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African schistosomes in small mammal communities: perspectives from a spatial-temporal survey in the vicinity of Lake Guiers, Senegal.&nbsp

When two species hybridize, the two parental genomes are brought together and some alleles might interact for the first time. To the date, the extent of the transcriptomic changes in first hybrid generations, along with their functional outcome constitute an important knowledge gap especially in non-model organisms. Here we explored the molecular and functional outcomes of hybridization in first-generation hybrid between the blood fluke parasitesS. haematobiumandS. bovis. To this aim we fist assembled a hybrid reference transcriptome allowing us to measure gene expression in both parental species and hybrids to further described and quantified the profiles of gene expression encountered in hybrids. We identified large-scale gene expression remodeling since up to 55% of genes were differentially expressed in hybrids compared to at least one of the parental species. We further showed that intermediate level of expression in hybrids compared to parental species was the most prevalent expression profile (38% of genes) in agreement withS. haematobium x S. bovishigh genomic compatibility and limited divergence. Also, among the differentially expressed genes of each of the identified profiles (intermediate, under-, over-expressed, or matching the expression of one of the parental species), only a few biological processes were found enriched without patterns being consistent through crosses and sexes. Our findings suggest that hybrid heterosis could be due to change in expression of a large portion of random genes which affect various biological processes.Author SummaryWhen two species manage to produce a viable offspring, due to different parental genetic material, new allelic interactions might arise. We do not know much about how genes are expressed in such hybrids compared to their parental species and especially for non-model species. Here we gene expressions in first generation hybrids of two blood flukes’ parasitesSchistosoma haematobiumandS. bovis.We quantified and categorized gene differentially expressed in first generation hybrids. We showed that more than half the genes of the hybrids were differentially expressed compared to at least one of their parental species, hence showing major gene expression remodeling occurring during hybridization. However, the most common hybrid expression pattern was intermediate level of expression compared to parental species and various but no specific biological processes were associated with hybrids differentially expressed genes. We hypothesized that becauseS. haematobiumandS. bovisremain very compatible, when hybridizing many non-specific genes can have their expression level remodeled hence impacting the overall molecular machinery of the offspring while still sustaining highly operational hybrids.

Contrary to the majority of other Trematoda

Species usually develop reproductive isolation mechanisms allowing them to avoid interbreeding. These preventive barriers can act before reproduction, “pre-zygotic barriers”, or after reproduction, “post-zygotic barriers”. Pre-zygotic barriers prevent unfavourable mating, while post-zygotic barriers determine the viability and selective success of the hybrid offspring. Hybridization in parasites and the underlying reproductive isolation mechanisms maintaining their genetic integrity have been overlooked. Using an integrated approach this work aims to quantify the relative importance of pre-zygotic barriers in Schistosoma haematobium x S. bovis crosses. These two co-endemic species cause schistosomiasis, one of the major debilitating parasitic diseases worldwide, and can hybridize naturally. Using mate choice experiments we first tested if a specific mate recognition system exists between both species. Second, using RNA-sequencing we analysed differential gene expression between homo- and hetero-specific pairing in male and female adult parasites. We show that homo- and hetero-specific pairing occurs randomly between these two species, and few genes in both sexes are affected by hetero-specific pairing. This suggests that i) mate choice is not a reproductive isolating factor, and that ii) no pre-zygotic barrier except spatial isolation “by the final vertebrate host” seems to limit interbreeding between these two species. Interestingly, among the few genes affected by the pairing status of the worms, some can be related to pathways affected during male and female interactions and may also present interesting candidates for species isolation mechanisms and hybridization in schistosome parasites., Author summary Understanding how species maintain their genetic integrity is a central question in evolutionary biology. While isolation mechanisms are well documented in free-living organisms, it is currently not the case for parasite species. Yet, occurrence of parasite hybrids is a critical global health concern since these hybrids are expected to be more harmful than parental species. We addressed the question of reproductive isolation mechanisms in parasitic species by conducting an integrative experimental study (from mate choice to gene expression) on two schistosome species (Schistosoma haematobium and S. bovis) that parasitize human and cattle, respectively. Importantly, their hybrid progeny has been involved in recent outbreaks, including outbreaks outside of endemic areas. We showed that rather than having a homo-specific mate choice, S. haematobium and S. bovis mate randomly. Also, male and female worms only express a few genes differentially when involved in a hetero-specific pair compared to a homo-specific pair. We consequently suggest that these two schistosome species lack strong reproduction isolation mechanisms, except those imposed by specificity to the final host species. Our results raise the concern that in the absence of post-zygotic barriers in sympatric zones hybridization might be more common than previously thought if these two species are able to encounter each other.

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., Author summary 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 comparative genomic study to assess the genomic diversity within S. haematobium and S. bovis species and genetic differentation at the genome scale between these two sister species over the African continent. We also investigated traces of possible ancient introgression from one species to another. We found that S. haematobium display low genetic diversity compared to S. bovis. We also found that most S. haematobium samples harbor signature of past introgression with S. bovis at some genomic positions. Our results strongly suggest that introgression occurred long time ago and that such introgression is unidirectional from S. bovis within S. haematobium. Such introgresssion event(s) result in diverging patterns of genomic introgression across S. haematobium lineages.

15 páginas, 3 figuras y 2 tablas., Environmental and anthropogenic changes are expected to promote emergence and spread of pathogens worldwide. Since 2013, human urogenital schistosomiasis is established in Corsica island (France). Schistosomiasis is a parasitic disease affecting both humans and animals. The parasite involved in the Corsican outbreak is a hybrid form between Schistosoma haematobium, a human parasite, and Schistosoma bovis, a livestock parasite. S. bovis has been detected in Corsican livestock few decades ago raising the questions whether hybridization occurred in Corsica and if animals could behave as a reservoir for the recently established parasite lineage. The latter hypothesis has huge epidemiological outcomes since the emergence of a zoonotic lineage of schistosomes would be considerably harder to control and eradicate the disease locally and definitively needs to be verified. In this study we combined a sero-epidemiological survey on ruminants and a rodent trapping campaign to check whether schistosomes could shift on vertebrate hosts other than humans. A total of 3,519 domesticated animals (1,147 cattle; 671 goats and 1,701 sheep) from 160 farms established in 14 municipalities were sampled. From these 3,519 screened animals, 17 were found to be serologically positive but were ultimately considered as false positive after complementary analyses. Additionally, our 7-day extensive rodent trapping (i.e. 1,949 traps placed) resulted in the capture of a total of 34 rats (Rattus rattus) and 4 mice (Mus musculus). Despite the low number of rodents captured, molecular diagnostic tests showed that two of them have been found to be infected by schistosomes. Given the low abundance of rodents and the low parasitic prevalence and intensity among rodents, it is unlikely that neither rats nor ruminants play a significant role in the maintenance of schistosomiasis outbreak in Corsica. Finally, the most likely hypothesis is that local people initially infected in 2013 re-contaminated the river during subsequent summers, however we cannot definitively rule out the possibility of an animal species acting as reservoir host., JB received a grant from the ANSES (Agence nationale de sécurité sanitaire de l’alimentation, de l’environnement et du travail) (https://www.anses.fr/fr). This study is set within the framework of the "Laboratoire d’Excellence (LABEX)" TULIP (ANR-10-LABX-41).

International audience; Schistosomiasis is frequently detected in persons entering Europe. In 2017, we detected a Schistosoma mansoni-Schistosoma haematobium hybrid parasite infection in a migrant boy from Côte d'Ivoire entering France. Because such parasites might be established in Europe, as illustrated by an outbreak on Corsica Island, vectors of these parasites should be investigated.

Schistosomes cause schistosomiasis, the world’s second most important parasitic disease after malaria. A peculiar feature of schistosomes is their ability to produce viable and fertile hybrids. Originally only present in the tropics, schistosomiasis is now also endemic in Europe. Based on two genetic markers the European species had been identified as a hybrid between the ruminant-infective Schistosoma bovis and the human-infective Schistosoma haematobium.Here we describe for the first time the genomic composition of the European schistosome hybrid (77% of S. haematobium and 23% of S. bovis origins), its morphometric parameters and its compatibility with the European vector snail and intermediate host Compatibility is a key parameter for the parasites life cycle progression. We also show that egg morphology (a classical diagnostic parameter) does not allow for differential diagnosis while genetic tests do so. Additionally, we performed genome assembly improvement and annotation of S. bovis, the parental species for which no satisfactory genome assembly was available.For the first time since the discovery of hybrid schistosomes, these results reveal at the whole genomic level a complex admixture of parental genomes highlighting (i) the high permeability of schistosomes to other species’ alleles, and (ii) the importance of hybrid formation for pushing species boundaries not only conceptionally but also geographically.

Schistosomes are the causative agents of schistosomiasis, a neglected tropical disease affecting over 230 million people worldwide. Additionally to their major impact on human health, they are also models 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 ZW females), as well 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, molecular mechanisms such as sex-biased gene expression could occur, but parent-of-origin gene expression also provides an alternative. In this work we investigated the latter mechanism, 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 in male and female transcriptomes were situated in genes that have the potential to explain sexual differences in schistosome parasites. Furthermore, we identified and validated four new Z-specific scaffolds.

Summary Background Schistosomiasis is a snail-borne parasitic disease endemic in several tropical and subtropical countries. However, in the summer of 2013, an unexpected outbreak of urogenital schistosomiasis occurred in Corsica, with more than 120 local people or tourists infected. We used a multidisciplinary approach to investigate the epidemiology of urogenital schistosomiasis in Corsica, aiming to elucidate the origin of the outbreak. Methods We did parasitological and malacological surveys at nine potential sites of infection. With the snails found, we carried out snail–parasite compatibility experiments by exposing snails to schistosome larvae recovered from the urine of a locally infected Corsican patient. Genetic analysis of both mitochondrial ( cox1 ) and nuclear (internal transcribed spacer) DNA data from the Schistosoma eggs or miracidia recovered from the infected patients was conducted to elucidate the epidemiology of this outbreak. Findings We identified two main infection foci along the Cavu River, with many Bulinus truncatus snails found in both locations. Of the 3544 snails recovered across all sites, none were naturally infected, but laboratory-based experimental infections confirmed their compatibility with the schistosomes isolated from patients. Molecular characterisation of 73 eggs or miracidia isolated from 12 patients showed infection with Schistosoma haematobium, S haematobium–Schistosoma bovis hybrids, and S bovis . Further sequence data analysis also showed that the Corsican schistosomes were closely related to those from Senegal in west Africa. Interpretation The freshwater swimming pools of the Cavu River harbour many B truncatus snails, which are capable of transmitting S haematobium -group schistosomes. Our molecular data suggest that the parasites were imported into Corsica by individuals infected in west Africa, specifically Senegal. Hybridisation between S haematobium and the cattle schistosome S bovis had a putative role in this outbreak, showing how easily and rapidly urogenital schistosomiasis can be introduced and spread into novel areas where Bulinus snails are endemic, and how hybridisation could increase the colonisation potential of schistosomes. Furthermore our results show the potential risk of schistosomiasis outbreaks in other European areas, warranting close monitoring and surveillance of all potential transmission foci. Funding WHO, ANSES, RICET, and the Ministry of Health and Consumption.

11 páginas, 2 tablas, 1 figura, For scientists working on gonochoric organisms, determining sex can be crucial for many biological questions and experimental studies, such as crossbreeding, but it can also be a challenging task, particularly when no sexual dimorphism is visible or cannot be directly observed. In metazoan parasites of the genus Schistosoma responsible for schistosomiasis, sex is genetically determined in the zygote with a female heterogametic ZW/ZZ system. Adult flukes have a pronounced sexual dimorphism, whereas the sexes of the larval stages are morphologically indistinguishable but can be distinguished uniquely by using molecular methods. Therefore, reliable methods are needed to identify the sex of larvae individuals. Here, we present an endpoint PCR-based assay using female-specific sequences identified using a genome-wide comparative analysis between males and females. This work allowed us to identify sex-markers for Schistosoma haematobium and Schistosoma bovis but also the hybrid between both species that has recently emerged in Corsica (France). Five molecular sex-markers were identified and are female-specific in S. haematobium and the hybrid parasite, whereas three of them are also female-specific in S. bovis. These molecular markers will be useful to conduct studies, such as experimental crosses on these disease-causing blood flukes, which are still largely neglected but no longer restricted to tropical areas.

International audience; La schistosomiase, ou bilharziose, est une maladie parasitaire tropicale et subtropicale causée par des parasites qui habitent les vaisseaux sanguins humains et sont transmis par des mollusques d’eau douce spécifiques. L’infection humaine se produit par la pénétration transcutanée du stade larvaire infectieux du parasite émis par le mollusque vecteur, dans l’eau de baignade.