Diverging patterns of introgression from Schistosoma bovis across S. haematobium African lineages

Olivier Rey,Eve Toulza,Bonnie L Webster,David Rollinson,Eglantine Mathieu-Begné,Cristian Chaparro,Fiona Allan,Julien Kincaid-Smith,Jean-François Allienne,Jérôme Boissier

doi:10.1371/journal.ppat.1009313

Abstract

Hybridization is a fascinating evolutionary phenomenon that raises the question of how species maintain their integrity. Inter-species hybridization occurs between certain Schistosoma species that can cause important public health and veterinary issues. In particular hybrids between Schistosoma haematobium and S. bovis associated with humans and animals respectively are frequently identified in Africa. Recent genomic evidence indicates that some S. haematobium populations show signatures of genomic introgression from S. bovis. Here, we conducted a genomic comparative study and investigated the genomic relationships between S. haematobium, S. bovis and their hybrids using 19 isolates originating from a wide geographical range over Africa, including samples initially classified as S. haematobium (n = 11), S. bovis (n = 6) and S. haematobium x S. bovis hybrids (n = 2). Based on a whole genomic sequencing approach, we developed 56,181 SNPs that allowed a clear differentiation of S. bovis isolates from a genomic cluster including all S. haematobium isolates and a natural S. haematobium-bovis hybrid. All the isolates from the S. haematobium cluster except the isolate from Madagascar harbored signatures of genomic introgression from S. bovis. Isolates from Corsica, Mali and Egypt harbored the S. bovis-like Invadolysin gene, an introgressed tract that has been previously detected in some introgressed S. haematobium populations from Niger. Together our results highlight the fact that introgression from S. bovis is widespread across S. haematobium and that the observed introgression is unidirectional.

Highlights

Hybridization is ubiquitous within the tree of life that raises the question of how species maintain their integrity [1,2,3]
We could clearly distinguish between isolates categorized as either S. haematobium or S. bovis based on a principal component analysis (i.e. PCA; Fig 2A)
Our study reveals that all the S. haematobium isolates analyzed here except the one from Madagascar, to some extent, harbor signals of introgression from S. bovis and constitute a cluster with very low genetic diversity at the African continent scale

Summary

Introduction

Hybridization is ubiquitous within the tree of life that raises the question of how species maintain their integrity [1,2,3]. Hybridization may often result in the production of nonviable or non-fertile offspring, increasing evidence suggests that certain interspecific crosses produce viable progeny, but those progeny may be more successful than their parental species, at least during the early generations (e.g. hybrid vigor) [4,5]). Genomic introgression resulting from hybridization events may be adaptive when genes and/or alleles from one species are maintained through subsequent generations and backcrosses by natural selection, becoming part of the genomic background [4,6,7]. Several studies suggest that interspecific crosses among parasite species can generate lineages that display increased virulence compared to parental species, possibly leading to atypical pathologies and/or a wider host spectrum [9,10,11] and new epidemiological dynamics [9,12]. Hybridization and introgression events in parasites are likely to pose serious challenges for prevention, control and therapies against parasitic diseases [9]

Methods

Results

Discussion

Conclusion