Ancient Hybridization and Adaptive Introgression of an Invadolysin Gene in Schistosome Parasites.

Roy N Platt,Aidan M Emery,Bonnie L Webster,Frédéric D Chevalier,Marina Mcdew-White,Shaali M Ame,Joanne P Webster,Fiona Allan,Timothy J C Anderson,Winka Le Clec’H,Amina A Hamidou,Amadou Garba,David Rollinson,Beth Shapiro

doi:10.1093/molbev/msz154

Abstract

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.

Highlights

Introgressive hybridization occurs when hybrid offspring repeatedly backcross with one or both parental types, acting as a conduit for genetic exchange between species
Previous studies have suggested that 0-41% of parasites sampled in West African locations have hybrid origins based on mitochondrial and rDNA genotyping (Table 1). This is clearly an underestimate: we found that 100% of S. haematobium miracidia sampled from Niger contain S. bovis ancestry, with 3-8% of autosomal loci derived from S. bovis
Genes involved in immune response (Abi-Rached, et al 2011), pathogen defense (Enard and Petrov 2018), and protection from sun exposure (Dannemann and Kelso 2017) have introgressed from archaic humans as a result of these ancient hybridization events

Summary

Introduction

Introgressive hybridization occurs when hybrid offspring repeatedly backcross with one or both parental types, acting as a conduit for genetic exchange between species. Once present in the “new” genetic background, introgressed loci are broken up through recombination and exposed to selection. Genes impacting skin pigmentation (Vernot and Akey 2014) and immune response (Gittelman, et al 2016) were transferred between Neanderthals and humans during the out-of-Africa migration(s). The gene underlying seasonal coat color changes in snowshoe hares are introgressed from jackrabbits (Jones, et al 2018). Introgression allows for complex phenotypic traits to be quickly introduced into a population over the course of a few generations allowing for rapid adaptation to new environments that may not be possible when relying on mutation or standing variation alone (Hedrick 2013)

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Conclusion