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Z chromosome features. (a) Map of the Z chromosome. Loci that had 0% recombination with other markers are shown adjacent to the marker used in the construction of the map. The Z-specific markers are shown in green. Asterisks (*P < 0.01, **P < 0.005, ***P < 0.001, ****P < 0.0005, *****P < 0.0001) indicate significance of deviation from Mendelian expectations, where brackets show recombination hotspots in the female meioses (recombination frequencies for each sex are listed next to the brackets). (b) Meiotic metaphase spreads from females showing the Z and W bivalents. This figure illustrates the non-recombining region between the Z and W chromosomes. The dark staining regions are heterochromatin of the W chromosome and the large black arrows mark chiasmata. Scale bars are 10 μm. (c) Fluorescent in situ hybridization (FISH) showing the hybridization position of bacterial artificial chromosome (BACs; names at lower left of each panel) that BLAST to scaffolds with mapped microsatellite markers. The white arrowheads show BAC hybridization and the white dash is the centromere. Scale bar is 10 μm. The inset for BAC 15B20 is the W chromosome, on which 15B20 does not hybridize (that is, it is Z-specific). The genetic map position of the markers on these BACs is shown in blue text in (a). FISH allows assignment of linkage groups to physical chromosomes (see also Additional data file 4 and ).
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Schistosoma mansoni is a blood fluke that infects approximately 90 million people. The complete life cycle of this parasite can be maintained in the laboratory, making this one of the few experimentally tractable human helminth infections, and a rich literature reveals heritable variation in important biomedical traits such as virulence, host-speci...
Citations
... Genetic cross data have been used to determine the mode of inheritance of genetic markers or phenotypes in parasitic helminths (Le Jambre & Royal, 1977;Le Jambre et al., 1979;Habe et al., 1985;Cioli et al., 1992;Hunt et al., 2010;Detwiler & Criscione, 2011;Redman et al., 2012). However, parasitic helminth linkage maps are relatively recent, with the first maps generated by targeted genotyping of microsatellites or other nuclear markers (Criscione et al., 2009; Sallé et al. (2019) for evidence of selection in region surrounding β-tubulin isotype 1. Also found elevated F ST in a region on chromosome 5 that was found associated with ivermectin resistance in a linkage mapping study (Doyle et al., 2019a) H. contortus [8] F ST and Fisher's exact test between ivermectin pre-treatment and post-treatment groups collected from a Swedish sheep farm with suspected treatment failure. ...
Next generation sequencing technologies have facilitated a shift from a few targeted loci in population genetic studies to whole genome approaches. Here, we review the types of questions and inferences regarding the population biology and evolution of parasitic helminths being addressed within the field of population genomics. Topics include parabiome, hybridization, population structure, loci under selection and linkage mapping. We highlight various advances, and note the current trends in the field, particularly a focus on human-related parasites despite the inherent biodiversity of helminth species. We conclude by advocating for a broader application of population genomics to reflect the taxonomic and life history breadth displayed by helminth parasites. As such, our basic knowledge about helminth population biology and evolution would be enhanced while the diversity of helminths in itself would facilitate population genomic comparative studies to address broader ecological and evolutionary concepts.
... Furthermore, research that used the RNAi approach to silence genes revealed the relevance of these certain proteins for parasite proliferation and survival [87]. Using mass spectrometry (MS)-based proteomics and information from the genome, transcriptome, and genetic maps, similar membrane protein was found in adult worm tegument preparations [88]. ...
The present study was carryout to review the antigens of three (3) medically important Schistosomes namely: Schistosoma mansoni, S. haematobium, and S. japonicum. The parasites-host relationship, the antigens, the species that produce the antigens, and the functions of the antigens were discussed. Identified antigens include: Sm-24 kDa, Sm108 kDa, Polymorphic mucins, 28/30 kDa Protease, 47 kDa protease, 60 kDa protease, Cercarial Elastase (CE) also called 28/30 kDa, Cathepsin, 22.6 kDa, 23 kDa, 16 kDa/SLP/SPO-1, Prostaglandin E2 (PGE2), SmEnolase, SmCalp1, 28-kD GST (rSh28GST), 29-kDa, Calpain (Sp80) and SG3PDH. The above mention antigens of the parasites were found to be much important since they enable them to compete with body immunity while carrying out their metabolic activities, reproduction, growth, defense, resistance, and so many other things within the host. Therefore, these antigens are very important in immunological studies; hence, it was recommended that, Since some parasite antigens were found to be promising candidates for developing a vaccine to protect against Schistosoma infection, more parasite antigens should be searched for the best planning and development of numerous strategies that aid in the prevention and control of schistosomiasis.
... This article is protected by copyright. All rights reserved Criscione, Valentim, Hirai, LoVerde, & Anderson, 2009) from previous work on S. mansoni. ...
Schistosoma mansoni, a snail‐borne, blood fluke that infects humans, was introduced into the Americas from Africa during the Trans‐Atlantic slave trade. As this parasite shows strong specificity to the snail intermediate host, we expected that adaptation to S. American Biomphalaria spp. snails would result in population bottlenecks and strong signatures of selection. We scored 475,081 single nucleotide variants (SNVs) in 143 S. mansoni from the Americas (Brazil, Guadeloupe, and Puerto Rico) and Africa (Cameroon, Niger, Senegal, Tanzania, and Uganda), and used these data to ask: (i) Was there a population bottleneck during colonization? (ii) Can we identify signatures of selection associated with colonization? And (iii) what were the source populations for colonizing parasites? We found a 2.4‐2.9‐fold reduction in diversity and much slower decay in linkage disequilibrium (LD) in parasites from East to West Africa. However, we observed similar nuclear diversity and LD in West Africa and Brazil, suggesting no strong bottlenecks and limited barriers to colonization. We identified five genome regions showing selection in the Americas, compared with three in West Africa and none in East Africa, which we speculate may reflect adaptation during colonization. Finally, we infer that unsampled populations from central African regions between Benin and Angola, with contributions from Niger, are likely the major source(s) for Brazilian S. mansoni. The absence of a bottleneck suggests that this is a rare case of a serendipitous invasion, where S. mansoni parasites were pre‐adapted to the Americas and able to establish with relative ease.
... Furthermore, research that used the RNAi approach to silence genes revealed the relevance of these certain proteins for parasite proliferation and survival [87]. Using mass spectrometry (MS)-based proteomics and information from the genome, transcriptome, and genetic maps, similar membrane protein was found in adult worm tegument preparations [88]. ...
The present study was carryout to review the antigens of three (3) medically important Schistosomes namely: Schistosoma mansoni, S. haematobium, and S. japonicum. The parasites-host relationship, the antigens, the species that produce the antigens, and the functions of the antigens were discussed. Identified antigens include: Sm-24 kDa, Sm108 kDa, Polymorphic mucins, 28/30 kDa Protease, 47 kDa protease, 60 kDa protease, Cercarial Elastase (CE) also called 28/30 kDa, Cathepsin, 22.6 kDa, 23 kDa, 16 kDa/SLP/SPO-1, Prostaglandin E2 (PGE2), SmEnolase, SmCalp1, 28-kD GST (rSh28GST), 29-kDa, Calpain (Sp80) and SG3PDH. The above mention antigens of the parasites were found to be much important since they enable them to compete with body immunity while carrying out their metabolic activities, reproduction, growth, defense, resistance, and so many other things within the host. Therefore, these antigens are very important in immunological studies; hence, it was recommended that, Since some parasite antigens were found to be promising candidates for developing a vaccine to protect against Schistosoma infection, more parasite antigens should be searched for the best planning and development of numerous strategies that aid in the prevention and control of schistosomiasis.
... Detection of genome-wide signatures of selection. Statistical phasing was performed using Beagle (v.5.0) and a recombination map based on perchromosome recombination rate estimates from Criscione et al. 128,129 . The effective population size was set at 65,000 based on estimates by Crellen et al. 17 . ...
Control and elimination of the parasitic disease schistosomiasis relies on mass administration of praziquantel. Whilst these programmes reduce infection prevalence and intensity, their impact on parasite transmission and evolution is poorly understood. Here we examine the genomic impact of repeated mass drug administration on Schistosoma mansoni populations with documented reduced praziquantel efficacy. We sequenced whole-genomes of 198 S. mansoni larvae from 34 Ugandan children from regions with contrasting praziquantel exposure. Parasites infecting children from Lake Victoria, a transmission hotspot, form a diverse panmictic population. A single round of treatment did not reduce this diversity with no apparent population contraction caused by long-term praziquantel use. We find evidence of positive selection acting on members of gene families previously implicated in praziquantel action, but detect no high frequency functionally impactful variants. As efforts to eliminate schistosomiasis intensify, our study provides a foundation for genomic surveillance of this major human parasite.
... In our work we used pooled samples and found that tri-and tetramer repeats provided the most satisfactory profiles. To date, there are 52 unique tri-and tetrameric microsatellite markers published for S. mansoni (Durand et al., 2000;Curtis et al., 2001;Rodrigues et al., 2002aRodrigues et al., , 2002bRodrigues et al., , 2007Silva et al., 2006;Criscione et al., 2009;Blank et al., 2010;Blanton et al., 2011). Although whole genome sequence and single nucleotide variations offer increased resolution, the numbers of samples that can be processed for epidemiological purposes is still very limited. ...
All Schistosoma mansoni tri- and tetranucleotide repeat microsatellites published as of December 2018 were identified. All 52 were evaluated for autosomal location, strength of amplification, scorability and behavior as single-copy loci by polyacrylamide and capillary gel electrophoresis. Of these, 27 were unique, autosomal, polymorphic, easily scored and single copy as assessed on pooled adult worm DNA from two different continental origins and adult worm clones. These microsatellites were distributed across all seven autosomal chromosomes. On laboratory strains their heterozygosity ranged from 0.22 – 0.77. Individual markers had 5-13 alleles, allelic richness of 2-10 and an effective allele number of 1.3-8.14. Those infected by Schistosoma mansoni carry many genetically distinct, sexually reproducing parasites, therefore, for an individual infection the complete allele frequency profile of their progeny consists of a pool of DNA from multiple diploid eggs. Using a set of 25 microsatellites, we calculated allele frequency profiles of eggs in fecal samples from people in two Brazilian communities separated by 6 km: Jenipapo (n=80) and Volta do Rio (n=38). There were no a priori characteristics that could predict the performance of markers in natural infections based on their performance with laboratory strains. Increasing marker number did not change accuracy for differentiation and diversity but did improve precision. Our data suggest that using a random set of 10-20 microsatellites appears to result in values that exhibit low standard deviations for diversity and differentiation indices. All identified microsatellites as well as PCR conditions, allele size, primer sequences and references for all tri- and tetramer microsatellites markers presented in this work are available at: https://sites.google.com/case.edu/cwru-and-fiocruz-wdrc/home.
... They are abundant and primarily located in noncoding regions of the genome. In the human genome, these repeats occur, on average, every 15,000 bases (40), and hundreds have been identified in the genomes of schistosomes (41,42). Microsatellites tend to vary stepwise in size, so a series of trinucleotide repeats varies by multiples of three and tetranucleotide repeats by four, etc. ...
Population Structure and Dynamics of Helminthic Infection: Schistosomiasis * , Page 1 of 2
Abstract
While disease and outbreaks are mainly clonal for bacteria and other asexually reproducing organisms, sexual reproduction in schistosomes and other helminths usually results in unique individuals. For sexually reproducing organisms, the traits conserved in clones will instead be conserved in the group of organisms that tends to breed together, the population. While the same tools are applied to characterize DNA, how results are interpreted can be quite different at times (see another article in this collection, http://www.asmscience.org/content/journal/microbiolspec/10.1128/microbiolspec.AME-0002-2018). It is difficult to know what the real effect any control program has on the parasite population without assessing the health of this population, how they respond to the control measure, and how they recover, if they do. This review, part of the Microbiology Spectrum Curated Collection: Advances in Molecular Epidemiology of Infectious Diseases, concentrates on one approach using pooled samples to study schistosome populations and shows how this and other approaches have contributed to our understanding of this parasite family’s biology and epidemiology. *This article is part of a curated collection.
... These should complement also new approaches for drug screening, such as that being developed in vitro that may enable a more logical and cost-effective approach to the design of antischistosomal drugs (Abdulla et al. 2009). For example, a 5 cM genetic map for S. mansoni was developed to allow genetic studies to identify genes that control phenotypes (Criscione et al. 2009). Using the genetic map, RNAi and biochemical assays, the gene responsible for oxamniquine (OXA) drug resistance was identified. ...
Schistosomiasis is a major cause of morbidity in the world; it is second only to malaria as a major infectious disease. Globally, it is estimated that the disease affects over 250 million people in 78 countries of the world and is responsible for some 280,000 deaths each year. The three major schistosomes infecting humans are Schistosoma mansoni, S. japonicum, and S. haematobium. This chapter covers a wide range of aspects of schistosomiasis, including basic biology of the parasites, epidemiology, immunopathology, treatment, control, vaccines, and genomics/proteomics. In this chapter, the reader will understand the significant toll this disease takes in terms of mortality and morbidity. A description of the various life stages of schistosomes is presented, which will be informative for both those unfamiliar with the disease and experienced scientists. Clinical and public health aspects are addressed that cover acute and chronic disease, diagnosis, current treatment regimens and alternative drugs, and schistosomiasis control programs. A brief overview of genomics and proteomics is included that details recent advances in the field that will help scientists investigate the molecular biology of schistosomes. The reader will take away an appreciation for general aspects of schistosomiasis and research advances.
... Using mutation (8.1e À9 /bp/generation) and recombination rates (244.2 kb/cM), reported for S. mansoni (Criscione et al. 2009;Crellen et al. 2016), we estimated the time since divergence of the 23-kb target region in the Nigerien haplotypes to be 476 generations ago (437.9-616.6; 95% CI; fig. ...
Introgression among parasite species has the potential to transfer traits of biomedical importance across species boundaries. The parasitic blood fluke Schistosoma haematobium causes urogenital schistosomiasis in humans across sub-Saharan Africa. Hybridization with other schistosome species is assumed to occur commonly, because genetic crosses between S. haematobium and livestock schistosomes, including S. bovis, can be staged in the laboratory, and sequencing of mtDNA and rDNA amplified from microscopic miracidia larvae frequently reveals markers from different species. However the frequency, direction, age and genomic consequences of hybridization are unknown. We hatched miracidia from eggs, and sequenced the exomes from 96 individual S. haematobium miracidia from infected patients from Niger and the Zanzibar archipelago. These data revealed no evidence for contemporary hybridization between S. bovis and S. haematobium in our samples. However, all Nigerien S. haematobium genomes sampled show hybrid ancestry, with 3.3-8.2% of their nuclear genomes derived from S. bovis, providing evidence of an ancient, introgression event that occurred at least 108-613 generations ago. Some S. bovis derived alleles have spread to high frequency or reached fixation and show strong signatures of directional selection; the strongest signal spans a single gene in the invadolysin gene family (Chr. 4). Our results suggest that S. bovis/S. haematobium hybridization occurs rarely, but demonstrate profound consequences of ancient introgression from a livestock parasite into the genome of S. haematobium, the most prevalent schistosome species infecting humans.
... Assembly was problematic because $40% of the genome consists of repetitive regions and transposable elements. To help resolve this problem, we conducted a three-generation genetic cross, and genotyped parents, F1s and multiple F2s, using 243 microsatellite markers [64]. We placed these markers in the 203 longest scaffolds in the draft genome to maximize the amount of the genome assembled. ...
... Furthermore, exome sequence can be unambiguously aligned, and is easier to store and manipulate than WGS data. [64] generated using a genetic cross allows unordered scaffolds assembled from short-read genome sequences to be anchored and ordered to chromosomes (only chr. 6 is shown here). ...
Linkage mapping - utilizing experimental genetic crosses to examine cosegregation of phenotypic traits with genetic markers - is now 100 years old. Schistosome parasites are exquisitely well suited to linkage mapping approaches because genetic crosses can be conducted in the laboratory, thousands of progeny are produced, and elegant experimental work over the last 75 years has revealed heritable genetic variation in multiple biomedically important traits such as drug resistance, host specificity, and virulence. Application of this approach is timely because the improved genome assembly for Schistosoma mansoni and developing molecular toolkit for schistosomes increase our ability to link phenotype with genotype. We describe current progress and potential future directions of linkage mapping in schistosomes.
