Abstract

BackgroundThe trematode flatworms of the genus Schistosoma, the causative agents of schistosomiasis, are among the most prevalent parasites in humans, affecting more than 200 million people worldwide. In this study, we focused on two well-characterized strains of S. mansoni, to explore signatures of selection. Both strains are highly inbred and exhibit differences in life history traits, in particular in their compatibility with the intermediate host Biomphalaria glabrata.Methodology/Principal FindingsWe performed high throughput sequencing of DNA from pools of individuals of each strain using Illumina technology and identified single nucleotide polymorphisms (SNP) and copy number variations (CNV). In total, 708,898 SNPs were identified and roughly 2,000 CNVs. The SNPs revealed low nucleotide diversity (π = 2×10−4) within each strain and a high differentiation level (Fst = 0.73) between them. Based on a recently developed in-silico approach, we further detected 12 and 19 private (i.e. specific non-overlapping) selective sweeps among the 121 and 151 sweeps found in total for each strain.Conclusions/SignificanceFunctional annotation of transcripts lying in the private selective sweeps revealed specific selection for functions related to parasitic interaction (e.g. cell-cell adhesion or redox reactions). Despite high differentiation between strains, we identified evolutionary convergence of genes related to proteolysis, known as a key virulence factor and a potential target of drug and vaccine development. Our data show that pool-sequencing can be used for the detection of selective sweeps in parasite populations and enables one to identify biological functions under selection.

Highlights

  • In addition to their obvious importance as threats to physical and economical well-being, parasites constitute an interesting group of organisms in which to investigate adaptation and selection

  • A comparison of the epigenomes of both strains had identified differences in chromatin structure in several loci, among them a metalloprotease of the neutral endopeptidase (NEP) family potentially involved in immuno-modulation of B. glabrata [12]

  • We identified the presence of (i) a member of immunophilins, a large group of proteins with peptidyl prolyl-isomerase activity (PPI-ase) that exhibit high specificity in binding to immunosuppressive agents; (ii) a homolog of SPARC, a secreted glycoprotein involved in interactions between cells and extracellular matrix [47], both with a higher copy numbers in BRE, and (iii) a M13 family peptidase, a type II membrane metallo-endopeptidase acting on extracellular substrates [48], belonging to a family of proteases for which another member was identified to be epigenetically different between the two strains [12]

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Summary

Introduction

In addition to their obvious importance as threats to physical and economical well-being, parasites constitute an interesting group of organisms in which to investigate adaptation and selection. Any change in a host population, which for example decreases parasite ability to penetrate host tissue, will reciprocally select for a change in the parasite such as mechanisms favouring evasion of host resistance to infection. Such an evolutionary arms race [1,2] has been well studied in Schistosoma mansoni during the interaction with its intermediate host snail [3,4,5,6]. We focused on two well-characterized strains of S. mansoni, to explore signatures of selection Both strains are highly inbred and exhibit differences in life history traits, in particular in their compatibility with the intermediate host Biomphalaria glabrata

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