yowell CA, Courtney CH, Dame JB: Host movement and the genetic structure of populations of parasitic nematodes. Genetics 1995, 141:1007-1014.
• [9]Frankham R, Briscoe D, Ballou J: Introduction to Conservation Genetics. Cambridge University Press, Cambridge; 2002.
• [10]Simon C, Frati F, Beckenbach A, Crespi B, Liu H, Flook P: Evolution, weighting, and phylogenetic utility of mitochondrial gene sequences and a compilation of conserved polymerase chain reaction primers. Ann Entomol Soc Am 1994, 87:651-701.
• [11]Sunnucks P: Efficient genetic markers for population biology. Trends Ecol Evol 2000, 15:199-203.
• [12]Farias IP, Ortí G, Sampaio I, Schneider H, Meyer A: The cytochrome b gene as a phylogenetic marker: the limits of resolution for analyzing relationships among cichlid fishes. J Mol Evol 2001, 53:89-103.
• [13]Franssen F, Xie K, Sprong H, van der Giessen J: Molecular analysis of Baylisascaris columnaris revealed mitochondrial and nuclear polymorphisms.Parasit Vectors 2013, 6:124.
• [14]Höglund J, Morrison D, Mattsson J, Engström A: Population genetics of the bovine/cattle lungworm (Dictyocaulus viviparus) based on mtDNA and AFLP marker techniques. Parasitology 2006, 133:89-99.
• [15]Troell K, Engström A, Morrison DA, Mattsson JG, Höglund J: Global patterns reveal strong population structure in Haemonchus contortus, a nematode parasite of domesticated ruminants. Int J Parasitol 2006, 36:1305-1316.
• [16]Yin F, Gasser RB, Li F, Bao M, Huang W, Zou F, Zhao G, Wang C, Yang X, Zhou Y, Zhao J, Fang R, Hu M: Genetic variability within and among Haemonchus contortus isolates from goats and sheep in China.Parasit Vectors 2013, 6:279.
• [17]Iñiguez AM, Leles D, Jaeger LH, Carvalho-Costa FA, Araújo A: Amazonas Research Group: Genetic characterisation and molecular epidemiology of Ascaris spp. from humans and pigs in Brazil. Trans R Soc Trop Med Hyg 2012, 106:604-612.
• [18]Zhou X, Xie Y, Zhang ZH, Wang CD, Sun Y, Gu XB, Wang SX, Peng XR, Yang GY: Analysis of the genetic diversity of the nematode parasite Baylisascaris schroederi from wild giant pandas in different mountain ranges in China.Parasit Vectors 2013, 6:233.
• [19]Zhang ZH, Wei FW: Giant Panda: Ex-Situ Conservation Theory and Practice. Science Press, Beijing; 2006.
• [20]State Forestry Administration: The Third National Survey Report on Giant Panda in China. Chinese Science Press House, Beijing; 2006.
• [21]Xie Y, Zhang Z, Wang C, Lan J, Li Y, Chen Z, Fu Y, Nie H, Yan N, Gu X, Wang S, Peng X, Yang G: Complete mitochondrial genomes of Baylisascaris schroederi, Baylisascaris ailuri and Baylisascaris transfuga from giant panda, red panda and polar bear. Gene 2011, 482:59-67.
• [22]Yang GY, Zhang ZH: Parasitic Diseases of Wildlife. Science Press, Beijing; 2013.
• [23]Loeffler K, Montali R, Rideout B: Diseases and pathology of giant pandas. In Giant Pandas: Biology, Veterinary Medicine and Management. Edited by Wildt DE, Zhang AJ, Zhang HM, Janssen DL, Ellis S. Cambridge University Press, Cambridge; 2006:377-409.
• [24]Wang T, He G, Yang G, Fei Y, Zhang Z, Wang C, Yang Z, Lan J, Luo L, Liu L: Cloning, expression and evaluation of the efficacy of a recombinant Baylisascaris schroederi Bs-Ag3 antigen in mice. Vaccine 2008, 26:6919-6924.
• [25]Lin Q, Li H, Gao M, Wang X, Ren W, Cong M, Tan X, Chen C, Yu S, Zhao G: Characterization of Baylisascaris schroederi from Qinling subspecies of giant panda in China by the first internal transcribed spacer (ITS-1) of nuclear ribosomal DNA. Parasitol Res 2012, 110:1297-1303.
• [26]McIntosh A: A new nematode, Ascaris schroederi, from a giant panda, Ailuropoda melanoleuca. Zoologica 1939, 24:355-357.
• [27]Sprent JF: Notes on Ascaris and Toxascaris, with a definition of Baylisascaris gen. nov. Parasitology 1968, 58:185-198.
• [28]Xie Y, Chen S, Yan Y, Zhang Z, Li D, Yu H, Wang C, Nong X, Zhou X, Gu X, Wang S, Peng X, Yang G: Potential of recombinant inorganic pyrophosphatase antigen as a new vaccine candidate against Baylisascaris schroederi in mice.Vet Res 2013, 44:90.
• [29]Zhao GH, Li HM, Ryan UM, Cong MM, Hu B, Gao M, Ren WX, Wang XY, Zhang SP, Lin Q, Zhu XQ, Yu SK: Phylogenetic study of Baylisascaris schroederi isolated from Qinling subspecies of giant panda in China based on combined nuclear 5.8S and the second internal transcribed spacer (ITS-2) ribosomal DNA sequences. Parasitol Int 2012, 61:497-500.
• [30]Zhao GH, Xu MJ, Zhu XQ: Identification and characterization of microRNAs in Baylisascaris schroederi of the giant panda.Parasit Vectors 2013, 6:216.
• [31]Hu M, Gasser RB: Mitochondrial genomes of parasitic nematodes–progress and perspectives. Trends Parasitol 2006, 22:78-84.
• [32]Jex AR, Littlewood DTJ, Gasser RB: Toward next-generation sequencing of mitochondrial genomes–focus on parasitic worms of animals and biotechnological implications. Biotechnol Adv 2010, 28:151-159.
• [33]Wang Y, Liu GH, Li JY, Xu MJ, Ye YG, Zhou DH, Song HQ, Lin RQ, Zhu XQ: Genetic variability among Trichuris ovis isolates from different hosts in Guangdong Province, China revealed by sequences of three mitochondrial genes. Mitochondrial DNA 2013, 24:50-54.
• [34]Thompson JD, Higgins DG, Gibson TJ: CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 1994, 22:4673-4680.
• [35]Castresana J: Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 2000, 17:540-552.
• [36]Falush D, Stephens M, Pritchard JK: Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 2003, 164:1567-1587.
• [37]Posada D: jModelTest: Phylogenetic model averaging. Mol Biol Evol 2008, 25:1253-1256.
• [38]Xia X, Lemey P: Assessing substitution saturation with DAMBE. Phylogen Handbook 2009, 2009:615-630.
• [39]Librado P, Rozas J: DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 2009, 25:1451-1452.
• [40]Bandelt HJ, Forster P, Röhl A: Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 1999, 16:37-48.
• [41]Excoffier L, Laval G, Schneider S: Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evol Bioinform Online 2007, 1:47-50.
• [42]Nei M: Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 1978, 89:583-590.
• [43]Wright S: The genetical structure of populations. Ann Eugen 1951, 15:323-354.
• [44]Hedrick PW: A standardized genetic differentiation measure. Evolution 2005, 59:1633-1638.
• [45]Fu YX: Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 1997, 147:915-925.
• [46]Schneider S, Excoffier L: Estimation of past demographic parameters from the distribution of pairwise differences when the mutation rates vary among sites: application to human mitochondrial DNA. Genetics 1999, 152:1079-1089.
• [47]Tajima F: Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 1989, 123:585-595.
• [48]Poulin R: Network analysis shining light on parasite ecology and diversity. Trends Parasitol 2010, 26:492-498.
• [49]Archie EA, Ezenwa VO: Population genetic structure and history of a generalist parasite infecting multiple sympatric host species. Int J Parasitol 2011, 41:89-98.
• [50]Höglund J, Morrison DA, Engström A, Nejsum P, Jansson DS: Population genetic structure of Ascaridia galli re-emerging in non-caged laying hens.Parasit Vectors 2012, 5:97.
• [51]Tydén E, Morrison D, Engström A, Nielsen M, Eydal M, Höglund J: Population genetics of Parascaris equorum based on DNA fingerprinting. Infect Genet Evol 2013, 13:236-241.
• [52]Hu M, Chilton NB, Gasser RB: The mitochondrial genomics of parasitic nematodes of socio-economic importance: recent progress, and implications for population genetics and systematics. Adv Parasitol 2004, 56:133-212.
• [53]Ngui R, Mahdy MA, Chua KH, Traub R, Lim YA: Genetic characterization of the partial mitochondrial cytochrome oxidase c subunit I (cox 1) gene of the zoonotic parasitic nematode, Ancylostoma ceylanicum from humans, dogs and cats. Acta Trop 2013, 128:154-157.
• [54]Blouin M: Mitochondrial DNA diversity in nematodes. J Helminthol 1998, 72:285-289.
• [55]Zhao S, Zheng P, Dong S, Zhan X, Wu Q, Guo X, Hu Y, He W, Zhang S, Fan W: Whole-genome sequencing of giant pandas provides insights into demographic history and local adaptation. Nat Genet 2013, 45:67-71.
• [56]Uddin W: Host Parasite Co-evolution: Case of nematode Parasites (Syphacia obvelata, Trichuris muris) and Host (Mus musculus) in Mouse Hybrid Zone. In: Current methods on speciation research: population genetic approaches, Průhonice, 2012.
• [57]Cutter AD, Payseur BA: Genomic signatures of selection at linked sites: unifying the disparity among species. Nat Rev Genet 2013, 14:262-274.
• [58]Anderson JL, Morran LT, Phillips PC: Outcrossing and the maintenance of males within C. elegans populations. J Hered 2010, 101:S62-S74.
• [59]Wildt DE, Zhang AJ, Zhang HM, Janssen DL, Ellis S: Giant Pandas: Biology, Veterinary Medicine and Management. Cambridge University Press, Cambridge; 2006.
• [60]Nejsum P, Frydenberg J, Roepstorff A, Parker ED Jr: Population structure in Ascaris suum (Nematoda) among domestic swine in Denmark as measured by whole genome DNA fingerprinting. Hereditas 2005, 142:7-14.
• [61]Zhou C, Yuan K, Tang X, Hu N, Peng W: Molecular genetic evidence for polyandry in Ascaris suum. Parasitol Res 2011, 108:703-708.
• [62]Posada D, Crandall KA: Intraspecific gene genealogies: trees grafting into networks. Trends Ecol Evol 2001, 16:37-45.
• [63]Anderson RM: Complex dynamic behaviours in the interaction between parasite populations and the host’s immune system. Int J Parasitol 1998, 28:551-566.
• [64]Louhi KR, Karvonen A, Rellstab C, Jokela J: Is the population genetic structure of complex life cycle parasites determined by the geographic range of the most motile host? Infect Genet Evol 2010, 10:1271-1277.
• [65]Bowen BW, Grant WS: Phylogeography of the sardines (Sardinops spp): assessing biogeographic models and population histories in temperate upwelling zones. Evolution 1997, 51:1601-1610.