Catharina Clewing

Invaders versus endemics: alien gastropod species in ancient Lake Ohrid

Species invasions into ancient lakes are an important but little understood phenomenon. At ancient Lake Ohrid, a systematic assessment of invasive mollusc species using morphological and genetic data was conducted from 2003 to 2012. Two globally invasive gastropod species, Physa acuta and Ferrissia fragilis, have recently been discovered at 4 out of 386 sites. These sites are anthropogenically impacted. The invasive species co-occur with endemics. Phylogenetic analyses of populations from native and invaded ranges of both species confirmed their identities and provided insights into their invasion histories. Accordingly, P. acuta is genetically more diverse than F. fragilis. Both species are currently present in a considerable number of lakes on the Balkan Peninsula. Possible future trends in Lake Ohrid and the Balkans are discussed and further spread of both species is likely. Given the ongoing environmental change in Lake Ohrid, the number of observations of non-indigenous or other widespread species will probably rise in the coming years and such species and their impact on native species should be carefully monitored. Moreover, ancient lakes with recurrent invasions of alien species might serve as interesting model systems for the study of important topics of invasion biology.

Molecular Phylogeny and Biogeography of a High Mountain Bivalve Fauna: The Sphaeriidae of the Tibetan Plateau

ABSTRACT Sphaeriids represent a highly diverse family of small bivalves inhabiting freshwater habitats worldwide. They are recognized for their high dispersal capacity as well as for a high capability to adapt to such extreme environments as high mountain regions over 4,000 m above sea level (a.s.l.). The Tibetan Plateau, located in central Asia, is such a high elevation area. Here, we present the first broad spatial sampling of sphaeriids from the Tibetan Plateau, which allowed us to describe the Recent fauna as well as their biogeographical background. Our study revealed six sphaeriid species inhabiting various habitats on the Tibetan Plateau: Pisidium nitidum, P. stewarti, P. subtruncatum, P. zugmayeri, Pisidium sp. I and Musculium kashmirensis. Four species are newly recorded for this region. Based on phylogenetic analyses using molecular information from three different genes (COI, 16S and 28S) we conclude that the extant diversity of Tibetan Plateau sphaeriids might have been caused by multiple colonization events. Furthermore, the zoogeographic affinities of Tibetan Plateau sphaeriids are mostly related to the Palearctic. Similar patterns have been observed in previous studies of other freshwater molluscan taxa in the area.

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).

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.

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

BackgroundNon-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.ResultsMolecular 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.ConclusionsWe 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.

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.

Exploring high-mountain limnic faunas: discovery of a novel endemic bivalve species (Sphaeriidae : Pisidium) in the Nepal Himalayas

Abstract. High-mountain regions are known to harbour considerable biodiversity, although it is not all well known. The terrestrial fauna of the world’s largest mountain range, the Himalayas, has been moderately well studied, but this is not the case with the limnic fauna, and especially molluscs. During intensive malacozoological field surveys conducted over the past 20 years, the bivalve family Sphaeriidae has been studied in Nepal along an elevational gradient from 100 to 4010 m above sea level (a.s.l.). Here we describe a new species of Sphaeriidae, Pisidium alexeii, sp. nov., based on comprehensive molecular phylogenetics, anatomy and shell morphology. The species can be clearly distinguished from all other sphaeriid species occurring in Nepal. A molecular phylogeny based on mitochondrial and nuclear data inferred the oriental biogeographical affinity of the new species. The species is ecologically restricted and only occurs at a few sites between 1010 and 1700 m a.s.l. A review and updated checklist of the sphaeriid fauna of Nepal is provided and biodiversity and biogeographical patterns are discussed.

Phylogenetic patterns of freshwater amphipods inhabiting the Tibetan Plateau

High-elevational areas such as the Tibetan Plateau — the highest and largest plateau on earth (Royden et al., 2008) — are typically inhabited by highly specialized biota, which are adapted to the prevailing extreme environmental conditions (see Körner, 2001; Favre et al., 2015). These conditions represent a significant challenge particularly for aquatic organisms occurring in freshwater habitats within alpine ecosystems. The Tibetan Plateau freshwater fauna is, besides several fish species, mainly composed of invertebrate taxa such as molluscs, insects and crustaceans. Whereas, for example, the phylogenetic and biogeographic history of the plateau molluscs is comparatively well studied (Von Oheimb et al., 2011, 2013; Clewing et al., 2013, 2014, 2015), the freshwater crustacean fauna has received less attention. The Holarctic amphipod genus Gammarus Fabricius, 1775, comprising about 204 species (Barnard & Barnard, 1983; Väinölä et al., 2008), is one of the most diverse crustacean genera with a comparatively high degree of endemism (Hou et al., 2014), and five species are described from the plateau: G. lacustris Sars, 1863, G. lasaensis Barnard & Dai, 1988, G. frigidus Hou & Li, 2004, G. jaspidus Hou & Li, 2004 and G. sinuolatus Hou & Li, 2004. The latter four species are endemic and, until today, only known from a single location (Hou & Li, 2004). Based on a comprehensive sampling and genetic data from two mitochondrial markers, the aim of this study was to investigate (i) the distribution patterns with special reference to altitudinal ranges, (ii) the genetic diversity and (iii) the phylogenetic affinities and colonization histories of gammarids across the Tibetan Plateau. This study represents the first phylogenetic or phylogeographic analysis of plateau-wide distributed crustaceans.

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.

Isolation, characterization and cross-species amplification of 15 microsatellite markers for the African species of the freshwater gastropod genus Bellamya

We isolated and characterized microsatellite markers for African species of the freshwater gastropod genus Bellamya. Fifteen out of 21 primer combinations, isolated from unpublished sequences, yielded in polymorphic products. The number of alleles ranged from 8 to 22 among the 37 scored individuals. The observed heterozygosity HO ranged from 0.571 to 0.919 and the expected heterozygosity HE ranged from 0.626 to 0.937. Evidence of null alleles were observed at three polymorphic loci. Cross-species amplifications were carried out for five additional African viviparid species and resulted in several polymorphic microsatellite markers, a high number of monomorphic loci as well as a few unsuccessful amplifications.