Skip to main content
SpringerLink
Log in

The genomic proliferation of transposable elements in colonizing populations: Schistosoma mansoni in the new world

  • Published:
Genetica Aims and scope Submit manuscript

Abstract

Transposable elements (TEs) are mobile genes with an inherent ability to move within and among genomes. Theory predicts that TEs proliferate extensively during physiological stress due to the breakdown of TE repression systems. We tested this hypothesis in Schistosoma mansoni, a widespread trematode parasite that causes the human disease schistosomiasis. According to phylogenetic analysis, S. mansoni invaded the new world during the last 500 years. We hypothesized that new world strains of S. mansoni would have more copies of TEs than old world strains due to the physiological stress associated with invasion of the new world. We quantified the copy number of six TEs (Saci-1, Saci-2 and Saci-3, Perere-1, Merlin-sm1, and SmTRC1) in the genome and the transcriptome of old world and new world strains of S. mansoni, using qPCR relative quantification. As predicted, the genomes of new world parasites contain significantly more copies of class I and class II TEs in both laboratory and field strains. However, such differences are not observed in the transcriptome suggesting that either TE silencing mechanisms have reactivated to control the expression of these elements or the presence of inactive truncated copies of TEs.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Batista TM, Marques JT (2011) RNAi pathways in parasitic protists and worms. J Proteomics 74:1504–1514

    Article  CAS  PubMed  Google Scholar 

  • Bayne CJ, Grevelding CG (2003) Cloning of Schistosoma mansoni sporocysts in vitro and detection of genetic heterogeneity among individuals within clones. J Parasitol 89:1056–1060

    Article  CAS  PubMed  Google Scholar 

  • Berriman M, Haas BJ, LoVerde PJ, Wilson RA, Dillon GP, Cerqueira GC, Mashiyama ST, Al-Lazikani B, Andrade LF, Ashton PD, Aslett MA, Bartholomeu DC, Blandin G, Caffrey CR, Coghlan A, Coulson R, Day TA, Delcher A, DeMarco R, Djikeng A, Eyre T, Gamble JA, Ghedin E, Gu Y, Hertz-Fowler C, Hirai H, Hirai Y, Houston R, Ivens A, Johnston DA, Lacerda D, Macedo CD, McVeigh P, Ning Z, Oliveira G, Overington JP, Parkhill J, Pertea M, Pierce RJ, Protasio AV, Quail MA, Rajandream M, Rogers J, Sajid M, Salzberg SL, Stanke M, Tivey AR, White O, Williams DL, Wortman J, Wu W, Zamanian M, Zerlotini A, Fraser-Liggett CM, Barrell BG, El-Sayed NM (2009) The genome of the blood fluke Schistosoma mansoni. Nature 460:352–358

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Bland JM, Altman DG (1995) Multiple significance tests: the Bonferroni method. BMJ 310:170

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Blank WA, Test MR, Liu SF, Lewis FA, Blanton RE (2010) Long-term genetic stability and population dynamics of laboratory strains of Schistosoma mansoni. J Parasitol 96:900–907

    Article  PubMed  Google Scholar 

  • Blumenstiel JP (2011) Evolutionary dynamics of transposable elements in a small RNA world. Trends Genet 27:23–31

    Article  CAS  PubMed  Google Scholar 

  • Bowen NJ, Jordan IK, Epstein JA, Wood V, Levin HL (2003) Retrotransposons and their recognition of pol II promoters: a comprehensive survey of the transposable elements from the complete genome sequence of Schizosaccharomyces pombe. Genome Res 13:1984–1997

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Brindley PJ, Hotez PJ (2013) Break out: urogenital schistosomiasis and Schistosoma haematobium infection in the post-genomic era. PLoS Negl Trop Dis 7(3):e1961. doi:10.1371/journal.pntd.0001961

    Article  PubMed Central  PubMed  Google Scholar 

  • Brunette GW (2014) CDC health information for international travel 2014. Oxford University Press, Oxford

    Google Scholar 

  • Capy P, Gasperi G, Biemont C, Bazin C (2000) Stress and transposable elements: co-evolution or useful parasites? Heredity 85:101–106

    Article  CAS  PubMed  Google Scholar 

  • Casacuberta E, Gonzalez J (2013) The impact of transposable elements in environmental adaptation. Mol Ecol 22:1503–1517

    Article  CAS  PubMed  Google Scholar 

  • Chakrani F, Capy P, David JR (1993) Developmental temperature and somatic excision rate of mariner transposable element in three natural populations of Drosophila simulans. Genet Sel Evol 25:121–132

    Article  PubMed Central  CAS  Google Scholar 

  • Chen J, Yang Y, Guo S, Peng J, Liu Z, Li J, Lin J, Cheng G (2010) Molecular cloning and expression profiles of Argonaute proteins in Schistosoma japonicum. Parasitol Res 107:889–899

    Article  PubMed  Google Scholar 

  • Chitsulo L, Engels D, Montresor A, Savioli L (2000) The global status of schistosomiasis and its control. Acta Trop 77:41–51

    Article  CAS  PubMed  Google Scholar 

  • Crompton DWT (1999) How much human helminthiasis is there in the world? J Parasitol 85:397–403

    Article  CAS  PubMed  Google Scholar 

  • DeJong RJ, Morgan JAT, Paraense WL, Pointier JP, Amarista M, Ayeh-Kumi PF, Babiker A, Barbosa CS, Brémond P, Pedro Canese A, de Souza CP, Dominguez C, File S, Gutierrez A, Incani RN, Kawano T, Kazibwe F, Kpikpi J, Lwambo NJ, Mimpfoundi R, Njiokou F, Noël Poda J, Sene M, Velásquez LE, Yong M, Adema CM, Hofkin BV, Mkoji GM, Loker ES (2001) Evolutionary relationships and biogeography of Biomphalaria (Gastropoda: Planorbidae) with implications regarding its role as host of the human bloodfluke, Schistosoma mansoni. Mol Biol Evol 18:2225–2239

    Article  CAS  PubMed  Google Scholar 

  • DeJong RJ, Morgan JAT, Wilson WD, Al-Jaser MH, Appleton CC, Coulibaly G, D’Andrea PS, Doenhoff MJ, Haas W, Idris MA, Magalhães LA, Moné H, Mouahid G, Mubila L, Pointier JP, Webster JP, Zanotti-Magalhães EM, Paraense WL, Mkoji GM, Loker ES (2003) Phylogeography of Biomphalaria glabrata and B. pfeifferi, important intermediate hosts of Schistosoma mansoni in the New and Old World tropics. Mol Ecol 12:3041–3056

    Article  CAS  PubMed  Google Scholar 

  • DeMarco R, Machado AA, Soares MB, Gargioni C, Kawano T, Rodrigues V, Madeira AMBN, Wilson RA, Menck CFM, Setubal JC, Dias-Neto E, Leite LCC, Verjovski-Almeida S (2004) Saci-1, -2, and -3 and Perere, four novel retrotransposons with high transcriptional activities from the human parasite Schistosoma mansoni. J Virol 78:967–2978

    Article  Google Scholar 

  • DeMarco R, Venancio TM, Verjovski-Almeida S (2006) SmTRC1, a novel Schistosoma mansoni DNA transposon, discloses new families of animal and fungi transposons belonging to the CACTA superfamily. BMC Evol Biol 6:89–102

    Article  PubMed Central  PubMed  Google Scholar 

  • Desprès L, Imbert-Establet D, Monnerot M (1993) Molecular characterization of mitochondrial-DNA provides evidence for the recent introduction of Schistosoma mansoni into America. Mol Biochem Parasitol 60:221–230

    Article  PubMed  Google Scholar 

  • Doyle JM, McCormick CR, DeWoody JA (2011) The quantification of spermatozoa by real-time quantitative PCR, spectrophotometry, and spermatophore cap size. Mol Ecol Res 11:101–106

    Article  Google Scholar 

  • Engels WR, Johnson-Schlitz DM, Eggleston WB, Sved J (1990) High-frequency P element loss in Drosophila is homolog dependent. Cell 62:515–525

    Article  CAS  PubMed  Google Scholar 

  • Feschotte C (2004) Merlin, a new superfamily of DNA transposons identified in diverse animal genomes and related to bacterial IS1016 insertion sequences. Mol Biol Evol 21:1769–1780

    Article  CAS  PubMed  Google Scholar 

  • Feschotte C, Swamy L, Wessler SR (2003) Genome-wide analysis of mariner-like transposable elements in rice reveals complex relationships with Stowaway MITEs. Genetics 163:747–758

    PubMed Central  CAS  PubMed  Google Scholar 

  • Files VS (1951) A study of the vector-parasite relationships in Schistosoma mansoni. Parasitology 41:264–269

    Article  CAS  PubMed  Google Scholar 

  • Fletcher M, Loverde PT, Woodruff DS (1981) Genetic variation in Schistosoma mansoni enzyme polymorphisms in poulations from Africa, southwest Asia, South America, and the West Indies. Am J Trop Med Hyg 30:406–421

    CAS  PubMed  Google Scholar 

  • García Guerreiro MP, Fontdevila A (2007) The evolutionary history of Drosophila buzzatii. XXXVI. Molecular structural analysis of Osvaldo retrotransposon insertions in colonizing populations unveils drift effects in founder events. Genetics 175:301–310

    Article  PubMed Central  PubMed  Google Scholar 

  • García Guerreiro MP, Chávez-Sandoval BE, Balanyà J, Serra L, Fontdevila A (2008) Distribution of the transposable elements bilbo and gypsy in original and colonizing populations of Drosophila subobscura. BMC Evol Biol 8:234. doi:10.1186/1471-2148-8-234

    Article  PubMed Central  PubMed  Google Scholar 

  • Garza D, Medhora M, Koga A, Hartl DL (1991) Introduction of the transposable element mariner into the germline of Drosophila melanogaster. Genetics 128:303–310

    PubMed Central  CAS  PubMed  Google Scholar 

  • Geyer KK, Rodríguez López CM, Chalmers IW, Munshi SE, Truscott M, Heald J, Wilkinson MJ, Hoffmann KF (2011) Cytosine methylation regulates oviposition in the pathogenic blood fluke Schistosoma mansoni. Nat Commun 2:424. doi:10.1038/ncomms1433

    Article  PubMed Central  PubMed  Google Scholar 

  • Gomes MS, Cabral FJ, Jannotti-Passos LK, Carvalho O, Rodrigues V, Baba EH, Renata GS (2009) Preliminary analysis of miRNA pathway in Schistosoma mansoni. Parasitol Int 58:61–68

    Article  CAS  PubMed  Google Scholar 

  • Grevelding CG (1995) The female-specific W1 sequence of the Puerto Rican strain of Schistosoma mansoni. Mol Biochem Parasitol 71:269–272

    Article  CAS  PubMed  Google Scholar 

  • Hao L, Cai P, Jiang N, Wang H, Chen Q (2010) Identification and characterization of microRNAs and endogenous siRNAs in Schistosoma japonicum. BMC Genom 11:55. doi:10.1186/1471-2164-11-55

    Article  Google Scholar 

  • Hua-Van A, Le Rouzic A, Boutin TS, Filee J, Capy P (2011) The struggle for life of the genome’s selfish architects. Biol Direct 6:19. doi:10.1186/1745-6150-6-19

    Article  PubMed Central  PubMed  Google Scholar 

  • Huber JA, Morrison HG, Huse SM, Neal PR, Sogin ML, Welch DBM (2009) Effect of PCR amplicon size on assessments of clone library microbial diversity and community structure. Environ Microbiol 11:1292–1302

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Jolly RA, Goldstein KM, Wei T, Gao H, Chen P, Huang S, Colet J, Ryan TP, Thomas CE, Estrem ST (2005) Pooling samples within microarray studies: a comparative analysis of rat liver transcription response to prototypical toxicants. Physiol Genomics 22:346–355

    Article  CAS  PubMed  Google Scholar 

  • Kidwell M (2002) Transposable elements and the evolution of genome size in eukaryotes. Genetica 115:49–63

    Article  CAS  PubMed  Google Scholar 

  • Korsunenko A, Chrisanfova G, Lopatkin A, Beer SA, Voronin M, Ryskov AP, Semyenova SK (2012) Genetic differentiation of cercariae infrapopulations of the avian schistosome Trichobilharzia szidati based on RAPD markers and mitochondrial cox1 gene. Parasitol Res 110:833–841

    Article  PubMed  Google Scholar 

  • Krautz-Peterson G, Radwanska M, Ndegwa D, Shoemaker CB, Skelly PJ (2007) Optimizing gene suppression in schistosomes using RNA interference. Mol Biochem Parasitol 153:194–202

    Article  CAS  PubMed  Google Scholar 

  • Lambertucci JR, Serufo JC, Gerspacher-Lara R, Rayes AA, Teixeira R, Nobre V, Antunes CM (2000) Schistosoma mansoni: assessment of morbidity before and after control. Acta Trop 77:101–109

    Article  CAS  PubMed  Google Scholar 

  • Lewis FA, Stirewalt MA, Souza CP, Gazzinelli G (1986) Large-scale laboratory maintenance of Schistosoma mansoni, with observations on three schistosome/snail host combinations. J Parasitol 72:813–829

    Article  CAS  PubMed  Google Scholar 

  • Lockton S, Ross-Ibarra J, Gaut BS (2008) Demography and weak selection drive patterns of transposable element diversity in natural populations of Arabidopsis lyrata. Proc Natl Acad Sci USA 105:13965–13970

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Lockyer AE, Olson PD, Ostergaard P, Rollins D, Johnston DA, Attwood SW, Horak P, Snyder SD, Le TH, Agatsuma T, McManus DP, Carmichael AC, Naem S, Littlewood DT (2003) The phylogeny of the Schistosomatidae based on three genes with emphasis on the interrelationships of Schistosoma Weinland, 1858. Parasitology 126:203–224

    Article  CAS  PubMed  Google Scholar 

  • Lynch M, Conery JS (2003) The origins of genome complexity. Science 302:1401–1404

    Article  CAS  PubMed  Google Scholar 

  • Marinov GK, Williams BA, McCue K, Schroth GP, Gertz J, Myers RM, Wold BJ (2014) From single-cell to cell-pool transcriptomes: stochasticity in gene expression and RNA splicing. Genome Res 24:496–510

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Messerli SM, Kasinathan RS, Morgan W, Spranger S, Greenberg RM (2006) Schistosoma mansoni P-glycoprotein levels increase in response to praziquantel exposure and correlate with reduced praziquantel susceptibility. Mol Biochem Parasitol 167:54–59

    Article  Google Scholar 

  • Morgan JA, Dejong RJ, Adeoye GO, Ansa ED, Barbosa CS, Bremond P, Cesari IM, Charbonnel N, Correa LR, Coulibaly G, D’Andrea PS, De Souza CP, Doenhoff MJ, File S, Idris MA, Incani RN, Jarne P, Karanja DM, Kazibwe F, Kpikpi J, Lwambo NJ, Mabaye A, Magalhaes LA, Makundi A, Mone H, Mouahid G, Muchemi GM, Mungai BN, Sene M, Southgate V, Tchuente LA, Theron A, Yousif F, Zanotti-Magalhaes EM, Mkoji GM, Loker ES (2005) Origin and diversification of the human parasite Schistosoma mansoni. Mol Ecol 14:3889–3902

    Article  CAS  PubMed  Google Scholar 

  • Naito K, Zhang F, Tsukiyama T, Saito H, Hancock CN, Richardson AO, Okumoto Y, Tanisaka T, Wessler SR (2009) Unexpected consequences of a sudden and massive transposon amplification on rice gene expression. Nature 461:1130–1134

    Article  CAS  PubMed  Google Scholar 

  • Nuzhdin SV (1999) Sure facts, speculations, and open questions about the evolution of transposable element copy number. Genetica 107:129–137

    Article  CAS  PubMed  Google Scholar 

  • Oliver KR, Greene WK (2009) Transposable elements: powerful facilitators of evolution. BioEssays 31:703–714

    Article  CAS  PubMed  Google Scholar 

  • Pritham EJ (2009) Transposable elements and factors influencing their success in eukaryotes. J Hered 100:648–655

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Protasio AV, Tsai IJ, Babbage A, Nichol S, Hunt M, Aslett MA, De Silva N, Velarde GS, Anderson TJC, Clark RC, Davidson C, Gary PG, Dillon S, Holroyd NE, LoVerde PT, Lloyd C, McQuillan J, Oliveira G, Otto TD, Parker-Manuel SJ, Quail MA, Wilson RA, Zerlotini A, Dunne DW, Berriman M (2012) A systematically improved high quality genome and transcriptome of the human blood fluke Schistosoma mansoni. PLoS Negl Trop Dis 6:e1455. doi:10.1371/journal.pntd.0001455

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Rebollo R, Horard B, Hubert B, Vieira C (2010) Jumping genes and epigenetics: towards new species. Gene 454:1–7

    Article  CAS  PubMed  Google Scholar 

  • Rinaldi G, Eckert SE, Tsai IJ, Suttiprapa S, Kines KJ et al (2012) Germline transgenesis and insertional mutagenesis in Schistosoma mansoni mediated by murine leukemia virus. PLoS Pathog 8(7):e1002820. doi:10.1371/journal.ppat.1002820

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ros F, Kunze R (2001) Regulation of activator/dissociation transposition by replication and DNA methylation. Genetics 157:1723–1733

    PubMed Central  CAS  PubMed  Google Scholar 

  • Sambrook J, Russell DW (2001) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, New York

    Google Scholar 

  • Schlenke TA, Begun DJ (2004) Strong selective sweep associated with a transposon insertion in Drosophila simulans. Proc Natl Acad Sci USA 101:1626–1631

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Schmittgen TD, Livak KJ (2008) Analyzing real-time PCR data by the comparative CT method. Nat Protoc 3:1101–1108

    Article  CAS  PubMed  Google Scholar 

  • Semyenova SK, Khrisanfova GG, Korsunenko AV, Voronin MV, Beer SV, Vodyanitskaya SV, Serbina EA, Yurlova NI, Ryskov AP (2007) Multilocus variation in cercariae, parthenogenetic progeny of different species of the class Trematoda. Dokl Biol Sci 414:235–238

    Article  CAS  PubMed  Google Scholar 

  • Slotkin RK, Martienssen R (2007) Transposable elements and the epigenetic regulation of the genome. Nat Rev Genet 8:272–285

    Article  CAS  PubMed  Google Scholar 

  • Snyder SD, Loker ES (2000) Evolutionary relationships among the Schistosomatidae (Platyhelminthes: Digenea) and an Asian origin for Schistosoma. J Parasitol 86:283–288

    Article  CAS  PubMed  Google Scholar 

  • Stohler RA, Curtis J, Minchella DJ (2004) A comparison of microsatellite polymorphism and heterozygosity among field and laboratory populations of Schistosoma mansoni. Int J Parasitol 34:595–601

    Article  CAS  PubMed  Google Scholar 

  • Thiele EA, Sorenson RE, Gazzinelli A, Minchella DJ (2008) Genetic diversity and population structuring of Schistosoma mansoni in a Brazilian village. Int J Parasitol 38:389–399

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Thomas M, Macias C, Alonso C, Lopez MC (2010) The Biology and Evolution of transposable elements in parasites. Trends Parasitol 26:350–362

    Article  CAS  PubMed  Google Scholar 

  • Tollis M, Boissinot S (2013) Biology Lizards and LINEs: selection and demography affect the fate of L1 retrotransposons in the genome of the green anole (Anolis carolinensis). Genome Biol Evol 5:1754–1768

    Article  PubMed Central  PubMed  Google Scholar 

  • Venancio TM, Wilson RA, Verjovski-Almeida S, DeMarco R (2010) Burst of transposition from non-long terminal repeat retrotransposon families of the RTE clade in Schistosoma mansoni. Int J Parasitol 40:743–749

    Article  CAS  PubMed  Google Scholar 

  • Vieira C, Biémont C (2004) Transposable element dynamics in two sibling species: Drosophila melanogaster and Drosophila simulans. Genetica 120:115–123

    Article  CAS  PubMed  Google Scholar 

  • Visser ME (2008) Keeping up with a warming world; assessing the rate of adaptation to climate change. Proc Biol Sci 275:649–659

  • Young ND, Jex AR, Li B, Liu S, Yang L, Xiong Z, Li Y, Cantacessi C, Hall RS, Xu X, Chen F, Wu X, Zerlotini A, Oliveira G, Hofmann A, Zhang G, Fang X, Kang Y, Campbell BE, Loukas A, Ranganathan S, Rollins D, Rinaldi G, Brindley P, Yang H, Yang J, Wang J, Gasser RB (2012) Whole-genome sequence of Schistosoma haematobium. Nat Genet 44:221–225

    Article  CAS  PubMed  Google Scholar 

  • Zeh DW, Zeh JA, Ishida Y (2009) Transposable elements and an epigenetic basis for punctuated equilibria. BioEssays 31:715–726

    Article  CAS  PubMed  Google Scholar 

  • Zhou Y, Zheng H, Chen Y, Zhang L, Wang K, Guo J, Huang Z, Zhang B, Huang W, Jin K, Dou T, Hasegawa M, Wang L, Zhang Y, Zhou J, Tao L, Cao Z, Li Y, Vinar T, Brejova B, Brown D, Li M, Miller DJ, Blair D, Zhong Y, Chen Z, Liu F, Hu W, Wang Z, Zhang Q, Song H, Chen S, Xu X, Xu B, Ju C, Huang Y, Brindley PJ, McManus DP, Feng Z, Han Z, Lu G, Ren S, WangY GuW, Kang H, Chen J, Chen X, Chen S, Wang L, Yan J, Wang B, Lv X, Jin L, Wang B, Pu S, Zhang X, Zhang W, Hu Q, Zhu G, Wang J, Yu J, Wang J, Yang H, Ning Z, Beriman M, Wei C, Ruan Y, Zhao G, Wang S (2009) The Schistosoma japonicum genome reveals features of host–parasite interplay. Nature 460:345–351

    Article  PubMed Central  CAS  Google Scholar 

  • Zhu YY, Machleder EM, Chenchik A, Li R, Siebert PD (2001) Reverse transcriptase template switching: a SMART™ approach for full-length cDNA library construction. Biotechniques 30:892–897

    CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We sincerely acknowledge Dr. Phil LoVerde and Dr. Eric Loker for sharing the LE, EGY and Kenyan field isolates with us. We also thank Dr. Fred Lewis, Dr. Matt Tucker and the staff of the Biomedical Research Institute for providing the following reagents through BEI Resources, NIAID, NIH: (1) Schistosoma mansoni, Strain NMRI, Exposed Biomphalaria glabrata strain NMRI, NR-21962 and (2) Schistosoma mansoni, Strain PR-1, Exposed Biomphalaria glabrata strain M-line, NR-21961. We greatly appreciate the members of the Minchella and DeWoody labs for their comments on an earlier version of the manuscript. This project was funded by the Purdue University Department of Biological Sciences (DJM), Sigma Xi grants-in-aid program (BKW), and the University Faculty Scholar program (JAD).

Author information

Authors and Affiliations

  1. Department of Biological Sciences, Purdue University, West Lafayette, IN, 47907, USA

    Bhagya K. Wijayawardena, J. Andrew DeWoody & Dennis J. Minchella

  2. Department of Forestry and Natural Resources, Purdue University, West Lafayette, IN, 47907, USA

    J. Andrew DeWoody

Authors
  1. Bhagya K. Wijayawardena
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. J. Andrew DeWoody
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Dennis J. Minchella
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Bhagya K. Wijayawardena.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 203 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wijayawardena, B.K., DeWoody, J.A. & Minchella, D.J. The genomic proliferation of transposable elements in colonizing populations: Schistosoma mansoni in the new world. Genetica 143, 287–298 (2015). https://doi.org/10.1007/s10709-015-9825-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10709-015-9825-6

Keywords

Search

Navigation