Whole-genome sequencing of Schistosoma mansoni reveals extensive diversity with limited selection despite mass drug administration
1.Hotez, P. J. et al. The Global Burden of Disease Study 2010: interpretation and implications for the neglected tropical diseases. PLoS Negl. Trop. Dis. 8, e2865 (2014).2.World Health Organization. Prevention and Control of Schistosomiasis and Soil-transmitted Helminthiasis: Report of a WHO Expert Committee (World Health Organization, 2002).3.Montresor, A., Engels, D., Ramsan, M., Foum, A. & Savioli, L. Field test of the ‘dose pole’ for praziquantel in Zanzibar. Trans. R. Soc. Trop. Med. Hyg. 96, 323–324 (2002).CAS
PubMed
Article
PubMed Central
Google Scholar
4.World Health Organization. Helminth Control in School-aged Children: A Guide for Managers of Control Programmes (World Health Organisation, 2006).5.World Health Organization. Schistosomiasis and soil-transmitted helminthiases: numbers of people treated in 2019. Wkly. Epidemiol. Rec. 95, 629–640 (2020).
Google Scholar
6.Kabatereine, N. B. et al. Impact of a national helminth control programme on infection and morbidity in Ugandan schoolchildren. Bull. World Health Organ 85, 91–99 (2007).PubMed
PubMed Central
Article
Google Scholar
7.Bronzan, R. N. et al. Impact of community-based integrated mass drug administration on schistosomiasis and soil-transmitted helminth prevalence in Togo. PLoS Negl. Trop. Dis. 12, e0006551 (2018).PubMed
PubMed Central
Article
Google Scholar
8.Deol, A. K. et al. Schistosomiasis—assessing progress toward the 2020 and 2025 global goals. N. Engl. J. Med. 381, 2519–2528 (2019).9.World Health Organization. Accelerating work to overcome the global impact of neglected tropical diseases: a roadmap for implementation. https://apps.who.int/iris/bitstream/handle/10665/338712/WHO-HTM-NTD-2012.5-eng.pdf (2012).10.World Health Organization. A road map for neglected tropical diseases 2021–2030. https://www.who.int/neglected_diseases/Ending-the-neglect-to-attain-the-SDGs–NTD-Roadmap.pdf (2020).11.Mutuku, M. W. et al. A search for snail-related answers to explain differences in response of Schistosoma mansoni to praziquantel treatment among responding and persistent hotspot villages along the Kenyan shore of Lake Victoria. Am. J. Tropical Med. Hyg. 101, 65–77 (2019).CAS
Article
Google Scholar
12.Assaré, R. K. et al. Characteristics of persistent hotspots of Schistosoma mansoni in western Côte d’Ivoire. Parasit. Vectors 13, 337 (2020).PubMed
PubMed Central
Article
CAS
Google Scholar
13.Kittur, N. et al. Persistent hotspots in schistosomiasis consortium for operational research and evaluation studies for gaining and sustaining control of schistosomiasis after four years of mass drug administration of praziquantel. Am. J. Trop. Med. Hyg. 101, 617–627 (2019).PubMed
PubMed Central
Article
Google Scholar
14.Wiegand, R. E. et al. A persistent hotspot of Schistosoma mansoni infection in a five-year randomized trial of praziquantel preventative chemotherapy strategies. J. Infect. Dis. 216, 1425–1433 (2017).PubMed
PubMed Central
Article
Google Scholar
15.Hedtke, S. M. et al. Genomic epidemiology in filarial nematodes: transforming the basis for elimination program decisions. Front. Genet. 10, 1282 (2019).CAS
PubMed
Article
PubMed Central
Google Scholar
16.Doyle, S. R. & Cotton, J. A. Genome-wide approaches to investigate anthelmintic resistance. Trends Parasitol. 35, 289–301 (2019).CAS
PubMed
Article
PubMed Central
Google Scholar
17.Crellen, T. et al. Whole genome resequencing of the human parasite Schistosoma mansoni reveals population history and effects of selection. Sci. Rep. 6, 1–13 (2016).Article
CAS
Google Scholar
18.Gower, C. M. et al. Population genetic structure of Schistosoma mansoni and Schistosoma haematobium from across six sub-Saharan African countries: implications for epidemiology, evolution and control. Acta Trop. 128, 261–274 (2013).PubMed
Article
PubMed Central
Google Scholar
19.Standley, C., Kabatereine, N., Lange, C., Lwambo, N. & Stothard, J. Molecular epidemiology and phylogeography of Schistosoma mansoni around Lake Victoria. Parasitology 137, 1937–1949 (2010).CAS
PubMed
Article
PubMed Central
Google Scholar
20.Faust, C. L. et al. Two-year longitudinal survey reveals high genetic diversity of Schistosoma mansoni with adult worms surviving praziquantel treatment at the start of mass drug administration in Uganda. Parasit. Vectors 12, 607 (2019).PubMed
PubMed Central
Article
Google Scholar
21.Stothard, J. R. et al. Molecular epidemiology of Schistosoma mansoni in Uganda: DNA barcoding reveals substantial genetic diversity within Lake Albert and Lake Victoria populations. Parasitology 136, 1813–1824 (2009).CAS
PubMed
Article
PubMed Central
Google Scholar
22.Norton, A. J. et al. Genetic consequences of mass human chemotherapy for Schistosoma mansoni: population structure pre- and post-praziquantel treatment in Tanzania. Am. J. Trop. Med. Hyg. 83, 951–957 (2010).PubMed
PubMed Central
Article
Google Scholar
23.Blanton, R. E. et al. Schistosoma mansoni population structure and persistence after praziquantel treatment in two villages of Bahia, Brazil. Int. J. Parasitol. 41, 1093–1099 (2011).PubMed
PubMed Central
Article
Google Scholar
24.Gower, C. M. et al. Phenotypic and genotypic monitoring of Schistosoma mansoni in Tanzanian schoolchildren five years into a preventative chemotherapy national control programme. Parasit. Vectors 10, 593 (2017).PubMed
PubMed Central
Article
CAS
Google Scholar
25.Chevalier, F. D. et al. Oxamniquine resistance alleles are widespread in Old World Schistosoma mansoni and predate drug deployment. PLoS Pathog. 15, e1007881 (2019).CAS
PubMed
PubMed Central
Article
Google Scholar
26.Platt, R. N. et al. Ancient hybridization and adaptive introgression of an invadolysin gene in schistosome parasites. Mol. Biol. Evol. 36, 2127–2142 (2019).PubMed
PubMed Central
Article
CAS
Google Scholar
27.Shortt, J. A. et al. Population genomic analyses of schistosome parasites highlight critical challenges facing endgame elimination efforts. Sci. Rep. 11, 6884 (2021).ADS
CAS
PubMed
PubMed Central
Article
Google Scholar
28.Truscott, J. E. et al. A comparison of two mathematical models of the impact of mass drug administration on the transmission and control of schistosomiasis. Epidemics 18, 29–37 (2017).CAS
PubMed
PubMed Central
Article
Google Scholar
29.Bouzat, J. L. Conservation genetics of population bottlenecks: the role of chance, selection, and history. Conserv. Genet. 11, 463–478 (2010).Article
Google Scholar
30.Andrews, P. Praziquantel: mechanisms of anti-schistosomal activity. Pharmacol. Ther. 29, 129–156 (1985).CAS
PubMed
Article
PubMed Central
Google Scholar
31.Cioli, D. & Pica-Mattoccia, L. Praziquantel. Parasitol. Res. 90, S3–S9 (2003).32.Caffrey, C. R. Schistosomiasis and its treatment. Future Med. Chem. 7, 675–676 (2015).CAS
PubMed
Article
PubMed Central
Google Scholar
33.Kaplan, R. M. & Vidyashankar, A. N. An inconvenient truth: global worming and anthelmintic resistance. Vet. Parasitol. 186, 70–78 (2012).PubMed
Article
PubMed Central
Google Scholar
34.Rose, H. et al. Widespread anthelmintic resistance in European farmed ruminants: a systematic review. Vet. Rec. 176, 546 (2015).CAS
PubMed
Article
PubMed Central
Google Scholar
35.Schwab, A. E., Boakye, D. A., Kyelem, D. & Prichard, R. K. Detection of benzimidazole resistance-associated mutations in the filarial nematode Wuchereria bancrofti and evidence for selection by albendazole and ivermectin combination treatment. Am. J. Trop. Med. Hyg. 73, 234–238 (2005).CAS
PubMed
Article
PubMed Central
Google Scholar
36.Fallon, P. G. & Doenhoff, M. J. Drug-resistant schistosomiasis: resistance to praziquantel and oxamniquine induced in Schistosoma mansoni in mice is drug specific. Am. J. Trop. Med. Hyg. 51, 83–88 (1994).CAS
PubMed
Article
Google Scholar
37.Couto, F. F. B. et al. Schistosoma mansoni: a method for inducing resistance to praziquantel using infected Biomphalaria glabrata snails. Mem. Inst. Oswaldo Cruz 106, 153–157 (2011).CAS
PubMed
Article
PubMed Central
Google Scholar
38.Mwangi, I. N. et al. Praziquantel sensitivity of Kenyan Schistosoma mansoni isolates and the generation of a laboratory strain with reduced susceptibility to the drug. Int. J. Parasitol. Drugs Drug Resist. 4, 296–300 (2014).PubMed
PubMed Central
Article
Google Scholar
39.Lamberton, P. H. L., Faust, C. L. & Webster, J. P. Praziquantel decreases fecundity in Schistosoma mansoni adult worms that survive treatment: evidence from a laboratory life-history trade-offs selection study. Infect. Dis. Poverty 6, 110 (2017).PubMed
PubMed Central
Article
Google Scholar
40.Stelma, F. F. et al. Efficacy and side effects of praziquantel in an epidemic focus of Schistosoma mansoni. Am. J. Trop. Med. Hyg. 53, 167–170 (1995).CAS
PubMed
Article
Google Scholar
41.Melman, S. D. et al. Reduced susceptibility to praziquantel among naturally occurring Kenyan isolates of Schistosoma mansoni. PLoS Negl. Trop. Dis. 3, e504 (2009).PubMed
PubMed Central
Article
CAS
Google Scholar
42.Crellen, T. et al. Reduced efficacy of praziquantel against Schistosoma mansoni is associated with multiple rounds of mass drug administration. Clin. Infect. Dis. 63, 1151–1159 (2016).CAS
PubMed
PubMed Central
Google Scholar
43.King, C. H., Muchiri, E. M. & Ouma, J. H. Evidence against rapid emergence of praziquantel resistance in Schistosoma haematobium, Kenya. Emerg. Infect. Dis. 6, 585–594 (2000).CAS
PubMed
PubMed Central
Article
Google Scholar
44.Gryseels, B. et al. Are poor responses to praziquantel for the treatment of Schistosoma mansoni infections in Senegal due to resistance? An overview of the evidence. Trop. Med. Int. Health 6, 864–873 (2001).CAS
PubMed
Article
Google Scholar
45.Fenwick, A. & Webster, J. P. Schistosomiasis: challenges for control, treatment and drug resistance. Curr. Opin. Infect. Dis. 19, 577–582 (2006).PubMed
Article
Google Scholar
46.Albonico, M. et al. Monitoring the efficacy of drugs for neglected tropical diseases controlled by preventive chemotherapy. J. Glob. Antimicrob. Resist 3, 229–236 (2015).CAS
PubMed
PubMed Central
Article
Google Scholar
47.Fukushige, M., Chase-Topping, M., Woolhouse, M. E. J. & Mutapi, F. Efficacy of praziquantel has been maintained over four decades (from 1977 to 2018): a systematic review and meta-analysis of factors influence its efficacy. PLoS Negl. Trop. Dis. 15, e0009189 (2021).CAS
PubMed
PubMed Central
Article
Google Scholar
48.Hodgkinson, J. E. et al. Refugia and anthelmintic resistance: concepts and challenges. Int. J. Parasitol. Drugs Drug Resist. 10, 51–57 (2019).PubMed
PubMed Central
Article
Google Scholar
49.Walker, M. et al. New approaches to measuring anthelminthic drug efficacy: parasitological responses of childhood schistosome infections to treatment with praziquantel. Parasit. Vectors 9, 41 (2016).PubMed
PubMed Central
Article
CAS
Google Scholar
50.Kittur, N. et al. Defining persistent hotspots: areas that fail to decrease meaningfully in prevalence after multiple years of mass drug administration with praziquantel for control of schistosomiasis. Am. J. Trop. Med. Hyg. 97, 1810–1817 (2017).PubMed
PubMed Central
Article
Google Scholar
51.Levecke, B. et al. Evaluation of the therapeutic efficacy of praziquantel against schistosomes in seven countries with ongoing large-scale deworming programs. Int. J. Parasitol. Drugs Drug Resist. 14, 183–187 (2020).CAS
PubMed
PubMed Central
Article
Google Scholar
52.Nei, M., Maruyama, T. & Chakraborty, R. The bottleneck effect and genetic variability in populations. Evolution 29, 1–10 (1975).PubMed
Article
PubMed Central
Google Scholar
53.Gattepaille, L. M., Jakobsson, M. & Blum, M. G. B. Inferring population size changes with sequence and SNP data: lessons from human bottlenecks. Heredity 110, 409–419 (2013).CAS
PubMed
PubMed Central
Article
Google Scholar
54.Kohn, A. B., Anderson, P. A. V., Roberts-Misterly, J. M. & Greenberg, R. M. Schistosome Calcium Channel β Subunits: unusual modulatory effects and potential role in the action of the antischistosomal drug praziquantel. J. Biol. Chem. 276, 36873–36876 (2001).CAS
PubMed
Article
Google Scholar
55.Greenberg, R. M. Are Ca2+ channels targets of praziquantel action? Int. J. Parasitol. 35, 1–9 (2005).CAS
PubMed
Article
Google Scholar
56.Pica-Mattoccia, L. et al. Cytochalasin D abolishes the schistosomicidal activity of praziquantel. Exp. Parasitol. 115, 344–351 (2007).CAS
PubMed
Article
Google Scholar
57.Nogi, T., Zhang, D., Chan, J. D. & Marchant, J. S. A novel biological activity of praziquantel requiring voltage-operated Ca2+ channel β subunits: subversion of flatworm regenerative polarity. PLoS Negl. Trop. Dis. 3, e464 (2009).PubMed
PubMed Central
Article
CAS
Google Scholar
58.Kohn, A. B., Roberts-Misterly, J. M., Anderson, P. A. V., Khan, N. & Greenberg, R. M. Specific sites in the Beta Interaction Domain of a schistosome Ca2+ channel beta subunit are key to its role in sensitivity to the anti-schistosomal drug praziquantel. Parasitology 127, 349–356 (2003).CAS
PubMed
Article
Google Scholar
59.Valle, C. et al. Sequence and level of endogenous expression of calcium channel β subunits in Schistosoma mansoni displaying different susceptibilities to praziquantel. Mol. Biochem. Parasitol. 130, 111–115 (2003).CAS
PubMed
Article
Google Scholar
60.Park, S.-K. et al. The anthelmintic drug praziquantel activates a schistosome transient receptor potential channel. J. Biol. Chem. https://doi.org/10.1074/jbc.AC119.011093 (2019).61.Park, S.-K. et al. Mechanism of praziquantel action at a parasitic flatworm ion channel. Preprint at bioRxiv https://doi.org/10.1101/2021.03.09.434291 (2021).62.Le Clec’h, W., Chevalier, F. D., Mattos, A. C. A. & Strickland, A. Genetic analysis of praziquantel resistance in schistosome parasites implicates a Transient Receptor Potential channel. Preprint at bioRxiv https://doi.org/10.1101/2021.06.09.447779 (2021).63.Standley, C. et al. Intestinal schistosomiasis and soil-transmitted helminthiasis in Ugandan schoolchildren: a rapid mapping assessment. Geospat. Health 4, 39–53 (2009).PubMed
Article
PubMed Central
Google Scholar
64.Steinauer, M. L., Hanelt, B., Agola, L. E., Mkoji, G. M. & Loker, E. S. Genetic structure of Schistosoma mansoni in western Kenya: the effects of geography and host sharing. Int. J. Parasitol. 39, 1353–1362 (2009).CAS
PubMed
PubMed Central
Article
Google Scholar
65.Agola, L. E. et al. Genetic diversity and population structure of Schistosoma mansoni within human infrapopulations in Mwea, central Kenya assessed by microsatellite markers. Acta Trop. 111, 219–225 (2009).CAS
PubMed
PubMed Central
Article
Google Scholar
66.Gower, C. M. et al. Population genetics of Schistosoma haematobium: development of novel microsatellite markers and their application to schistosomiasis control in Mali. Parasitology 138, 978–994 (2011).CAS
PubMed
Article
PubMed Central
Google Scholar
67.Betson, M., Sousa-Figueiredo, J. C., Kabatereine, N. B. & Stothard, J. R. New insights into the molecular epidemiology and population genetics of Schistosoma mansoni in Ugandan pre-school children and mothers. PLoS Negl. Trop. Dis. 7, e2561 (2013).PubMed
PubMed Central
Article
Google Scholar
68.Van den Broeck, F. et al. Inbreeding within human Schistosoma mansoni: do host-specific factors shape the genetic composition of parasite populations? Heredity 113, 32–41 (2014).PubMed
PubMed Central
Article
CAS
Google Scholar
69.Thiele, E. A., Sorensen, R. E., Gazzinelli, A. & Minchella, D. J. Genetic diversity and population structuring of Schistosoma mansoni in a Brazilian village. Int. J. Parasitol. 38, 389–399 (2008).CAS
PubMed
Article
PubMed Central
Google Scholar
70.Kebede, T., Negash, Y. & Erko, B. Schistosoma mansoni infection in human and nonhuman primates in selected areas of Oromia Regional State, Ethiopia. J. Vector Borne Dis. 55, 116–121 (2018).PubMed
Article
PubMed Central
Google Scholar
71.Aemero, M. et al. Genetic diversity, multiplicity of infection and population structure of Schistosoma mansoni isolates from human hosts in Ethiopia. BMC Genet. 16, 137 (2015).PubMed
PubMed Central
Article
CAS
Google Scholar
72.Neves, M. I., Webster, J. P. & Walker, M. Estimating helminth burdens using sibship reconstruction. Parasit. Vectors 12, 441 (2019).PubMed
PubMed Central
Article
Google Scholar
73.Mawa, P. A., Kincaid-Smith, J., Tukahebwa, E. M., Webster, J. P. & Wilson, S. Schistosomiasis morbidity hotspots: roles of the human host, the parasite and their interface in the development of severe morbidity. Front. Immunol. 12, 751 (2021).
Google Scholar
74.Theron, A., Sire, C., Rognon, A., Prugnolle, F. & Durand, P. Molecular ecology of Schistosoma mansoni transmission inferred from the genetic composition of larval and adult infrapopulations within intermediate and definitive hosts. Parasitology 129, 571–585 (2004).CAS
PubMed
Article
PubMed Central
Google Scholar
75.Parker, M. et al. Border parasites: schistosomiasis control among Uganda’s fisherfolk. J. East. Afr. Stud. 6, 98–123 (2012).Article
Google Scholar
76.Messer, P. W. & Petrov, D. A. Population genomics of rapid adaptation by soft selective sweeps. Trends Ecol. Evol. 28, 659–669 (2013).PubMed
Article
PubMed Central
Google Scholar
77.Gilleard, J. S. & Redman, E. Genetic diversity and population structure of haemonchus contortus. Adv. Parasitol. 93, 31–68 (2016).CAS
PubMed
Article
PubMed Central
Google Scholar
78.Huyse, T. et al. Regular treatments of praziquantel do not impact on the genetic make-up of Schistosoma mansoni in Northern Senegal. Infect. Genet. Evol. 18, 100–105 (2013).CAS
PubMed
Article
PubMed Central
Google Scholar
79.Lelo, A. E. et al. No apparent reduction in schistosome burden or genetic diversity following four years of school-based mass drug administration in mwea, central kenya, a heavy transmission area. PLoS Negl. Trop. Dis. 8, e3221 (2014).PubMed
PubMed Central
Article
Google Scholar
80.French, M. D. et al. Reductions in genetic diversity of Schistosoma mansoni populations under chemotherapeutic pressure: the effect of sampling approach and parasite population definition. Acta Trop. 128, 196–205 (2013).PubMed
Article
PubMed Central
Google Scholar
81.Van den Broeck, F., Vanoverbeeke, J., Polman, K. & Huyse, T. A Darwinian outlook on schistosomiasis elimination. Preprint at bioRxiv. https://doi.org/10.1101/2020.10.28.358523 (2020).82.Hayeshi, R., Masimirembwa, C., Mukanganyama, S. & Ungell, A.-L. B. The potential inhibitory effect of antiparasitic drugs and natural products on P-glycoprotein mediated efflux. Eur. J. Pharm. Sci. 29, 70–81 (2006).CAS
PubMed
Article
PubMed Central
Google Scholar
83.Hines-Kay, J. et al. Transcriptional analysis of Schistosoma mansoni treated with praziquantel in vitro. Mol. Biochem. Parasitol. 186, 87–94 (2012).CAS
PubMed
PubMed Central
Article
Google Scholar
84.Lespine, A., Ménez, C., Bourguinat, C. & Prichard, R. K. P-glycoproteins and other multidrug resistance transporters in the pharmacology of anthelmintics: prospects for reversing transport-dependent anthelmintic resistance. Int. J. Parasitol. Drugs Drug Resist. 2, 58–75 (2012).PubMed
Article
CAS
PubMed Central
Google Scholar
85.Greenberg, R. M. ABC multidrug transporters in schistosomes and other parasitic flatworms. Parasitol. Int. 62, 647–653 (2013).CAS
PubMed
PubMed Central
Article
Google Scholar
86.Hermisson, J. & Pennings, P. S. Soft sweeps: molecular population genetics of adaptation from standing genetic variation. Genetics 169, 2335–2352 (2005).CAS
PubMed
PubMed Central
Article
Google Scholar
87.Redman, E. et al. The emergence of resistance to the benzimidazole anthlemintics in parasitic nematodes of livestock is characterised by multiple independent hard and soft selective sweeps. PLoS Neglected Tropical Dis. 9, e0003494 (2015).Article
CAS
Google Scholar
88.Doyle, S. R. et al. Genome-wide analysis of ivermectin response by Onchocerca volvulus reveals that genetic drift and soft selective sweeps contribute to loss of drug sensitivity. PLoS Negl. Trop. Dis. 11, e0005816 (2017).PubMed
PubMed Central
Article
CAS
Google Scholar
89.Choi, Y.-J. et al. Genomic introgression mapping of field-derived multiple-anthelmintic resistance in Teladorsagia circumcincta. PLoS Genet. 13, e1006857 (2017).PubMed
PubMed Central
Article
CAS
Google Scholar
90.Chami, G. F. et al. Influence of Schistosoma mansoni and hookworm infection intensities on anaemia in Ugandan villages. PLoS Negl. Trop. Dis. 9, e0004193 (2015).PubMed
PubMed Central
Article
CAS
Google Scholar
91.Adriko, M. et al. Impact of a national deworming campaign on the prevalence of soil-transmitted helminthiasis in Uganda (2004–2016): implications for national control programs. PLoS Negl. Trop. Dis. 12, e0006520 (2018).PubMed
PubMed Central
Article
Google Scholar
92.Webster, J. P., Gower, C. M. & Norton, A. J. Evolutionary concepts in predicting and evaluating the impact of mass chemotherapy schistosomiasis control programmes on parasites and their hosts. Evol. Appl. 1, 66–83 (2008).PubMed
PubMed Central
Article
Google Scholar
93.Leathwick, D. M., Ganesh, S. & Waghorn, T. S. Evidence for reversion towards anthelmintic susceptibility in Teladorsagia circumcincta in response to resistance management programmes. Int. J. Parasitol. Drugs Drug Resist. 5, 9–15 (2015).PubMed
PubMed Central
Article
Google Scholar
94.Kenyon, F. et al. The role of targeted selective treatments in the development of refugia-based approaches to the control of gastrointestinal nematodes of small ruminants. Vet. Parasitol. 164, 3–11 (2009).CAS
PubMed
Article
PubMed Central
Google Scholar
95.Chabasse, D., Bertrand, G., Leroux, J. P., Gauthey, N. & Hocquet, P. Developmental bilharziasis caused by Schistosoma mansoni discovered 37 years after infestation. Bull. Soc. Pathol. Exot. Filiales 78, 643–647 (1985).CAS
PubMed
PubMed Central
Google Scholar
96.Warren, K. S., Mahmoud, A. A., Cummings, P., Murphy, D. J. & Houser, H. B. Schistosomiasis mansoni in Yemeni in California: duration of infection, presence of disease, therapeutic management. Am. J. Trop. Med. Hyg. 23, 902–909 (1974).CAS
PubMed
Article
PubMed Central
Google Scholar
97.William, S. et al. Stability and reproductive fitness of Schistosoma mansoni isolates with decreased sensitivity to praziquantel. Int. J. Parasitol. 31, 1093–1100 (2001).CAS
PubMed
Article
PubMed Central
Google Scholar
98.Viana, M., Faust, C. L., Haydon, D. T., Webster, J. P. & Lamberton, P. H. L. The effects of subcurative praziquantel treatment on life‐history traits and trade‐offs in drug‐resistant Schistosoma mansoni. Evol. Appl. 11, 488–500 (2018).CAS
PubMed
Article
PubMed Central
Google Scholar
99.Standley, C. J., Goodacre, S. L., Wade, C. M. & Stothard, J. R. The population genetic structure of Biomphalaria choanomphala in Lake Victoria, East Africa: implications for schistosomiasis transmission. Parasit. Vectors 7, 524 (2014).PubMed
PubMed Central
Article
Google Scholar
100.Mitta, G. et al. The compatibility between Biomphalaria glabrata snails and Schistosoma mansoni: an increasingly complex puzzle. Adv. Parasitol. 97, 111–145 (2017).CAS
PubMed
Article
PubMed Central
Google Scholar
101.Rowel, C. et al. Environmental epidemiology of intestinal schistosomiasis in Uganda: population dynamics of Biomphalaria (Gastropoda: Planorbidae) in Lake Albert and Lake Victoria with observations on natural infections with digenetic trematodes. BioMed. Res. Int. 2015, 1–11 (2015).Article
Google Scholar
102.Anderson, L. C., Loker, E. S. & Wearing, H. J. Modeling schistosomiasis transmission: the importance of snail population structure. Parasit. Vectors 14, 94 (2021).PubMed
PubMed Central
Article
Google Scholar
103.Nikolakis, Z. L. et al. Patterns of relatedness and genetic diversity inferred from whole genome sequencing of archival blood fluke miracidia (Schistosoma japonicum). PLoS Negl. Trop. Dis. 15, e0009020 (2021).CAS
PubMed
PubMed Central
Article
Google Scholar
104.Kovač, J. et al. Pharmacokinetics of praziquantel in Schistosoma mansoni- and Schistosoma haematobium-infected school- and preschool-aged children. Antimicrob. Agents Chemother. 62, e02253-17 (2018).105.Secor, W. E. Faculty opinions recommendation of sensitivity and specificity of multiple Kato-Katz thick smears and a circulating cathodic antigen test for Schistosoma mansoni diagnosis pre- and post-repeated-praziquantel treatment. Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature. https://doi.org/10.3410/f.718871676.793510451 (2015).106.Stothard, J. R., Sousa-Figueiredo, J. C. & Navaratnam, A. M. D. Advocacy, policies and practicalities of preventive chemotherapy campaigns for African children with schistosomiasis. Expert Rev. Anti. Infect. Ther. 11, 733–752 (2013).CAS
PubMed
Article
PubMed Central
Google Scholar
107.Fenwick, A. et al. The Schistosomiasis Control Initiative (SCI): rationale, development and implementation from 2002–2008. Parasitology 136, 1719–1730 (2009).CAS
PubMed
Article
PubMed Central
Google Scholar
108.Colley, D. G., Bustinduy, A. L., Secor, W. E. & King, C. H. Human schistosomiasis. Lancet 383, 2253–2264 (2014).PubMed
PubMed Central
Article
Google Scholar
109.Crellen, T. et al. Schistosoma mansoni egg count reduction data, Ugandan Primary Schools 2014. https://doi.org/10.13140/RG.2.2.12687.84640 (2018).110.Hadfield, J. D. MCMC methods for multi-response generalized linear mixed models: the MCMCglmm R package. J. Stat. Softw. 33, 1–22 (2010).Article
Google Scholar
111.Emery, A. M., Allan, F. E., Rabone, M. E. & Rollinson, D. Schistosomiasis collection at NHM (SCAN). Parasites Vectors 5, 1 (2012).Article
Google Scholar
112.Howe, K. L., Bolt, B. J., Shafie, M., Kersey, P. & Berriman, M. WormBase ParaSite—a comprehensive resource for helminth genomics. Mol. Biochem. Parasitol. 215, 2–10 (2017).CAS
PubMed
PubMed Central
Article
Google Scholar
113.Protasio, A. V. et al. A systematically improved high quality genome and transcriptome of the human blood fluke Schistosoma mansoni. PLoS Negl. Trop. Dis. 6, e1455 (2012).CAS
PubMed
PubMed Central
Article
Google Scholar
114.Wood, D. E. & Salzberg, S. L. Kraken: ultrafast metagenomic sequence classification using exact alignments. Genome Biol. 15, R46 (2014).PubMed
PubMed Central
Article
Google Scholar
115.McKenna, A. et al. The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res. 20, 1297–1303 (2010).CAS
PubMed
PubMed Central
Article
Google Scholar
116.Li, H. Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM. Preprint at https://arxiv.org/abs/1303.3997 (2013).117.Danecek, P. et al. The variant call format and VCFtools. Bioinformatics 27, 2156–2158 (2011).CAS
PubMed
PubMed Central
Article
Google Scholar
118.Quinlan, A. R. & Hall, I. M. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 26, 841–842 (2010).CAS
PubMed
PubMed Central
Article
Google Scholar
119.Manichaikul, A. et al. Robust relationship inference in genome-wide association studies. Bioinformatics 26, 2867–2873 (2010).CAS
PubMed
PubMed Central
Article
Google Scholar
120.Gómez-Rubio, V. ggplot2—elegant graphics for data analysis (2nd edn). J. Stat. Softw., Book Rev. 77, 1–3 (2017).
Google Scholar
121.Purcell, S. et al. PLINK: a tool set for whole-genome association and population-based linkage analyses. Am. J. Hum. Genet. 81, 559–575 (2007).CAS
PubMed
PubMed Central
Article
Google Scholar
122.Alexander, D. H., Novembre, J. & Lange, K. Fast model-based estimation of ancestry in unrelated individuals. Genome Res. 19, 1655–1664 (2009).CAS
PubMed
PubMed Central
Article
Google Scholar
123.Paradis, E. & Schliep, K. ape 5.0: an environment for modern phylogenetics and evolutionary analyses in R. Bioinformatics https://doi.org/10.1093/bioinformatics/bty633 (2018).124.Schliep, K. P. phangorn: phylogenetic analysis in R. Bioinformatics 27, 592–593 (2011).CAS
PubMed
Article
PubMed Central
Google Scholar
125.Yu, G., Smith, D. K., Zhu, H., Guan, Y. & Lam, T. T.-Y. ggtree: an R package for visualization and annotation of phylogenetic trees with their covariates and other associated data. Methods Ecol. Evol. 8, 28–36 (2017).Article
Google Scholar
126.Korunes, K. L. & Samuk, K. pixy: unbiased estimation of nucleotide diversity and divergence in the presence of missing data. Mol. Ecol. Resour. 21, 1359–1368 (2021).PubMed
PubMed Central
Article
Google Scholar
127.Kassambara, A. ggpubr:‘ggplot2’ based publication ready plots. R package version 0.25 (2018).128.Criscione, C. D., Valentim, C. L. L., Hirai, H., LoVerde, P. T. & Anderson, T. J. C. Genomic linkage map of the human blood fluke Schistosoma mansoni. Genome Biol. 10, R71 (2009).PubMed
PubMed Central
Article
CAS
Google Scholar
129.Browning, S. R. & Browning, B. L. Rapid and accurate haplotype phasing and missing-data inference for whole-genome association studies by use of localized haplotype clustering. Am. J. Hum. Genet. 81, 1084–1097 (2007).CAS
PubMed
PubMed Central
Article
Google Scholar
130.Szpiech, Z. A. & Hernandez, R. D. selscan: an efficient multithreaded program to perform EHH-based scans for positive selection. Mol. Biol. Evol. 31, 2824–2827 (2014).CAS
PubMed
PubMed Central
Article
Google Scholar
131.Vitti, J. J., Grossman, S. R. & Sabeti, P. C. Detecting natural selection in genomic data. Annu. Rev. Genet. 47, 97–120 (2013).CAS
PubMed
Article
PubMed Central
Google Scholar
132.Terhorst, J., Kamm, J. A. & Song, Y. S. Robust and scalable inference of population history from hundreds of unphased whole genomes. Nat. Genet. 49, 303–309 (2017).CAS
PubMed
Article
PubMed Central
Google Scholar
133.Gutenkunst, R. N., Hernandez, R. D., Williamson, S. H. & Bustamante, C. D. Inferring the joint demographic history of multiple populations from multidimensional SNP frequency data. PLoS Genet. 5, e1000695 (2009).PubMed
PubMed Central
Article
CAS
Google Scholar
134.R Core Team. R: a language and environment for statistical computing. R Foundation for statistical computing, Vienna (2013).135.Wilke, C. O. cowplot: Streamlined plot theme and plot annotations for ‘ggplot2’. R package version 0.7.0 (2016).136.Tange, O. GNU Parallel: The Command-Line Power Tool | USENIX. https://www.usenix.org/publications/login/february-2011-volume-36-number-1/gnu-parallel-command-line-power-tool (2011).137.Li, H. A statistical framework for SNP calling, mutation discovery, association mapping and population genetical parameter estimation from sequencing data. Bioinformatics 27, 2987–2993 (2011).CAS
PubMed
PubMed Central
Article
Google Scholar
138.Berger, D. et al. Data release: Whole-genome sequencing of Schistosoma mansoni reveals extensive diversity with limited selection despite mass drug administration. https://doi.org/10.5281/ZENODO.4940588 (2021).139.Berger, D. duncanberger/PZQ_POPGEN. https://doi.org/10.5281/zenodo.4975909 (2021). More