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

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.

Frontloading of stress response genes enhances robustness to environmental change in chimeric corals.

BACKGROUND: Chimeras are genetically mixed entities resulting from the fusion of two or more conspecifics. This phenomenon is widely distributed in nature and documented in a variety of animal and plant phyla. In corals, chimerism initiates at early ontogenic states (larvae to young spat) and results from the fusion between two or more closely settled conspecifics. When compared to genetically homogenous colonies (non-chimeras), the literature has listed ecological and evolutionary benefits for traits at the chimeric state, further positioning coral chimerism as an evolutionary rescue instrument. However, the molecular mechanisms underlying this suggestion remain unknown. RESULTS: To address this question, we developed field monitoring and multi-omics approaches to compare the responses of chimeric and non-chimeric colonies acclimated for 1 year at 10-m depth or exposed to a stressful environmental change (translocation from 10- to 2-m depth for 48h). We showed that chimerism in the stony coral Stylophora pistillata is associated with higher survival over a 1-year period. Transcriptomic analyses showed that chimeras lose transcriptomic plasticity and constitutively express at higher level (frontload) genes responsive to stress. This frontloading may prepare the colony to face at any time environmental stresses which explain its higher robustness. CONCLUSIONS: These results show that chimeras are environmentally robust entities with an enhanced ability to cope with environmental stress. Results further document the potential usefulness of chimeras as a novel reef restoration tool to enhance coral adaptability to environmental change, and confirm that coral chimerism can be an evolutionary rescue instrument.

Developing Endemicity of Schistosomiasis, Corsica, France.

Urogenital schistosomiasis was diagnosed in a man from Germany who had never traveled outside Europe. He likely acquired the infection in Corsica, France, but did not swim in the Cavu River, which was linked to a previous outbreak. This case highlights that transmission of schistosomiasis in Corsica is ongoing.

Sympatric versus allopatric evolutionary contexts shape differential immune response in Biomphalaria / Schistosoma interaction.

Selective pressures between hosts and their parasites can result in reciprocal evolution or adaptation of specific life history traits. Local adaptation of resident hosts and parasites should lead to increase parasite infectivity/virulence (higher compatibility) when infecting hosts from the same location (in sympatry) than from a foreign location (in allopatry). Analysis of geographic variations in compatibility phenotypes is the most common proxy used to infer local adaptation. However, in some cases, allopatric host-parasite systems demonstrate similar or greater compatibility than in sympatry. In such cases, the potential for local adaptation remains unclear. Here, we study the interaction between Schistosoma and its vector snail Biomphalaria in which such discrepancy in local versus foreign compatibility phenotype has been reported. Herein, we aim at bridging this gap of knowledge by comparing life history traits (immune cellular response, host mortality, and parasite growth) and molecular responses in highly compatible sympatric and allopatric Schistosoma/Biomphalaria interactions originating from different geographic localities (Brazil, Venezuela and Burundi). We found that despite displaying similar prevalence phenotypes, sympatric schistosomes triggered a rapid immune suppression (dual-RNAseq analyses) in the snails within 24h post infection, whereas infection by allopatric schistosomes (regardless of the species) was associated with immune cell proliferation and triggered a non-specific generalized immune response after 96h. We observed that, sympatric schistosomes grow more rapidly. Finally, we identify miRNAs differentially expressed by Schistosoma mansoni that target host immune genes and could be responsible for hijacking the host immune response during the sympatric interaction. We show that despite having similar prevalence phenotypes, sympatric and allopatric snail-Schistosoma interactions displayed strong differences in their immunobiological molecular dialogue. Understanding the mechanisms allowing parasites to adapt rapidly and efficiently to new hosts is critical to control disease emergence and risks of Schistosomiasis outbreaks.

Differential basal expression of immune genes confers Crassostrea gigas resistance to Pacific oyster mortality syndrome.

BACKGROUND: As a major threat to the oyster industry, Pacific Oyster Mortality Syndrome (POMS) is a polymicrobial disease affecting the main oyster species farmed across the world. POMS affects oyster juveniles and became panzootic this last decade, but POMS resistance in some oyster genotypes has emerged. While we know some genetic loci associated with resistance, the underlying mechanisms remained uncharacterized. So, we developed a comparative transcriptomic approach using basal gene expression profiles between different oyster biparental families with contrasted phenotypes when confronted to POMS (resistant or susceptible). RESULTS: We showed that POMS resistant oysters show differential expression of genes involved in stress responses, protein modifications, maintenance of DNA integrity and repair, and immune and antiviral pathways. We found similarities and clear differences among different molecular pathways in the different resistant families. These results suggest that the resistance process is polygenic and partially varies according to the oyster genotype. CONCLUSIONS: We found differences in basal expression levels of genes related to TLR-NFκB, JAK-STAT and STING-RLR pathways. These differences could explain the best antiviral response, as well as the robustness of resistant oysters when confronted to POMS. As some of these genes represent valuable candidates for selective breeding, we propose future studies should further examine their function.

High prevalence of Schistosoma haematobium × Schistosoma bovis hybrids in schoolchildren in Côte d'Ivoire.

Schistosomiasis is a neglected tropical disease, though it is highly prevalent in many parts of sub-Saharan Africa. While Schistosoma haematobium-bovis hybrids have been reported in West Africa, no data about Schistosoma hybrids in humans are available from Côte d'Ivoire. This study aimed to identify and quantify S. haematobium-bovis hybrids among schoolchildren in four localities of Côte d'Ivoire. Urine samples were collected and examined by filtration to detect Schistosoma eggs. Eggs were hatched and 503 miracidia were individually collected and stored on Whatman® FTA cards for molecular analysis. Individual miracidia were molecularly characterized by analysis of mitochondrial cox1 and nuclear internal transcribed spacer 2 (ITS 2) DNA regions. A mitochondrial cox1-based diagnostic polymerase chain reaction was performed on 459 miracidia, with 239 (52.1%) exhibiting the typical band for S. haematobium and 220 (47.9%) the S. bovis band. The cox1 and ITS 2 amplicons were Sanger sequenced from 40 randomly selected miracidia to confirm species and hybrids status. Among the 33 cox1 sequences analysed, we identified 15 S. haematobium sequences (45.5%) belonging to seven haplotypes and 18 S. bovis sequences (54.5%) belonging to 12 haplotypes. Of 40 ITS 2 sequences analysed, 31 (77.5%) were assigned to pure S. haematobium, four (10.0%) to pure S. bovis and five (12.5%) to S. haematobium-bovis hybrids. Our findings suggest that S. haematobium-bovis hybrids are common in Côte d'Ivoire. Hence, intense prospection of domestic and wild animals is warranted to determine whether zoonotic transmission occurs.

Cattle as natural host for Schistosoma haematobium (Bilharz, 1852) Weinland, 1858 x Schistosoma bovis Sonsino, 1876 interactions, with new cercarial emergence and genetic patterns.

Schistosomiasis remains a parasitic infection which poses serious public health consequences around the world, particularly on the African continent where cases of introgression/hybridization between human and cattle schistosomiasis are being discovered on a more frequent basis in humans, specifically between Schistosoma haematobium and S. bovis. The aim of this paper is to analyze the occurrence of S. bovis in cattle and its relationship with S. haematobium in an area where cattle and humans share the same site in Benin (West Africa). We used the chronobiology of cercarial emergence as an ecological parameter and both molecular biology (COI mtDNA and ITS rDNA) of the larvae and morphology of the eggs as taxonomic parameters. The results showed a chronobiological polymorphism in the cercarial emergence rhythm. They showed for the first time the presence of S. bovis in Benin, the presence of introgressive hybridization between S. bovis and S. haematobium in domestic cattle, and the presence of atypical chronobiological patterns in schistosomes from cattle, with typical S. haematobium shedding pattern, double-peak patterns, and nocturnal patterns. Our results showed that the chronobiological life-history trait is useful for the detection of new hosts and also may reveal the possible presence of introgressive hybridization in schistosomes. Our results, for the first time, place cattle as reservoir host for S. haematobium and S. bovis x S. haematobium. The consequences of these results on the epidemiology of the disease, the transmission to humans, and the control of the disease are very important.

Schistosoma haematobium-Schistosoma mansoni Hybrid Parasite in Migrant Boy, France, 2017.

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.

A Shift from Cellular to Humoral Responses Contributes to Innate Immune Memory in the Vector Snail Biomphalaria glabrata.

Discoveries made over the past ten years have provided evidence that invertebrate antiparasitic responses may be primed in a sustainable manner, leading to the failure of a secondary encounter with the same pathogen. This phenomenon called "immune priming" or "innate immune memory" was mainly phenomenological. The demonstration of this process remains to be obtained and the underlying mechanisms remain to be discovered and exhaustively tested with rigorous functional and molecular methods, to eliminate all alternative explanations. In order to achieve this ambitious aim, the present study focuses on the Lophotrochozoan snail, Biomphalaria glabrata, in which innate immune memory was recently reported. We provide herein the first evidence that a shift from a cellular immune response (encapsulation) to a humoral immune response (biomphalysin) occurs during the development of innate memory. The molecular characterisation of this process in Biomphalaria/Schistosoma system was undertaken to reconcile mechanisms with phenomena, opening the way to a better comprehension of innate immune memory in invertebrates. This prompted us to revisit the artificial dichotomy between innate and memory immunity in invertebrate systems.

Persistence of schistosomal transmission linked to the Cavu river in southern Corsica since 2013.

Seven cases of urogenital schistosomiasis occurred in Corsica in 2015 and 2016. The episodes were related to exposure to the same river and involved the same parasite strain as an outbreak with 106 cases in summer 2013. The connection calls for further investigations on the presence of an animal reservoir and the survival of infested snails during winter. However, recontamination of the river from previously infected bathers remains the most likely hypothesis.

Biomphalysin, a new ß pore-forming toxin involved in Biomphalaria glabrata immune defense against Schistosoma mansoni.

Aerolysins are virulence factors belonging to the ß pore-forming toxin (ß-PFT) superfamily that are abundantly distributed in bacteria. More rarely, ß-PFTs have been described in eukaryotic organisms. Recently, we identified a putative cytolytic protein in the snail, Biomphalaria glabrata, whose primary structural features suggest that it could belong to this ß-PFT superfamily. In the present paper, we report the molecular cloning and functional characterization of this protein, which we call Biomphalysin, and demonstrate that it is indeed a new eukaryotic ß-PFT. We show that, despite weak sequence similarities with aerolysins, Biomphalysin shares a common architecture with proteins belonging to this superfamily. A phylogenetic approach revealed that the gene encoding Biomphalysin could have resulted from horizontal transfer. Its expression is restricted to immune-competent cells and is not induced by parasite challenge. Recombinant Biomphalysin showed hemolytic activity that was greatly enhanced by the plasma compartment of B. glabrata. We further demonstrated that Biomphalysin with plasma is highly toxic toward Schistosoma mansoni sporocysts. Using in vitro binding assays in conjunction with Western blot and immunocytochemistry analyses, we also showed that Biomphalysin binds to parasite membranes. Finally, we showed that, in contrast to what has been reported for most other members of the family, lytic activity of Biomphalysin is not dependent on proteolytic processing. These results provide the first functional description of a mollusk immune effector protein involved in killing S. mansoni.

Introgressive hybridizations of Schistosoma haematobium by Schistosoma bovis at the origin of the first case report of schistosomiasis in Corsica (France, Europe).

This study concerns the first urinary schistosomiasis case observed in Corsica (France, Europe) occurring in a 12-year-old German boy. The aim was to identify the relationship between this Schistosoma haematobium infection and other schistosomes of the Schistosoma group with terminal-spined ova. Morphological and molecular analyses were conducted on the ova. The results showed that the schistosome responsible for the emergence of schistosomiasis in Corsica was due to S. haematobium introgressed by genes from S. bovis.

The abundance of snail hosts mediates the effects of antagonist interactions between trematodes on the transmission of human schistosomes.

BACKGROUND: Combating infectious diseases and halting biodiversity loss are intertwined challenges crucial to ensure global health. Biodiversity can constrain the spread of vector-borne pathogens circulation, necessitating a deeper understanding of ecological mechanisms underlying this pattern. Our study evaluates the relative importance of biodiversity and the abundance of Bulinus truncatus, a major intermediate host for the trematode Schistosoma haematobium on the circulation of this human pathogen at aquatic transmission sites. METHODS: We combined mathematical modelling and a molecular based empirical study to specifically assess the effect of co-infections between S. haematobium and other trematodes within their B. truncatus snail hosts; and B. truncatus abundance at transmission sites, on the production of S. haematobium infective cercariae stages released into the aquatic environment. RESULTS: Our modelling approach shows that more competitive trematode species exploiting B. truncatus as an intermediate host at the transmission site level leads to higher co-infection rates within snail hosts, subsequently reducing the production of S. haematobium cercariae. Conversely, an increase in B. truncatus abundance results in lower co-infection rates, and a higher proportion of S. haematobium cercariae released into the environment. Our empirical data from the field support these findings, indicating a significant negative effect of local trematode species richness (P-value = 0.029; AIC = 14.9) and co-infection rates (P-value = 0.02, AIC = 17.4) on the dominance of S. haematobium based on our GLMM models, while B. truncatus abundance positively influences S. haematobium dominance (P-value = 0.047, AIC = 20.1). CONCLUSIONS: Our study highlights the importance of biodiversity in influencing the transmission of S. haematobium through the effect of antagonistic interactions between trematodes within bulinid snail hosts. This effect intensifies when B. truncatus populations are low, promoting co-infections within snails. In line with the One Health concept, our results suggest that maintaining high level of freshwater biodiversity to sustain global trematode diversity at transmission sites can help reducing the circulation of Schistosoma species locally.

Schistosoma haematobium and Schistosoma bovis first generation hybrids undergo gene expressions changes consistent with species compatibility and heterosis.

When two species hybridize, the two parental genomes are brought together and some alleles might interact for the first time. To date, the extent of the transcriptomic changes in first hybrid generations, along with their functional outcome constitute an important knowledge gap, especially in parasite species. Here we explored the molecular and functional outcomes of hybridization in first-generation hybrids between the blood fluke parasites Schistosoma haematobium and S. bovis. Through a transcriptomic approach, we measured gene expression in both parental species and hybrids. We described and quantified expression profiles encountered in hybrids along with the main biological processes impacted. Up to 7,100 genes fell into a particular hybrid expression profile (intermediate between the parental expression levels, over-expressed, under-expressed, or expressed like one of the parental lines). Most of these genes were different depending on the direction of the parental cross (S. bovis mother and S. haematobium father or the reverse) and depending on the sex. For a given sex and cross direction, the vast majority of genes were hence unassigned to a hybrid expression profile: either they were differentially expressed genes but not typical of any hybrid expression profiles or they were not differentially expressed neither between hybrids and parental lines nor between parental lines. The most prevalent profile of gene expression in hybrids was the intermediate one (24% of investigated genes). These results suggest that transcriptomic compatibility between S. haematobium and S. bovis remains quite high. We also found support for an over-dominance model (over- and under-expressed genes in hybrids compared to parental lines) potentially associated with heterosis. In females in particular, processes such as reproductive processes, metabolism and cell interactions as well as signaling pathways were indeed affected. Our study hence provides new insight on the biology of Schistosoma hybrids with evidences supporting compatibility and heterosis.

MORPHOLOGICAL AND MOLECULAR CHARACTERIZATION OF DICHELYNE (NEOCULLANELLUS) DAKARENSIS N. SP. (NEMATODA: CUCULLANIDAE) PARASITIZING AN ECONOMICALLY IMPORTANT MARINE FISH, THE SOMPAT GRUNT, POMADASYS JUBELINI (PERCIFORMES: HAEMULIDAE), FROM HANN BAY IN DAKAR, SENEGAL.

Nematodes collected from the intestine of sompat grunt Pomadasys jubelini Cuvier, 1830 from Hann Bay in Dakar, Senegal represent a new species described herein as Dichelyne (Neocucullanellus) dakarensis n. sp., and investigated with the use of light and scanning electron microscopy. The new species differs from its congeners based on several characteristics, especially because the subgenus Neocucullanellus is the only 1 that has 2 ceca. In addition, the new species diagnosis is based on the number and arrangement of the caudal papillae as well as the size of the veil of spicules. Morphological data were supported by molecular analysis. Results obtained using SSU rDNA and COI distinguished the present specimens from other cucullanids. Molecular data indicated the close relatedness between the new species and Dichelyne cotylophora Ward and Magath, 1917.

Combining a transcriptomic approach and a targeted metabolomics approach for deciphering the molecular bases of compatibility phenotype in the snail Biomphalaria glabrata toward Schistosoma mansoni.

Biomphalaria glabrata is a freshwater snail and the obligatory intermediate host of Schistosoma mansoni parasite, the etiologic agent of intestinal Schistosomiasis, in South America and Caribbean. Interestingly in such host-parasite interactions, compatibility varies between populations, strains or individuals. This observed compatibility polymorphism is based on a complex molecular-matching-phenotype, the molecular bases of which have been investigated in numerous studies, notably by comparing between different strains or geographical isolates or clonal selected snail lines. Herein we propose to decipher the constitutive molecular support of this interaction in selected non-clonal resistant and susceptible snail strain originating from the same natural population from Brazil and thus having the same genetic background. Thanks to a global RNAseq transcriptomic approach on whole snail, we identified a total of 328 differentially expressed genes between resistant and susceptible phenotypes among which 129 were up-regulated and 199 down-regulated. Metabolomic studies were used to corroborate the RNAseq results. The activation of immune genes and specific metabolic pathways in resistant snails might provide them with the capacity to better respond to parasite infection.

Lepidapedon sereti n. sp. (Digenea: Lepidapedidae) in Coelorinchus sereti (Gadiformes: Macrouridae) from deep waters off Vanuatu.

Lepidapedon sereti n. sp. is described from the macrourid Coelorinchus sereti from the deep water off Vanuatu. It is placed in the Elongatum group and Elongatum subgroup. It differs from the other species described in this subgroup by the distinctly dorsally subterminal excretory pore. It also differs from other species in combinations of size, excretory vesicle length, proportions of forebody, post-testicular region and other metric features. This constitutes the first record of a Lepidapedon (sensu stricto) from the Central Western Pacific Ocean.

Correlating early evolution of parasitic platyhelminths to Gondwana breakup.

Investigating patterns and processes of parasite diversification over ancient geological periods should involve comparisons of host and parasite phylogenies in a biogeographic context. It has been shown previously that the geographical distribution of host-specific parasites of sarcopterygians was guided, from Palaeozoic to Cainozoic times, mostly by evolution and diversification of their freshwater hosts. Here, we propose phylogenies of neobatrachian frogs and their specific parasites (Platyhelminthes, Monogenea) to investigate coevolutionary processes and historical biogeography of polystomes and further discuss all the possible assumptions that may account for the early evolution of these parasites. Phylogenetic analyses of concatenated rRNA nuclear genes (18S and partial 28S) supplemented by cophylogenetic and biogeographic vicariance analyses reveal four main parasite lineages that can be ascribed to centers of diversity, namely Australia, India, Africa, and South America. In addition, the relationships among these biogeographical monophyletic groups, substantiated by molecular dating, reflect sequential origins during the breakup of Gondwana. The Australian polystome lineage may have been isolated during the first stages of the breakup, whereas the Indian lineage would have arisen after the complete separation of western and eastern Gondwanan components. Next, polystomes would have codiverged with hyloid sensu stricto and ranoid frog lineages before the completion of South American and African plate separation. Ultimately, they would have undergone an extensive diversification in South America when their ancestral host families diversified. Therefore, the presence of polystome parasites in specific anuran host clades and in discrete geographic areas reveals the importance of biogeographic vicariance in diversification processes and supports the occurrence and radiation of amphibians over ancient and recent geological periods.

Proctophantastes nettastomatis (Digenea: Zoogonidae) from Vanuatu deep-sea fish: new morphological features, allometric growth, and phenotypic plasticity aspects.

The present paper deals with Proctophantastes nettastomatis (Digenea: Zoogonidae; Lepidophyllinae) found in the intestine of three species of deep-sea fish, Dicrolene longimana (Ophidiidae, Ophidiiformes), Bathyuroconger sp. (Congridae, Anguilliformes), and Venefica tentaculata (Nettastomatidae, Anguilliformes). The fish were collected near the islands of Espiritu Santo, Erromango, and Epi, respectively, in the archipelago of Vanuatu (Southern Pacific Ocean) at depths ranging from 561 to 990 m. Morphological and histological analyses showed that the Vanuatu specimens differ from Proctophantastes abyssorum, Proctophantastes gillissi, Proctophantastes glandulosum, Proctophantastes infundibulum, and Proctophantastes brayi but are close to P. nettastomatis discovered in Suruga Bay, Japan. P. nettastomatis is redescribed based both on the observations of our specimens and of the Japanese holotype and paratype. The morphological variability of the species is described. Morphometric data allowed the identification of positive allometric growth for the hindbody, negative allometric growth for the ventral sucker, and a growth phenotypic plasticity between Ophidiiformes and Anguilliformes definitive hosts.

Natural Interactions between S. haematobium and S. guineensis in the Republic of Benin.

Schistosomiasis is a parasitic disease which affects millions of people around the world, particularly in Africa. In this continent, different species are able to interbreed, like Schistosoma haematobium and Schistosoma guineensis, two schistosome species infecting humans. The Republic of Benin is known to harbor S. haematobium, but its geographical situation in between Nigeria, Mali, and Burkina Faso, where S. guineensis was found, raises the question about the possible presence of S. haematobium/S. guineensis hybrids in this country. We conducted morphological analyses on schistosome eggs and molecular analyses on schistosome larvae (high resolution melting (HRM) analysis and gene sequencing) in order to detect any natural interaction between these two species of schistosomes. The morphological results showed the presence of three egg morphotypes (S. haematobium, S. guineensis, and intermediate). Three genotypes were detected by ITS2 rDNA HRM analysis: S. haematobium, S. guineensis, and hybrid, and their percentages confirmed the results of the morphological analysis. However, sequencing of the CO1 mtDNA gene showed that all the samples from Benin belonged to S. haematobium. Our results provide the first evidence of introgression of S. guineensis genes in S. haematobium in Benin.