The fingernail clams (Bivalvia: Veneroida: Sphaeriidae) of Morocco: Diversity, distribution and conservation status.

BACKGROUND: In Morocco, many uncertainties surround the current diversity and distribution of the bivalve family Sphaeriidae. Such information, including taxonomy and conservation status, are vital for further studies to improve the knowledge of this family in Morocco and represents the first step towards the development of a national conservation plan for all freshwater bivalves.Between 2016 and 2019, several investigations were carried out to assess the diversity and distribution of Sphaeriidae in the different basins of Morocco, covering different types of habitat (lakes, springs, rivers and small ponds). The identification of specimens and their morpho-ecological features was based on morphological and morphometric analyses. The data on the general distribution of the collected species allowed the evaluation of their conservation status as well.The shell morphology and morphometric analyses revealed the existence of five species belonging to the genus Pisidium [P.casertanum (Poli, 1791), P. (cf.) personatum Malm, 1855, P.subtruncatum Malm, 1855, P.amnicum (O. F. Müller, 1774) and Pisidium sp.] and one species to the genus of Musculium [M.lacustre (O. F. Müller, 1774)]. Sphaeriidae were found in all Moroccan basins, except Bouregreg and Sakia El Hamra-Oued Eddahab Basins. The results showed that Sebou Basin was the species richest with the occurrence of the five species, while Loukkos and Sous-Massa Basins had the lowest-species richness with one species only. The conservation status of sphaeriids in Morocco was evaluated for the first time and resulted in P. (cf.) personatum and P.subtruncatum being proposed as Least Concern and Vulnerable, respectively, while the status of Regionally Extinct is suggested for both species P.amnicum and M.lacustre. NEW INFORMATION: First evaluation of the diversity and species richness of the family Sphaeriidae in Morocco with an assignment of an updated conservation status of the recorded species.

Population collapse in viviparid gastropods of the Lake Victoria ecoregion started before the Last Glacial Maximum.

Ecosystems of Lake Victoria and riparian communities have been strongly disrupted by the introduction of the invasive Nile perch and its fishing industry. Beyond this invasion and other recent anthropogenic stressors, the Lake Victoria ecoregion also underwent phases of pronounced aridity over the Late Pleistocene, lastly during the Last Glacial Maximum (LGM). The consequences of recent and historic environmental change have been canvassed for the adaptive radiation of haplochromine cichlids occupying the ecoregion, but their effect on freshwater invertebrate diversity remains largely unknown. Here, we use 15 microsatellite loci and approximate Bayesian computation to test whether viviparid gastropods experienced a population bottleneck during the LGM, as did cichlids. Clustering analyses support three viviparid gene pools in the Lake Victoria ecoregion, gathering specimens from 1) Lake Albert and the White Nile, 2) the Victoria Nile and Lake Kyoga and 3) Lake Victoria and tributaries. The last group contains the highest genetic diversity, but all groups have a considerable number of private alleles and are inferred to predate the LGM. Examinations of demographic history reveal a 190- to 500-fold population decline that started ~ 125-150 ka ago, thus substantially before the LGM bottleneck documented in haplochromine cichlids. Population collapses in viviparids are an order of magnitude more severe than declines in cichlids and have not been halted by the re-establishment of freshwater ecosystems since the LGM. Recent anthropogenic ecosystem deterioration is causing homogenization of previously diversified microhabitats, which may contribute to (local) extinction and enhanced gene flow among species within gene pools.

Cryptic intermediate snail host of the liver fluke Fasciola hepatica in Africa.

BACKGROUND: Snails such as Galba truncatula are hosts for trematode flukes causing fascioliasis, a zoonosis that is a major public health problem. Galba truncatula has recently been shown to be a cryptic species complex. African populations of Galba spp. are not yet studied using molecular assessments and is imperative to do so and reconstruct the centre of origin of Galba and to understand when and by what means it may have colonized the highlands of Africa and to what extent humans might have been involved in that process. METHODS: Samples from all known sub-ranges throughout Africa and new samples from Europe and Asia were obtained. We used a combination of two mitochondrial (cox1 and 16S) and one nuclear (ITS2) markers and phylogenetic, divergence time estimates and phylogeographical methods to determine the identity and biogeographical affinities. We also reconstructed the colonization history including the likely mode of dispersal and tested for the presence of cryptic Galba species in Africa. RESULTS: Galba truncatula is restricted to the Palaearctic region of the continent, namely Morocco. All sub-Saharan populations proved to be a distinct species according to the phylogenetic analyses and genetic distance. We propose to use the existing name Galba mweruensis (Connolly, 1929) for this species which is morphologically indistinguishable from the other two species hitherto known to occur in northern Africa, i.e. G. truncatula and G. schirazensis. Sub-tropical Africa has been colonized only once in either the Pliocene and possibly Miocene. Diversification within G. mweruensis is dated to the Plio-Pleistocene and thus human-mediated dispersal can be ruled out for the initial colonization of the isolated mountain ranges. There are potentially even more cryptic species in high altitude areas of Africa as outlined by the distinctness of the population found at the top of Mt. Elgon, Uganda. CONCLUSIONS: From a novel genetic inspection of available African material, a hitherto neglected distinct species, G. mweruensis, now appears a major host of F. hepatica throughout sub-Saharan Africa. A closer examination of trematode parasites hosted by this species is needed in order to understand transmission patterns in highlands throughout eastern and southern Africa. We encourage future studies to inspect other high altitudes areas in Africa in light of parasites of either veterinary or medical importance.

Molecular identification of Bulinus spp. intermediate host snails of Schistosoma spp. in crater lakes of western Uganda with implications for the transmission of the Schistosoma haematobium group parasites.

BACKGROUND: Human schistosomiasis is the second most important tropical disease and occurs in two forms in Africa (intestinal and urogenital) caused by the digenetic trematodes Schistosoma mansoni and Schistosoma haematobium, respectively. A proposed recent shift of schistosomiasis above a previously established altitudinal threshold of 1400 m above sea level in western Ugandan crater lakes has triggered more research interest there. METHODS: Based on extensive field sampling in western Uganda and beyond and employing an approach using sequences of the mitochondrial barcoding gene cytochrome c oxidase subunit 1 (cox1) this study aims were: (i) identification and establishment of the phylogenetic affinities of Bulinus species as potential hosts for Schistosoma spp.; (ii) determining diversity, frequency and distribution patterns of Bulinus spp.; and (iii) establishing genetic variability and phylogeographical patterns using Bayesian inference and parsimony network analyses. RESULTS: Out of the 58 crater lakes surveyed, three species of Bulinus snails were found in 34 crater lakes. Bulinus tropicus was dominating, Bulinus forskalii was found in two lakes and Bulinus truncatus in one. The latter two species are unconfirmed potential hosts for S. haematobium in this region. However, Bulinus tropicus is an important species for schistosomiasis transmission in ruminants. Bulinus tropicus comprised 31 haplotypes while both B. forskalii and B. truncatus exhibited only a single haplotype in the crater lakes. All species clustered with most of the haplotypes from surrounding lake systems forming source regions for the colonization of the crater lakes. CONCLUSIONS: This first detailed malacological study of the crater lakes systems in western Uganda revealed presence of Bulinus species that are either not known or not regionally known to be hosts for S. haematobium, the causing agent of human urogenital schistosomiasis. Though this disease risk is almost negligible, the observed dominance of B. tropicus in the crater lakes shows that there is a likelihood of a high risk of infections with Schistosoma bovis. Thus, extra attention should be accorded to safeguard wild and domestic ruminants in this region as the population benefits from these animals.

Genetic Evidence of Contemporary Dispersal of the Intermediate Snail Host of Schistosoma japonicum: Movement of an NTD Host Is Facilitated by Land Use and Landscape Connectivity.

BACKGROUND: While the dispersal of hosts and vectors-through active or passive movement-is known to facilitate the spread and re-emergence of certain infectious diseases, little is known about the movement ecology of Oncomelania spp., intermediate snail host of the parasite Schistosoma japonicum, and its consequences for the spread of schistosomiasis in East and Southeast Asia. In China, despite intense control programs aimed at preventing schistosomiasis transmission, there is evidence in recent years of re-emergence and persistence of infection in some areas, as well as an increase in the spatial extent of the snail host. A quantitative understanding of the dispersal characteristics of the intermediate host can provide new insights into the spatial dynamics of transmission, and can assist public health officials in limiting the geographic spread of infection. METHODOLOGY/PRINCIPAL FINDINGS: Oncomelania hupensis robertsoni snails (n = 833) were sampled from 29 sites in Sichuan, China, genotyped, and analyzed using Bayesian assignment to estimate the rate of recent snail migration across sites. Landscape connectivity between each site pair was estimated using the geographic distance distributions derived from nine environmental models: Euclidean, topography, incline, wetness, land use, watershed, stream use, streams and channels, and stream velocity. Among sites, 14.4% to 32.8% of sampled snails were identified as recent migrants, with 20 sites comprising >20% migrants. Migration rates were generally low between sites, but at 8 sites, over 10% of the overall host population originated from one proximal site. Greater landscape connectivity was significantly associated with increased odds of migration, with the minimum path distance (as opposed to median or first quartile) emerging as the strongest predictor across all environmental models. Models accounting for land use explained the largest proportion of the variance in migration rates between sites. A greater number of irrigation channels leading into a site was associated with an increase in the site's propensity to both attract and retain snails. CONCLUSIONS/SIGNIFICANCE: Our findings have important implications for controlling the geographic spread of schistosomiasis in China, through improved understanding of the dispersal capacity of the parasite's intermediate host.

A Complex System of Glacial Sub-Refugia Drives Endemic Freshwater Biodiversity on the Tibetan Plateau.

Although only relatively few freshwater invertebrate families are reported from the Tibetan Plateau, the degree of endemism may be high. Many endemic lineages occur within permafrost areas, raising questions about the existence of isolated intra-plateau glacial refugia. Moreover, if such refugia existed, it might be instructive to learn whether they were associated with lakes or with more dynamic ecosystems such as ponds, wetlands, or springs. To study these hypotheses, we used pulmonate snails of the plateau-wide distributed genus Radix as model group and the Lake Donggi Cona drainage system, located in the north-eastern part of the plateau, as model site. First, we performed plateau-wide phylogenetic analyses using mtDNA data to assess the overall relationships of Radix populations inhabiting the Lake Donggi Cona system for revealing refugial lineages. We then conducted regional phylogeographical analyses applying a combination of mtDNA and nuclear AFLP markers to infer the local structure and demographic history of the most abundant endemic Radix clade for identifying location and type of (sub-)refugia within the drainage system. Our phylogenetic analysis showed a high diversity of Radix lineages in the Lake Donggi Cona system. Subsequent phylogeographical analyses of the most abundant endemic clade indicated a habitat-related clustering of genotypes and several Late Pleistocene spatial/demographic expansion events. The most parsimonious explanation for these patterns would be a scenario of an intra-plateau glacial refugium in the Lake Donggi Cona drainage system, which might have consisted of isolated sub-refugia. Though the underlying processes remain unknown, an initial separation of lake and watershed populations could have been triggered by lake-level fluctuations before and during the Last Glacial Maximum. This study inferred the first intra-plateau refugium for freshwater animals on the Tibetan Plateau. It thus sheds new light on the evolutionary history of its endemic taxa and provides important insights into the complex refugial history of a high-altitude ecosystem.

Ecophenotypic plasticity leads to extraordinary gastropod shells found on the "Roof of the World".

The often extraordinary shell forms and shapes of gastropods found in palaeolakes, such as the highly diverse Gyraulus fauna of the famous Steinheim Basin, have been puzzling evolutionary biologists for centuries, and there is an ongoing debate whether these aberrant shell forms are indicative of true species (or subspecies) or ecophenotypic morphs. Interestingly, one of the Steinheim Gyraulus morphs - a corkscrew-like open-coiled shell - has a recent analogue in the Lake Bangong drainage system on the western Tibetan Plateau. Therefore, a combination of morphological, molecular, palaeolimnological, and ecological analyses was used in this study to assess whether the extraordinary shell shape in Gyraulus sp. from this drainage system represents a (young) ecophenotypic phenomenon or if it has been genetically fixed over an extended period of time. Our morphological, ecological, and palaeolimnological data suggest that the corkscrew-like specimens remain restricted to a small pond near Lake Bangong with an elevated pH value and that the colonization may have occurred recently. The phylogenetic reconstruction based on two gene fragments shows that these nonplanispiral specimens cluster within the previous described Tibetan Plateau Gyraulus clade N2. A network analysis indicates that some haplotypes are even shared by planispiral and nonplanispiral specimens. Given the ephemerality of the phenomenon, the compact network patterns inferred, the likely young phylogenetic age of the aberrant Gyraulus shells studied, and the ecological peculiarities of the study site, we suggest that the evolution of the aberrant shell forms on the Tibetan Plateau could likely be considered as a rapid ecophenotypic response, possibly induced by ecological stress. This finding may thus have implications for the ongoing debate about the processes that have caused the extraordinary shell diversity in palaeolakes such as the Steinheim Basin.

Conquest of the deep, old and cold: an exceptional limpet radiation in Lake Baikal.

Lake Baikal is the deepest, oldest and most speciose ancient lake in the world. The lake is characterized by high levels of molluscan species richness and endemicity, including the limpet family Acroloxidae with 25 endemic species. Members of this group generally inhabit the littoral zone, but have been recently found in the abyssal zone at hydrothermal vents and oil-seeps. Here, we use mitochondrial and nuclear data to provide a first molecular phylogeny of the Lake Baikal limpet radiation, and to date the beginning of intra-lacustrine diversification. Divergence time estimates suggest a considerably younger age for the species flock compared with lake age estimates, and the beginning of extensive diversification is possibly related to rapid deepening and cooling during rifting. Phylogenetic relationships and divergence time estimates do not clearly indicate when exactly the abyssal was colonized but suggest a timeframe coincident with the formation of the abyssal in the northern basin (Middle to Late Pleistocene).

Recurrent camouflaged invasions and dispersal of an Asian freshwater gastropod in tropical Africa.

BACKGROUND: Non-indigenous taxa currently represent a large fraction of the species and biomass of freshwater ecosystems. The accumulation of invasive taxa in combination with other stressors in these ecosystems may alter the habitats to which native taxa are adapted, which could elicit evolutionary changes in native populations and their ecological interactions. Assessing ecological and evolutionary consequences of invasions simultaneously may therefore be the most effective approach to study taxa with complex invasion histories. Here we apply such an integrated approach to the cerithioid gastropod Melanoides tuberculata, a model system in invasion biology. RESULTS: Molecular phylogenetics and ancestral range reconstructions allowed us to identify several independent Asian invasions in Lakes Malawi and Tanganyika, the Congo River, Nigeria and Cameroon. Some invasive M. tuberculata populations display much variation in shell morphology, and overlap in morphospace with M. tuberculata populations native to Africa. Experiments confirmed great ecophenotyic plasticity in some invasive populations, which, in combination with the overlap in disparity with native populations, masks invaders and their dispersal through Africa. Finally, the results of geographic modeling indicate that cryptic M. tuberculata invasions occurred primarily in densely populated areas. CONCLUSIONS: We reveal the continental nature of invasions of Asian M. tuberculata to Africa. Several of the affected ecosystems have high endemicity in Cerithioidea: Lake Tanganyika has an unparalleled diversity in freshwater cerithioids (>10 endemic genera) and the Congo Basin and Lake Malawi are home to the two largest endemic species clusters of Melanoides in Africa (~12 and ~8 species, respectively). Cerithioids perform ecologically important functions in the benthic ecosystems of African freshwaters, but invaders and ecosystem change pose risks to their native diversity. We draw suggestions for more effective conservation strategies from our integrated approach.