Taxonomy, phylogeny, and biodiversity of Lumbrineridae (Annelida, Polychaeta) from the Central Pacific Clarion-Clipperton Zone.

The DNA taxonomy of six species of the annelid family Lumbrineridae collected from the Clarion-Clipperton Zone (CCZ) in the Central Pacific, an area of potential mining interest for polymetallic nodules, is presented. Lumbrinerids are an ecologically important and understudied annelid family within the deep sea, with many species still undescribed. This study aims to document the taxonomy and biodiversity of the CCZ using specimens collected from the UK-1, OMS, and NORI-D exploration contract areas and Areas of Particular Environmental Interest. Species were identified through a combination of morphological and molecular phylogenetic analysis. We present informal species descriptions associated with voucher specimens, accessible through the Natural History Museum (London) collections, to improve future taxonomic and biodiversity studies of this region. Five taxa in this study had no morphological or genetic matches within the literature and therefore are possibly new to science, but their suboptimal morphological preservation prevented the formalisation of new species. The most abundant taxon Lumbrineridescf.laubieri (NHM_0020) was compared with the holotype of Lumbrinerideslaubieri Miura, 1980 from the deep Northeast Atlantic. Currently no reliable morphological characters separating the Pacific and Atlantic specimens have been found and molecular data from the Atlantic specimens was not available.

How many metazoan species live in the world's largest mineral exploration region?

The global surge in demand for metals such as cobalt and nickel has created unprecedented interest in deep-sea habitats with mineral resources. The largest area of activity is a 6 million km2 region known as the Clarion-Clipperton Zone (CCZ) in the central and eastern Pacific, regulated by the International Seabed Authority (ISA). Baseline biodiversity knowledge of the region is crucial to effective management of environmental impact from potential deep-sea mining activities, but until recently this has been almost completely lacking. The rapid growth in taxonomic outputs and data availability for the region over the last decade has allowed us to conduct the first comprehensive synthesis of CCZ benthic metazoan biodiversity for all faunal size classes. Here we present the CCZ Checklist, a biodiversity inventory of benthic metazoa vital to future assessments of environmental impacts. An estimated 92% of species identified from the CCZ are new to science (436 named species from a total of 5,578 recorded). This is likely to be an overestimate owing to synonyms in the data but is supported by analysis of recent taxonomic studies suggesting that 88% of species sampled in the region are undescribed. Species richness estimators place total CCZ metazoan benthic diversity at 6,233 (+/-82 SE) species for Chao1, and 7,620 (+/-132 SE) species for Chao2, most likely representing lower bounds of diversity in the region. Although uncertainty in estimates is high, regional syntheses become increasingly possible as comparable datasets accumulate. These will be vital to understanding ecological processes and risks of biodiversity loss.

Checklist of newly-vouchered annelid taxa from the Clarion-Clipperton Zone, central Pacific Ocean, based on morphology and genetic delimitation.

Background: We present a checklist of annelids from recent United Kingdom Seabed Resources (UKSR) expeditions (Abyssal Baseline - ABYSSLINE project) to the eastern abyssal Pacific Clarion-Clipperton Zone (CCZ) polymetallic nodule fields, based on DNA species delimitation, including imagery of voucher specimens, Darwin Core (DwC) data and links to vouchered specimen material and new GenBank sequence records. This paper includes genetic and imagery data for 129 species of annelids from 339 records and is restricted to material that is, in general, in too poor a condition to describe formally at this time, but likely contains many species new to science. We make these data available both to aid future taxonomic studies in the CCZ that will be able to link back to these genetic data and specimens and to better underpin ongoing ecological studies of potential deep-sea mining impacts using the principles of FAIR (Findable, Accessible, Interoperable, Reusuable) data and specimens that will be available for all. New information: We include genetic, imagery and all associated metadata in Darwin Core format for 129 species of annelids from the Clarion-Clipperton Zone, eastern abyssal Pacific, with 339 records.

Potential drivers for schistosomiasis persistence: Population genetic analyses from a cluster-randomized urogenital schistosomiasis elimination trial across the Zanzibar islands.

The World Health Organization's revised NTD Roadmap and the newly launched Guidelines target elimination of schistosomiasis as a public health problem in all endemic areas by 2030. Key to meeting this goal is elucidating how selective pressures imposed by interventions shape parasite populations. Our aim was to identify any differential impact of a unique cluster-randomized tri-armed elimination intervention (biannual mass drug administration (MDA) applied alone or in association with either mollusciciding (snail control) or behavioural change interventions) across two Zanzibarian islands (Pemba and Unguja) on the population genetic composition of Schistosoma haematobium over space and time. Fifteen microsatellite loci were used to analyse individual miracidia collected from infected individuals across islands and intervention arms at the start (2012 baseline: 1,522 miracidia from 176 children; 303 from 43 adults; age-range 6-75, mean 12.7 years) and at year 5 (2016: 1,486 miracidia from 146 children; 214 from 25 adults; age-range 9-46, mean 12.4 years). Measures of genetic diversity included allelic richness (Ar), Expected (He) and Observed heterozygosity (Ho), inbreeding coefficient (FST), parentage analysis, estimated worm burden, worm fecundity, and genetic sub-structuring. There was little evidence of differential selective pressures on population genetic diversity, inbreeding or estimated worm burdens by treatment arm, with only the MDA+snail control arm within Unguja showing trends towards reduced diversity and altered inbreeding over time. The greatest differences overall, both in terms of parasite fecundity and genetic sub-structuring, were observed between the islands, consistent with Pemba's persistently higher mean infection intensities compared to neighbouring Unguja, and within islands in terms of infection hotspots (across three definitions). These findings highlight the important contribution of population genetic analyses to elucidate extensive genetic diversity and biological drivers, including potential gene-environmental factors, that may override short term selective pressures imposed by differential disease control strategies. Trial Registration: ClinicalTrials.gov ISRCTN48837681.

Genomic evidence of contemporary hybridization between Schistosoma species.

Hybridization between different species of parasites is increasingly being recognised as a major public and veterinary health concern at the interface of infectious diseases biology, evolution, epidemiology and ultimately control. Recent research has revealed that viable hybrids and introgressed lineages between Schistosoma spp. are prevalent across Africa and beyond, including those with zoonotic potential. However, it remains unclear whether these hybrid lineages represent recent hybridization events, suggesting hybridization is ongoing, and/or whether they represent introgressed lineages derived from ancient hybridization events. In human schistosomiasis, investigation is hampered by the inaccessibility of adult-stage worms due to their intravascular location, an issue which can be circumvented by post-mortem of livestock at abattoirs for Schistosoma spp. of known zoonotic potential. To characterise the composition of naturally-occurring schistosome hybrids, we performed whole-genome sequencing of 21 natural livestock infective schistosome isolates. To facilitate this, we also assembled a de novo chromosomal-scale draft assembly of Schistosoma curassoni. Genomic analyses identified isolates of S. bovis, S. curassoni and hybrids between the two species, all of which were early generation hybrids with multiple generations found within the same host. These results show that hybridization is an ongoing process within natural populations with the potential to further challenge elimination efforts against schistosomiasis.

Transmission and diversity of Schistosoma haematobium and S. bovis and their freshwater intermediate snail hosts Bulinus globosus and B. nasutus in the Zanzibar Archipelago, United Republic of Tanzania.

BACKGROUND: The Zanzibar Archipelago (Pemba and Unguja islands) is targeted for the elimination of human urogenital schistosomiasis caused by infection with Schistosoma haematobium where the intermediate snail host is Bulinus globosus. Following multiple studies, it has remained unclear if B. nasutus (a snail species that occupies geographically distinct regions on the Archipelago) is involved in S. haematobium transmission on Zanzibar. Additionally, S. haematobium was thought to be the only Schistosoma species present on the Zanzibar Archipelago until the sympatric transmission of S. bovis, a parasite of ruminants, was recently identified. Here we re-assess the epidemiology of schistosomiasis on Pemba and Unguja together with the role and genetic diversity of the Bulinus spp. involved in transmission. METHODOLOGY/PRINCIPAL FINDINGS: Malacological and parasitological surveys were conducted between 2016 and 2019. In total, 11,116 Bulinus spp. snails were collected from 65 of 112 freshwater bodies surveyed. Bulinus species identification were determined using mitochondrial cox1 sequences for a representative subset of collected Bulinus (n = 504) and together with archived museum specimens (n = 6), 433 B. globosus and 77 B. nasutus were identified. Phylogenetic analysis of cox1 haplotypes revealed three distinct populations of B. globosus, two with an overlapping distribution on Pemba and one on Unguja. For B. nasutus, only a single clade with matching haplotypes was observed across the islands and included reference sequences from Kenya. Schistosoma haematobium cercariae (n = 158) were identified from 12 infected B. globosus and one B. nasutus collected between 2016 and 2019 in Pemba, and cercariae originating from 69 Bulinus spp. archived in museum collections. Schistosoma bovis cercariae (n = 21) were identified from seven additional B. globosus collected between 2016 and 2019 in Pemba. By analysing a partial mitochondrial cox1 region and the nuclear ITS (1-5.8S-2) rDNA region of Schistosoma cercariae, we identified 18 S. haematobium and three S. bovis haplotypes representing populations associated with mainland Africa and the Indian Ocean Islands (Zanzibar, Madagascar, Mauritius and Mafia). CONCLUSIONS/SIGNIFICANCE: The individual B. nasutus on Pemba infected with S. haematobium demonstrates that B. nasutus could also play a role in the local transmission of S. haematobium. We provide preliminary evidence that intraspecific variability of S. haematobium on Pemba may increase the transmission potential of S. haematobium locally due to the expanded intermediate host range, and that the presence of S. bovis complicates the environmental surveillance of schistosome infections.

Genomic analysis of a parasite invasion: Colonization of the Americas by the blood fluke Schistosoma mansoni.

Schistosoma mansoni, a snail-borne, blood fluke that infects humans, was introduced into the Americas from Africa during the Trans-Atlantic slave trade. As this parasite shows strong specificity to the snail intermediate host, we expected that adaptation to South American Biomphalaria spp. snails would result in population bottlenecks and strong signatures of selection. We scored 475,081 single nucleotide variants in 143 S. mansoni from the Americas (Brazil, Guadeloupe and Puerto Rico) and Africa (Cameroon, Niger, Senegal, Tanzania, and Uganda), and used these data to ask: (i) Was there a population bottleneck during colonization? (ii) Can we identify signatures of selection associated with colonization? (iii) What were the source populations for colonizing parasites? We found a 2.4- to 2.9-fold reduction in diversity and much slower decay in linkage disequilibrium (LD) in parasites from East to West Africa. However, we observed similar nuclear diversity and LD in West Africa and Brazil, suggesting no strong bottlenecks and limited barriers to colonization. We identified five genome regions showing selection in the Americas, compared with three in West Africa and none in East Africa, which we speculate may reflect adaptation during colonization. Finally, we infer that unsampled populations from central African regions between Benin and Angola, with contributions from Niger, are probably the major source(s) for Brazilian S. mansoni. The absence of a bottleneck suggests that this is a rare case of a serendipitous invasion, where S. mansoni parasites were pre-adapted to the Americas and able to establish with relative ease.

Genome-wide insights into adaptive hybridisation across the Schistosoma haematobium group in West and Central Africa.

Schistosomiasis remains a public health concern across sub-Saharan Africa; current control programmes rely on accurate mapping and high mass drug administration (MDA) coverage to attempt disease elimination. Inter-species hybridisation can occur between certain species, changing epidemiological dynamics within endemic regions, which has the potential to confound control interventions. The impact of hybridisation on disease dynamics is well illustrated in areas of Cameroon where urogenital schistosomiasis, primarily due to Schistosoma haematobium and hybrid infections, now predominate over intestinal schistosomiasis caused by Schistosoma guineensis. Genetic markers have shown the ability to identify hybrids, however the underlying genomic architecture of divergence and introgression between these species has yet to be established. In this study, restriction site associated DNA sequencing (RADseq) was used on archived adult worms initially identified as; Schistosoma bovis (n = 4), S. haematobium (n = 9), S. guineensis (n = 3) and S. guineensis x S. haematobium hybrids (n = 4) from Mali, Senegal, Niger, São Tomé and Cameroon. Genome-wide evidence supports the existence of S. guineensis and S. haematobium hybrid populations across Cameroon. The hybridisation of S. guineensis x S. haematobium has not been demonstrated on the island of São Tomé, where all samples showed no introgression with S. haematobium. Additionally, all S. haematobium isolates from Nigeria, Mali and Cameroon indicated signatures of genomic introgression from S. bovis. Adaptive loci across the S. haematobium group showed that voltage-gated calcium ion channels (Cav) could play a key role in the ability to increase the survivability of species, particularly in host systems. Where admixture has occurred between S. guineensis and S. haematobium, the excess introgressive influx of tegumental (outer helminth body) and antigenic genes from S. haematobium has increased the adaptive response in hybrids, leading to increased hybrid population fitness and viability.

Abyssal fauna of polymetallic nodule exploration areas, eastern Clarion-Clipperton Zone, central Pacific Ocean: Amphinomidae and Euphrosinidae (Annelida, Amphinomida).

This is a contribution in a series of taxonomic publications on benthic fauna of polymetallic nodule fields in the eastern abyssal Clarion-Clipperton Zone (CCZ). The material was collected during environmental surveys targeting exploration contract areas 'UK-1', 'OMS' and 'NORI-D', as well as an Area of Particular Environmental Interest, 'APEI-6'. The annelid families Amphinomidae and Euphrosinidae are investigated here. Taxonomic data are presented for six species from 41 CCZ-collected specimens as identified by a combination of morphological and genetic approaches; of the six species, three are here described as new, one species is likely to be new but in too poor condition to be formalised and the two others likely belong to known species. Description of three new species Euphrosinellageorgievae sp. nov., Euphrosinopsisahearni sp. nov., and Euphrosinopsishalli sp. nov. increases the number of formally described new annelid species from the targeted areas to 21 and CCZ-wide to 52. Molecular data suggest that four of the species reported here are known from CCZ only, but within CCZ they have a wide distribution. In contrast, the species identified as Bathychloeiacf.sibogae Horst, 1910 was found to have a wide distribution within the Pacific based on both morphological and molecular data, using comparative material from the abyssal South Pacific. Bathychloeiacf.balloniformis Böggemann, 2009 was found to be restricted to APEI-6 based on DNA data available from CCZ specimens only, but morphological data from other locations suggest potentially a wide abyssal distribution. The genus Euphrosinopsis was previously known only from Antarctic waters, and Euphrosinellageorgievae sp. nov. was recovered as a sister taxon to the Antarctic specimens of Euphrosinellacf.cirratoformis in our molecular phylogenetic analysis, strengthening the hypothesised link between the deep-sea and Antarctic benthic fauna.

Benthic megafauna of the western Clarion-Clipperton Zone, Pacific Ocean.

There is a growing interest in the exploitation of deep-sea mineral deposits, particularly on the abyssal seafloor of the central Pacific Clarion-Clipperton Zone (CCZ), which is rich in polymetallic nodules. In order to effectively manage potential exploitation activities, a thorough understanding of the biodiversity, community structure, species ranges, connectivity, and ecosystem functions across a range of scales is needed. The benthic megafauna plays an important role in the functioning of deep-sea ecosystems and represents an important component of the biodiversity. While megafaunal surveys using video and still images have provided insight into CCZ biodiversity, the collection of faunal samples is needed to confirm species identifications to accurately estimate species richness and species ranges, but faunal collections are very rarely carried out. Using a Remotely Operated Vehicle, 55 specimens of benthic megafauna were collected from seamounts and abyssal plains in three Areas of Particular Environmental Interest (APEI 1, APEI 4, and APEI 7) at 3100-5100 m depth in the western CCZ. Using both morphological and molecular evidence, 48 different morphotypes belonging to five phyla were found, only nine referrable to known species, and 39 species potentially new to science. This work highlights the need for detailed taxonomic studies incorporating genetic data, not only within the CCZ, but in other bathyal, abyssal, and hadal regions, as representative genetic reference libraries that could facilitate the generation of species inventories.

Strengthening the global network for sharing of marine biological collections: recommendations for a new agreement for biodiversity beyond national jurisdiction.

Biological collections are fundamental to marine scientific research and understanding of biodiversity at various scales. Despite their key importance, sample collections and the institutes that house them are often underfunded and receive comparatively little attention in the discussions associated with global biodiversity agreements. Furthermore, access to collections can be limited by inadequate systems, infrastructure, and networks. With negotiations underway for a new implementing agreement on biodiversity beyond national jurisdiction, marine genetic resources (MGR), including questions on the sharing of benefits, remains the most debated and contentious element. Disparities remain between States regarding access to and utilization of marine biological samples (including MGR) from areas beyond national jurisdiction. Addressing capacity gaps related to collections could provide a point of agreement during negotiations and enhance global inclusivity in access to and utilization of MGR. Here, we examine both existing capacity and regional gaps in marine collections. We propose the strengthening of a distributed network of marine biological collections, building on existing initiatives and emphasizing best practices to bridge regional gaps. Our recommendations include: promoting scientific best practice for the curation of collections; alignment with ocean observing, and sampling initiatives; a potential pairing scheme for collections in developing and developed States; raising awareness of collections and benefits to marine science including through a global registry/directory; and promoting sustainable funding mechanisms to support collections and sustain global generation of contributors and users.

Endemicity of Paragonimus and paragonimiasis in Sub-Saharan Africa: A systematic review and mapping reveals stability of transmission in endemic foci for a multi-host parasite system.

Paragonimiasis is caused by zoonotic trematodes of Paragonimus spp., found in Asia, the Americas and Africa, particularly in tropical regions. These parasites have a complex, multi-host life cycle, with mammalian definitive hosts and larval stages cycling through two intermediate hosts (snails and freshwater decapod crustaceans). In Africa, paragonimiasis is particularly neglected, and remains the only human parasitic disease without a fully characterised life cycle. However paragonimiasis has potentially significant impacts on public health in Africa, and prevalence has likely been underestimated through under-reporting and misdiagnosis as tuberculosis due to a similar clinical presentation. We identified the need to synthesise current knowledge and map endemic foci for African Paragonimus spp. together with Poikilorchis congolensis, a rare, taxonomically distant trematode with a similar distribution and morphology. We present the first systematic review of the literature relating to African paragonimiasis, combined with mapping of all reported occurrences of Paragonimus spp. throughout Africa, from the 1910s to the present. In human surveys, numerous reports of significant recent transmission in Southeast Nigeria were uncovered, with high prevalence and intensity of infection. Overall prevalence was significantly higher for P. uterobilateralis compared to P. africanus across studies. The potential endemicity of P. africanus in Côte d'Ivoire is also reported. In freshwater crab intermediate hosts, differences in prevalence and intensity of either P. uterobilateralis or P. africanus were evident across genera and species, suggesting differences in susceptibility. Mapping showed temporal stability of endemic foci, with the majority of known occurrences of Paragonimus found in the rainforest zone of West and Central Africa, but with several outliers elsewhere on the continent. This suggests substantial under sampling and localised infection where potential host distributions overlap. Our review highlights the urgent need for increased sampling in active disease foci in Africa, particularly using molecular analysis to fully characterise Paragonimus species and their hosts.

Prevalence and distribution of schistosomiasis in human, livestock, and snail populations in northern Senegal: a One Health epidemiological study of a multi-host system.

BACKGROUND: Schistosomiasis is a neglected tropical disease of global medical and veterinary importance. As efforts to eliminate schistosomiasis as a public health problem and interrupt transmission gather momentum, the potential zoonotic risk posed by livestock Schistosoma species via viable hybridisation in sub-Saharan Africa have been largely overlooked. We aimed to investigate the prevalence, distribution, and multi-host, multiparasite transmission cycle of Haematobium group schistosomiasis in Senegal, West Africa. METHODS: In this epidemiological study, we carried out systematic surveys in definitive hosts (humans, cattle, sheep, and goats) and snail intermediate hosts, in 2016-18, in two areas of Northern Senegal: Richard Toll and Lac de Guiers, where transmission is perennial; and Barkedji and Linguère, where transmission is seasonal. The occurrence and distribution of Schistosoma species and hybrids were assessed by molecular analyses of parasitological specimens obtained from the different hosts. Children in the study villages aged 5-17 years and enrolled in school were selected from school registers. Adults (aged 18-78 years) were self-selecting volunteers. Livestock from the study villages in both areas were also randomly sampled, as were post-mortem samples from local abattoirs. Additionally, five malacological surveys of snail intermediate hosts were carried out at each site in open water sources used by the communities and their animals. FINDINGS: In May to August, 2016, we surveyed 375 children and 20 adults from Richard Toll and Lac de Guiers, and 201 children and 107 adults from Barkedji and Linguère; in October, 2017, to January, 2018, we surveyed 386 children and 88 adults from Richard Toll and Lac de Guiers, and 323 children and 85 adults from Barkedji and Linguère. In Richard Toll and Lac de Guiers the prevalence of urogenital schistosomiasis in children was estimated to be 87% (95% CI 80-95) in 2016 and 88% (82-95) in 2017-18. An estimated 63% (in 2016) and 72% (in 2017-18) of infected children were shedding Schistosoma haematobium-Schistosoma bovis hybrids. In adults in Richard Toll and Lac de Guiers, the prevalence of urogenital schistosomiasis was estimated to be 79% (52-97) in 2016 and 41% (30-54) in 2017-18, with 88% of infected samples containing S haematobium-S bovis hybrids. In Barkedji and Linguère the prevalence of urogenital schistosomiasis in children was estimated to be 30% (23-38) in 2016 and 42% (35-49) in 2017-18, with the proportion of infected children found to be shedding S haematobium-S bovis hybrid miracidia much lower than in Richard Toll and Lac de Guiers (11% in 2016 and 9% in 2017-18). In adults in Barkedji and Linguère, the prevalence of urogenital schistosomiasis was estimated to be 26% (17-36) in 2016 and 47% (34-60) in 2017-18, with 10% of infected samples containing S haematobium-S bovis hybrids. The prevalence of S bovis in the sympatric cattle population of Richard Toll and the Lac de Guiers was 92% (80-99), with S bovis also found in sheep (estimated prevalence 14% [5-31]) and goats (15% [5-33]). In Barkedji and Linguère the main schistosome species in livestock was Schistosoma curassoni, with an estimated prevalence of 73% (48-93) in sheep, 84% (61-98) in goats and 8% (2-24) in cattle. S haematobium-S bovis hybrids were not found in livestock. In Richard Toll and Lac de Guiers 35% of infected Bulinus spp snail intermediate hosts were found to be shedding S haematobium-S bovis hybrids (68% shedding S haematobium; 17% shedding S bovis); however, no snails were found to be shedding S haematobium hybrids in Barkedji and Linguère (29% shedding S haematobium; 71% shedding S curassoni). INTERPRETATION: Our findings suggest that hybrids originate in humans via zoonotic spillover from livestock populations, where schistosomiasis is co-endemic. Introgressive hybridisation, evolving host ranges, and wider ecosystem contexts could affect the transmission dynamics of schistosomiasis and other pathogens, demonstrating the need to consider control measures within a One Health framework. FUNDING: Zoonoses and Emerging Livestock Systems programme (UK Biotechnology and Biological Sciences Research Council, UK Department for International Development, UK Economic and Social Research Council, UK Medical Research Council, UK Natural Environment Research Council, and UK Defence Science and Technology Laboratory).

Interactions between Schistosoma haematobium group species and their Bulinus spp. intermediate hosts along the Niger River Valley.

BACKGROUND: Urogenital schistosomiasis, caused by infection with Schistosoma haematobium, is endemic in Niger but complicated by the presence of Schistosoma bovis, Schistosoma curassoni and S. haematobium group hybrids along with various Bulinus snail intermediate host species. Establishing the schistosomes and snails involved in transmission aids disease surveillance whilst providing insights into snail-schistosome interactions/compatibilities and biology. METHODS: Infected Bulinus spp. were collected from 16 villages north and south of the Niamey region, Niger, between 2011 and 2015. From each Bulinus spp., 20-52 cercariae shed were analysed using microsatellite markers and a subset identified using the mitochondrial (mt) cox1 and nuclear ITS1 + 2 and 18S DNA regions. Infected Bulinus spp. were identified using both morphological and molecular analysis (partial mt cox1 region). RESULTS: A total of 87 infected Bulinus from 24 sites were found, 29 were molecularly confirmed as B. truncatus, three as B. forskalii and four as B. globosus. The remaining samples were morphologically identified as B. truncatus (n = 49) and B. forskalii (n = 2). The microsatellite analysis of 1124 cercariae revealed 186 cercarial multilocus genotypes (MLGs). Identical cercarial genotypes were frequently (60%) identified from the same snail (clonal populations from a single miracidia); however, several (40%) of the snails had cercariae of different genotypes (2-10 MLG's) indicating multiple miracidial infections. Fifty-seven of the B. truncatus and all of the B. forskalii and B. globosus were shedding the Bovid schistosome S. bovis. The other B. truncatus were shedding the human schistosomes, S. haematobium (n = 6) and the S. haematobium group hybrids (n = 13). Two B. truncatus had co-infections with S. haematobium and S. haematobium group hybrids whilst no co-infections with S. bovis were observed. CONCLUSIONS: This study has advanced our understanding of human and bovid schistosomiasis transmission in the Niger River Valley region. Human Schistosoma species/forms (S. haematobium and S. haematobium hybrids) were found transmitted only in five villages whereas those causing veterinary schistosomiasis (S. bovis), were found in most villages. Bulinus truncatus was most abundant, transmitting all Schistosoma species, while the less abundant B. forskalii and B. globosus, only transmitted S. bovis. Our data suggest that species-specific biological traits may exist in relation to co-infections, snail-schistosome compatibility and intramolluscan schistosome development.

Snail-Related Contributions from the Schistosomiasis Consortium for Operational Research and Evaluation Program Including Xenomonitoring, Focal Mollusciciding, Biological Control, and Modeling.

The Schistosomiasis Consortium for Operational Research and Evaluation (SCORE) was created in 2008 to answer questions of importance to program managers working to reduce the burden of schistosomiasis in Africa. In the past, intermediate host snail monitoring and control was an important part of integrated schistosomiasis control. However, in Africa, efforts to control snails have declined dramatically over the last 30 years. A resurgence of interest in the control of snails has been prompted by the realization, backed by a World Health Assembly resolution (WHA65.21), that mass drug administration alone may be insufficient to achieve schistosomiasis elimination. SCORE has supported work on snail identification and mapping and investigated how xenomonitoring techniques can aid in the identification of infected snails and thereby identify potential transmission areas. Focal mollusciciding with niclosamide was undertaken in Zanzibar and Côte d'Ivoire as a part of elimination studies. Two studies involving biological control of snails were conducted: one explored the association of freshwater riverine prawns and snail hosts in Côte d'Ivoire and the other assessed the current distribution of Procambarus clarkii, the invasive Louisiana red swamp crayfish, in Kenya and its association with snail hosts and schistosomiasis transmission. SCORE also supported modeling studies on the importance of snail control in achieving elimination and a meta-analysis of the impact of molluscicide-based snail control programs on human schistosomiasis prevalence and incidence. SCORE's snail control studies contributed to increased investment in building capacity, and specimens collected during SCORE research deposited in the Schistosomiasis Collections at the Natural History Museum (SCAN) will provide a valuable resource for the years to come.

Parasite Population Genetic Contributions to the Schistosomiasis Consortium for Operational Research and Evaluation within Sub-Saharan Africa.

Analyses of the population genetic structure of schistosomes under the "Schistosomiasis Consortium for Operational Research and Evaluation" (SCORE) contrasting treatment pressure scenarios in Tanzania, Niger, and Zanzibar were performed to provide supplementary critical information with which to evaluate the impact of these large-scale control activities and guide how activities could be adjusted. We predicted that population genetic analyses would reveal information on a range of important parameters including, but not exclusive to, recruitment and transmission of genotypes, occurrence of hybridization events, differences in reproductive mode, and degrees of inbreeding, and hence, the evolutionary potential, and responses of parasite populations under contrasting treatment pressures. Key findings revealed that naturally high levels of gene flow and mixing of the parasite populations between neighboring sites were likely to dilute any effects imposed by the SCORE treatment arms. Furthermore, significant inherent differences in parasite fecundity were observed, independent of current treatment arm, but potentially of major impact in terms of maintaining high levels of ongoing transmission in persistent "biological hotspot" sites. Within Niger, naturally occurring Schistosoma haematobium/Schistosoma bovis viable hybrids were found to be abundant, often occurring in significantly higher proportions than that of single-species S. haematobium infections. By examining parasite population genetic structures across hosts, treatment regimens, and the spatial landscape, our results to date illustrate key transmission processes over and above that which could be achieved through standard parasitological monitoring of prevalence and intensity alone, as well as adding to our understanding of Schistosoma spp. life history strategies in general.

Precision mapping of snail habitat provides a powerful indicator of human schistosomiasis transmission.

Recently, the World Health Organization recognized that efforts to interrupt schistosomiasis transmission through mass drug administration have been ineffective in some regions; one of their new recommended strategies for global schistosomiasis control emphasizes targeting the freshwater snails that transmit schistosome parasites. We sought to identify robust indicators that would enable precision targeting of these snails. At the site of the world's largest recorded schistosomiasis epidemic-the Lower Senegal River Basin in Senegal-intensive sampling revealed positive relationships between intermediate host snails (abundance, density, and prevalence) and human urogenital schistosomiasis reinfection (prevalence and intensity in schoolchildren after drug administration). However, we also found that snail distributions were so patchy in space and time that obtaining useful data required effort that exceeds what is feasible in standard monitoring and control campaigns. Instead, we identified several environmental proxies that were more effective than snail variables for predicting human infection: the area covered by suitable snail habitat (i.e., floating, nonemergent vegetation), the percent cover by suitable snail habitat, and size of the water contact area. Unlike snail surveys, which require hundreds of person-hours per site to conduct, habitat coverage and site area can be quickly estimated with drone or satellite imagery. This, in turn, makes possible large-scale, high-resolution estimation of human urogenital schistosomiasis risk to support targeting of both mass drug administration and snail control efforts.

Freshwater snails of biomedical importance in the Niger River Valley: evidence of temporal and spatial patterns in abundance, distribution and infection with Schistosoma spp.

BACKGROUND: Sound knowledge of the abundance and distribution of intermediate host snails is key to understanding schistosomiasis transmission and to inform effective interventions in endemic areas. METHODS: A longitudinal field survey of freshwater snails of biomedical importance was undertaken in the Niger River Valley (NRV) between July 2011 and January 2016, targeting Bulinus spp. and Biomphalaria pfeifferi (intermediate hosts of Schistosoma spp.), and Radix natalensis (intermediate host of Fasciola spp.). Monthly snail collections were carried out in 92 sites, near 20 localities endemic for S. haematobium. All bulinids and Bi. pfeifferi were inspected for infection with Schistosoma spp., and R. natalensis for infection with Fasciola spp. RESULTS: Bulinus truncatus was the most abundant species found, followed by Bulinus forskalii, R. natalensis and Bi. pfeifferi. High abundance was associated with irrigation canals for all species with highest numbers of Bulinus spp. and R. natalensis. Seasonality in abundance was statistically significant in all species, with greater numbers associated with dry season months in the first half of the year. Both B. truncatus and R. natalensis showed a negative association with some wet season months, particularly August. Prevalences of Schistosoma spp. within snails across the entire study were as follows: Bi. pfeifferi: 3.45% (79/2290); B. truncatus: 0.8% (342/42,500); and B. forskalii: 0.2% (24/11,989). No R. natalensis (n = 2530) were infected. Seasonality of infection was evident for B. truncatus, with highest proportions shedding in the middle of the dry season and lowest in the rainy season, and month being a significant predictor of infection. Bulinus spp. and Bi. pfeifferi showed a significant correlation of snail abundance with the number of snails shedding. In B. truncatus, both prevalence of Schistosoma spp. infection, and abundance of shedding snails were significantly higher in pond habitats than in irrigation canals. CONCLUSIONS: Evidence of seasonality in both overall snail abundance and infection with Schistosoma spp. in B. truncatus, the main intermediate host in the region, has significant implications for monitoring and interrupting transmission of Schistosoma spp. in the NRV. Monthly longitudinal surveys, representing intensive sampling effort have provided the resolution needed to ascertain both temporal and spatial trends in this study. These data can inform planning of interventions and treatment within the region.

A 5-Year intervention study on elimination of urogenital schistosomiasis in Zanzibar: Parasitological results of annual cross-sectional surveys.

BACKGROUND: The Zanzibar Elimination of Schistosomiasis Transmission (ZEST) project aimed to eliminate urogenital schistosomiasis as a public health problem from Pemba and to interrupt Schistosoma haematobium transmission from Unguja in 5 years. METHODOLOGY: A repeated cross-sectional cluster-randomized trial was implemented from 2011/12 till 2017. On each island, 45 shehias were randomly assigned to receive one of three interventions: biannual mass drug administration (MDA) with praziquantel alone, or in combination with snail control or behavior change measures. In cross-sectional surveys, a single urine sample was collected from ~9,000 students aged 9- to 12-years and from ~4,500 adults aged 20- to 55-years annually, and from ~9,000 1st year students at baseline and the final survey. Each sample was examined for S. haematobium eggs by a single urine filtration. Prevalence and infection intensity were determined. Odds of infection were compared between the intervention arms. PRINCIPAL FINDINGS: Prevalence was reduced from 6.1% (95% confidence interval (CI): 4.5%-7.6%) to 1.7% (95% CI: 1.2%-2.2%) in 9- to 12-year old students, from 3.9% (95% CI: 2.8%-5.0%) to 1.5% (95% CI: 1.0%-2.0%) in adults, and from 8.8% (95% CI: 6.5%-11.2%) to 2.6% (95% CI: 1.7%-3.5%) in 1st year students from 2011/12 to 2017. In 2017, heavy infection intensities occurred in 0.4% of 9- to 12-year old students, 0.1% of adults, and 0.8% of 1st year students. Considering 1st year students in 2017, 13/45 schools in Pemba and 4/45 schools in Unguja had heavy infection intensities >1%. There was no significant difference in prevalence between the intervention arms in any study group and year. CONCLUSIONS/SIGNIFICANCE: Urogenital schistosomiasis was eliminated as public health problem from most sites in Pemba and Unguja. Prevalence was significantly reduced, but transmission was not interrupted. Continued interventions that are adaptive and tailored to the micro-epidemiology of S. haematobium in Zanzibar are needed to sustain and advance the gains made by ZEST.

Molecular characterization and distribution of Schistosoma cercariae collected from naturally infected bulinid snails in northern and central Côte d'Ivoire.

BACKGROUND: Accurate identification of schistosome species infecting intermediate host snails is important for understanding parasite transmission, schistosomiasis control and elimination. Cercariae emerging from infected snails cannot be precisely identified morphologically to the species level. We used molecular tools to clarify the distribution of the Schistosoma haematobium group species infecting bulinid snails in a large part of Côte d'Ivoire and confirmed the presence of interspecific hybrid schistosomes. METHODS: Between June 2016 and March 2017, Bulinus snails were sampled in 164 human-water contact sites from 22 villages of the northern and central parts of Côte d'Ivoire. Multi-locus genetic analysis (mitochondrial cox1 and nuclear ITS) was performed on individual schistosome cercariae shed from snails, in the morning and in the afternoon, for species and hybrid identification. RESULTS: Overall, 1923 Bulinus truncatus, 255 Bulinus globosus and 1424 Bulinus forskalii were obtained. Among 2417 Bulinus screened, 25 specimens (18 B. truncatus and seven B. globosus) shed schistosomes, with up to 14% infection prevalence per site and time point. Globally, infection rates per time point ranged between 0.6 and 4%. Schistosoma bovis, S. haematobium and S. bovis × S. haematobium hybrids infected 0.5%, 0.2% and 0.4% of the snails screened, respectively. Schistosoma bovis and hybrids were more prevalent in B. truncatus, whereas S. haematobium and hybrid infections were more prevalent in B. globosus. Schistosoma bovis-infected Bulinus were predominantly found in northern sites, while S. haematobium and hybrid infected snails were mainly found in central parts of Côte d'Ivoire. CONCLUSIONS: The data highlight the necessity of using molecular tools to identify and understand which schistosome species are transmitted by specific intermediate host snails. The study deepens our understanding of the epidemiology and transmission dynamics of S. haematobium and S. bovis in Côte d'Ivoire and provides the first conclusive evidence for the transmission of S. haematobium × S. bovis hybrids in this West African country. Trial registration ISRCTN, ISRCTN10926858. Registered 21 December 2016; retrospectively registered (see: http://www.isrctn.com/ISRCTN10926858 ).