Recent range expansion of an intermediate host for animal schistosome parasites in the Indo-Australian Archipelago: phylogeography of the freshwater gastropod Indoplanorbis exustus in South and Southeast Asia

Background: The planorbid snail Indoplanorbis exustus is the sole intermediate host for the Schistosoma indicum species group, trematode parasites responsible for cattle schistosomiasis and human cercarial dermatitis. This freshwater snail is widely distributed in Southern Asia, ranging from Iran to China eastwards including India and from the southeastern Himalayas to Southeast Asia southwards. The veterinary and medical importance of this snail explains the interest in understanding its geographical distribution patterns and evolutionary history. In this study, we used a large and comprehensive sampling throughout Indo-Malaya, including specimens from South India and Indonesia, areas that have been formerly less studied. Results: The phylogenetic inference revealed five highly divergent clades (genetic distances among clades: 4.4–13.9%) that are morphologically indistinguishable, supporting the assumption that this presumed nominal species may represent a cryptic species complex. The species group may have originated in the humid subtropical plains of Nepal or in southern adjacent regions in the Early Miocene. The major cladogenetic events leading to the fives clades occurred successively from the Early Miocene to the Early Pleistocene, coinciding with major periods of monsoonal intensification associated with major regional paleogeographic events in the Miocene and repeated climate changes due to the Plio-Pleistocene climatic oscillations. Our coverage of the Indo-Australian Archipelago (IAA) highlights the presence of a single clade there. Contrary to expectations, an AMOVA did not reveal any population genetic structure among islands or along a widely recognised zoogeographical regional barrier, suggesting a recent colonisation independent of natural biogeographical constraints. Neutrality tests and mismatch distributions suggested a sudden demographic and spatial population expansion that could have occurred naturally in the Pleistocene or may possibly result of a modern colonisation triggered by anthropogenic activities. Conclusions: Even though Indoplanorbis is the main focus of this study, our findings may also have important implications for fully understanding its role in hosting digenetic trematodes. The existence of a cryptic species complex, the historical phylogeographical patterns and the recent range expansion in the IAA provide meaningful insights to the understanding and monitoring of the parasites potential spread. It brings a substantial contribution to veterinary and public health issues

Origin and diversification of Lake Ohrid’s endemic acroloxid limpets: the role of geography and ecology

Background: Ancient Lake Ohrid, located on the Albania-Macedonia border, is the most biodiverse freshwater lake in Europe. However, the processes that gave rise to its extraordinary endemic biodiversity, particularly in the species-rich gastropods, are still poorly understood. A suitable model taxon to study speciation processes in Lake Ohrid is the pulmonate snail genus Acroloxus, which comprises two morphologically distinct and ecologically (vertically) separated endemic species. Using a multilocus phylogenetic framework of Acroloxus limpets from the Euro-Mediterranean subregion, together with molecular-clock and phylogeographic analyses of Ohrid taxa, we aimed to infer their geographic origin and the timing of colonization as well as the role of geography and ecology in intra-lacustrine diversification. Results: In contrast to most other endemic invertebrate groups in Lake Ohrid, the phylogenetic relationships of the endemic Ohrid Acroloxus species indicate that the Balkan region probably did not serve as their ancestral area. The inferred monophyly and estimated divergence times further suggest that these freshwater limpets colonized the lake only once and that the onset of intra-lacustrine diversification coincides with the time when the lake reached deep-water conditions ca 1.3 Mya. However, the difference in vertical distribution of these two ecologically distinct species is not reflected in the phylogeographic pattern observed. Instead, western and eastern populations are genetically more distinct, suggesting a horizontal structure. Conclusions: We conclude that both geography and ecology have played a role in the intra-lacustrine speciation process. Given the distinct morphology (sculptured vs. smooth shell) and ecology (littoral vs. sublittoral), and the timing of intra-lacustrine diversification inferred, we propose that the onset of deep-water conditions initially triggered ecological speciation. Subsequent geographic processes then gave rise to the phylogeographic patterns observed today. However, the generally weak genetic differentiation observed suggests incipient speciation, which might be explained by the comparatively young age of the lake system and thus the relatively recent onset of intra-lacustrine diversification

Constant diversification rates of endemic gastropods in ancient Lake Ohrid: ecosystem resilience likely buffers environmental fluctuations

Ancient lakes represent key ecosystems for endemic freshwater species. This high endemic biodiversity has been shown to be mainly the result of intra-lacustrine diversification. Whereas the principle role of this mode of diversification is generally acknowledged, actual diversification rates in ancient lakes remain little understood. At least four types are conceivable. Diversification rates may be constant over time, they may fluctuate, rates may be higher in the initial phase of diversification, or there may be a pronounced lag phase between colonization and subsequent diversification. As understanding the tempo of diversification in ancient lake environments may help reveal the underlying processes that drive speciation and extinction, we here use the Balkan Lake Ohrid as a model system and the largest species flock in the lake, the non-pyrgulinid Hydrobiidae, as a model taxon to study changes in diversification rates over time together with the respective drivers. Based on phylogenetic, molecular-clock, lineage-through-time plot, and diversification-rate analyses we found that this potentially monophyletic group is comparatively old and that it most likely evolved with a constant diversification rate. Preliminary data of the SCOPSCO (Scientific Collaboration On Past Speciation Conditions in Lake Ohrid) deep-drilling program do indicate signatures of severe environmental/climatic perturbations in Lake Ohrid. However, so far there is no evidence for the occurrence of catastrophic environmental events. We therefore propose that the constant diversification rate observed in endemic gastropods has been caused by two factors: (i) a potential lack of catastrophic environmental events in Lake Ohrid and/or (ii) a probably high ecosystem resilience, buffering environmental changes. Parameters potentially contributing to the lake´s high ecosystem resilience are its distinct bathymetry, ongoing tectonic activities, and karst hydrology. The current study not only contributes to one of the overall goals of the SCOPSCO deep-drilling program – inferring the driving forces for biotic evolution in Lake Ohrid. It might also enhance our understanding of how ecosystem resilience, in general, may promote relatively constant diversification rates in isolated ecosystems. However, we encourage future studies testing hypotheses about the lack of catastrophic events in Lake Ohrid. These studies should be based on high-resolution data for the entire geological history of the lake, and they should potentially involve information from the sediment fossil record, not only for gastropods but also for other groups with a high share of endemic taxa

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

Paleo-Drainage Basin Connectivity Predicts Evolutionary Relationships across Three Southeast Asian Biodiversity Hotspots

Understanding factors driving diversity across biodiversity hotspots is critical for formulating conservation priorities in the face of ongoing and escalating environmental deterioration. While biodiversity hotspots encompass a small fraction of Earth's land surface, more than half the world's plants and two-thirds of terrestrial vertebrate species are endemic to these hotspots. Tropical Southeast (SE) Asia displays extraordinary species richness, encompassing four biodiversity hotspots, though disentangling multiple potential drivers of species richness is confounded by the region's dynamic geological and climatic history. Here, we use multilocus molecular genetic data from dense multispecies sampling of freshwater fishes across three biodiversity hotspots, to test the effect of Quaternary climate change and resulting drainage rearrangements on aquatic faunal diversification. While Cenozoic geological processes have clearly shaped evolutionary history in SE Asian halfbeak fishes, we show that paleo-drainage re-arrangements resulting from Quaternary climate change played a significant role in the spatiotemporal evolution of lowland aquatic taxa, and provide priorities for conservation efforts. [Freshwater; geology; halfbeak; island radiation; Miocene; Pleistocene; river; Southeast Asia.

Environmental filtering drives assembly of diatom communities over evolutionary time‐scales

Aim Ecological communities are structured through the interplay of deterministic assembly processes such as competition and environmental filtering. Whereas the drivers of spatial community structure are frequently studied in extant communities, little is known about the relative importance of assembly processes in response to environmental factors over evolutionary time-scales. Here, we use an integrative framework to unravel community assembly processes since the inception of a long-lived lake ecosystem. Location Lake Ohrid. Time period From lake formation 1.36 million years ago to the present. Major taxa studied Planktonic diatoms. Methods We constructed a dated phylogeny of extant and extinct diatoms and collected trait data for 380 fossil communities to quantify phylogenetic community structure and functional richness and to determine the relative importance of deterministic assembly processes over time. We then used regression analysis to correlate the phylogenetic community structure with palaeoenvironmental and intrinsic biological predictors and to identify primary drivers of assembly processes. Results Our results suggest a dense packing of niche space with higher species richness and co-occurrence of closely related species. There are only two short episodes in the very recent past dominated by distantly related taxa. We found distinct changes in phylogenetic community structure upon speciation or extinction events and an increase in mean community relatedness over time. Main conclusions Our finding of closely related co-occurring species implies environmental filtering as the primary assembly mechanism, with a minor but increasingly important role of competition towards the present, driven by evolutionary dynamics. Such an increase in the relative contribution of competition to the assembly of communities in relation to the aging of an insular ecosystem, together with a denser packing of morphospace in the early phase of system ontogeny is compatible with ecological predictions according to the theory of island biogeography

Deep drilling reveals massive shifts in evolutionary dynamics after formation of ancient ecosystem

The scarcity of high-resolution empirical data directly tracking diversity over time limits our understanding of speciation and extinction dynamics and the drivers of rate changes. Here, we analyze a continuous species-level fossil record of endemic diatoms from ancient Lake Ohrid, along with environmental and climate indicator time series since lake formation 1.36 million years (Ma) ago. We show that speciation and extinction rates nearly simultaneously decreased in the environmentally dynamic phase after ecosystem formation and stabilized after deep-water conditions established in Lake Ohrid. As the lake deepens, we also see a switch in the macroevolutionary trade-off, resulting in a transition from a volatile assemblage of short-lived endemic species to a stable community of long-lived species. Our results emphasize the importance of the interplay between environmental/climate change, ecosystem stability, and environmental limits to diversity for diversification processes. The study also provides a new understanding of evolutionary dynamics in long-lived ecosystems

Scientific drilling projects in ancient lakes: integrating geological and biological histories

Sedimentary sequences in ancient or long-lived lakes can reach several thousands of meters in thickness and often provide an unrivalled perspective of the lake's regional climatic, environmental, and biological history. Over the last few years, deep drilling projects in ancient lakes became increasingly multi- and interdisciplinary, as, among others, seismological, sedimentological, biogeochemical, climatic, environmental, paleontological, and evolutionary information can be obtained from sediment cores. However, these multi- and interdisciplinary projects pose several challenges. The scientists involved typically approach problems from different scientific perspectives and backgrounds, and setting up the program requires clear communication and the alignment of interests. One of the most challenging tasks, besides the actual drilling operation, is to link diverse datasets with varying resolution, data quality, and age uncertainties to answer interdisciplinary questions synthetically and coherently. These problems are especially relevant when secondary data, i.e., datasets obtained independently of the drilling operation, are incorporated in analyses. Nonetheless, the inclusion of secondary information, such as isotopic data from fossils found in outcrops or genetic data from extant species, may help to achieve synthetic answers. Recent technological and methodological advances in paleolimnology are likely to increase the possibilities of integrating secondary information, e.g., through molecular dating of molecular phylogenies. Some of the new approaches have started to revolutionize scientific drilling in ancient lakes, but at the same time, they also add a new layer of complexity to the generation and analysis of sediment core data. The enhanced opportunities presented by new scientific approaches to study the paleolimnological history of these lakes, therefore, come at the expense of higher logistic, communication, and analytical efforts. Here we review types of data that can be obtained in ancient lake drilling projects and the analytical approaches that can be applied to empirically and statistically link diverse datasets for creating an integrative perspective on geological and biological data. In doing so, we highlight strengths and potential weaknesses of new methods and analyses, and provide recommendations for future interdisciplinary deep drilling projects

Mediterranean winter rainfall in phase with African monsoons during the past 1.36 million years

Mediterranean climates are characterized by strong seasonal contrasts between dry summers and wet winters. Changes in winter rainfall are critical for regional socioeconomic development, but are difficult to simulate accurately1 and reconstruct on Quaternary timescales. This is partly because regional hydroclimate records that cover multiple glacial–interglacial cycles2,3 with different orbital geometries, global ice volume and atmospheric greenhouse gas concentrations are scarce. Moreover, the underlying mechanisms of change and their persistence remain unexplored. Here we show that, over the past 1.36 million years, wet winters in the northcentral Mediterranean tend to occur with high contrasts in local, seasonal insolation and a vigorous African summer monsoon. Our proxy time series from Lake Ohrid on the Balkan Peninsula, together with a 784,000-year transient climate model hindcast, suggest that increased sea surface temperatures amplify local cyclone development and refuel North Atlantic low-pressure systems that enter the Mediterranean during phases of low continental ice volume and high concentrations of atmospheric greenhouse gases. A comparison with modern reanalysis data shows that current drivers of the amount of rainfall in the Mediterranean share some similarities to those that drive the reconstructed increases in precipitation. Our data cover multiple insolation maxima and are therefore an important benchmark for testing climate model performance

A biogeographic view on Southeast Asia's history

Das tropische Südostasien, und besonders der Indo-Australische Archipel, ist bekannt für seine bemerkenswerte floristische und faunistische Diversität, besonders konzentriert in vier der identifizierten Biodiversitäts-Hotspots (Indochina, Sundaland, die Philippinen und Wallacea). In dieser Arbeit wird die biogeographische Geschichte Südostasiens beleuchtet, um Regionen mit einer erhöhten Biodiversität zu identifizieren und zu testen, ob dies mit Diversifikationen innerhalb der Region und Einwanderungen und/oder Auswanderungen korreliert und ob sich diese Faktoren über die Zeit hinweg ausgleichen. Ein besonderer Augenmerk wird auf Sulawesi und seine besondere Fauna gelegt, um zu testen, ob ein Ursprung durch Vikarianz für verschiedene Tiergruppen plausibel erscheint und wann Diversifikationen innerhalb der Fisch- und Schnecken-Radiationen im Malili-Seensystem begannen. Dabei wird auf Meta-Analysen und mehrere Disziplinen zurückgegriffen für eine integrative biogeographische Geschichte Südoastasiens und seiner Fauna, indem molekulare Uhr-Analysen, Berechnungen zur Ermittlung des Ursprungsortes mit tektonischen, paläogeographischen und klimatischen Rekonstruktionen verbunden werden, um potentielle Ursachen für die heutige Verbreitung zu finden.Tropical Southeast Asia, and particularly the Indo-Australian Archipelago, is known for its tremendous floral and faunal biodiversity, mainly accumulated in four of the world’s biodiversity hotspots identified (Indochina, Sundaland, the Philippines, and Wallacea). Here, Southeast Asia’s biogeographic history is examined to identify areas being characterized by high levels of biodiversity (number of lineages, species richness) through time and to test whether the respective biota is mainly due to in situ diversification, immigration and/or emigration, or equilibrium dynamics. Moreover, this thesis focuses particularly on Sulawesi and its peculiar fauna to test if a vicariant origin appears plausible for certain groups and when the remarkable fish and snail radiations found in the Malili Lakes system started to diversify. To achieve this, meta-analytical and multi-disciplinary approaches are considered for an integrative historical biogeographic history of Southeast Asia and its biota by using molecular clock analyses and ancestral area estimations together with tectonic, palaeogeographic and climatic reconstructions to reveal potential causes for present-day distribution