Parent-of-origin-dependent gene expression in male and female schistosome parasites

Abstract

Schistosomes are the causative agents of schistosomiasis, a neglected tropical disease affecting over 230 million peopleworldwide. Additionally to theirmajor impact onhuman health, they are alsomodels of choice in evolutionary biology. These parasitic flatworms are unique among the common hermaphroditic trematodes as they have separate sexes. This so-called "evolutionary scandal" displays a female heterogametic genetic sex-determination system(ZZ males and ZWfemales), aswell as a pronounced adult sexual dimorphism. These phenotypic differences are determined by a shared set of genes in both sexes, potentially leading to intralocus sexual conflicts. To resolve these conflicts in sexually selected traits,molecularmechanisms such as sex-biased gene expression could occur, but parent-of-origin gene expression also provides an alternative. In this work we investigated the lattermechanism, that is, genes expressed preferentially from either the maternal or the paternal allele, in Schistosoma mansoni species. To this end, transcriptomes from male and female hybrid adults obtained by strain crosses were sequenced. Strain-specific single nucleotide polymorphism (SNP) markers allowed us to discriminate the parental origin, while reciprocal crosses helped to differentiate parental expression from strain-specific expression.We identified genes containing SNPs expressed in a parent-of-origin manner consistent with paternal and maternal imprints. Although the majority of the SNPs was identified in mitochondrial and Z-specific loci, the remaining SNPs found inmale and female transcriptomeswere situated in genes that have the potential to explain sexual differences in schistosome parasites. Furthermore, we identified and validated four new Z-specific scaffolds.