Molecular diversity of freshwater crabs from Sulawesi and the sequential colonization of ancient lakes

Ancient lakes represent one of the most stable freshwater environments on Earth, with a species richness clearly exceeding that of younger and more short-lived limnic habitats. In most cases, the biological colonization of old lake systems must have occurred via the surrounding rivers. Two ancient lake systems of Sulawesi (Malili lake system and Lake Poso) have been studied in terms of the taxonomy and phylogeny of freshwater crabs (Decapoda: Brachyura: Gecarcinucidae: Parathelphusinae). Both systems have been colonized twice independently, and in both systems we can find three trophic niches which are always occupied by different crab species: molluskivores, omnivores, and detritivores. In the present study, we reconstruct phylogenies of freshwater crabs from more than 20 river systems of Sulawesi. We thereby confirm two independent colonization events for both ancient lake systems, with subsequent radiations. The phylogenies imply that the lineages which evolved into the molluskivore forms were the first ones to colonize, whereas omnivores and detritivores are derived from later colonization events and, based on their monophyletic relationship, resulted from minor lacustrine radiations. Most of the diversity of freshwater crabs from Sulawesi remains taxonomically undescribed. This study uncovers several undocumented phylogenetic units, with long independent evolutionary histories according to patristic distances.     

The Radiation of Hydrobioid Gastropods (Caenogastropoda, Rissooidea) in Ancient Lake Poso, Sulawesi

A survey of the fauna of hydrobioid gastropods living in ancient Lake Poso in Sulawesi revealed a total of 16 species, 14 of them new, belonging to two genera, Sulawesidrobia and Keindahan gen. nov. Most species occurred on hard substrates, water plants or rootlets of trees. Since only the upper 0.5 m of the lake have been sampled, many more species probably remain to be discovered. Already, Lake Posoȁ9s fauna ranks among the four most diverse hydrobioid lake faunas worldwide. The Sulawesi lakes including Lake Poso and the Malili Lakes are the only lakes where sizeable radiations of hydrobioid and cerithioid gastropods coexist. Outside Lake Poso, hydrobioid gastropods have not been investigated so far apart from a single species reported from Lake Lindoe similar to or identical with S. bonnei [Abbott, 1945. Occasional Papers on Mollusks 1: 1–4], which has its type locality in Lake Poso and may in fact be a complex of species. Therefore endemicity in Lake Poso cannot be estimated nor is it possible to say, whether the radiation is of lacustrine origin. The introduction of alien fish has had a severe impact on the native fish fauna. The impact on the invertebrate fauna is not known but chances are that this survey based on collections from 1991 no longer reflects the original assemblage in the lake.     

Brood care among basommatophorans: a unique reproductive strategy in the freshwater limpet snail Protancylus (Heterobranchia: Protancylidae), endemic to ancient lakes on Sulawesi, Indonesia

In molluscan taxa inhabiting marine environments oviparity and reproduction via planktonic larvae is predominant while incubation and viviparity is most frequently found in taxa inhabiting brackish or freshwater aquatic habitats. Brooding has evolved repeatedly and independently in several limnic taxa among Bivalvia and Gastropoda. However, among basommatophoran gastropods no such cases were yet known. We here report on a unique reproductive strategy involving brood care in the lacustrine freshwater limpet genus Protancylus, endemic to the ancient lakes on central Sulawesi (former Celebes), Indonesia, namely the Lake Poso and the Malili lake system, because this constitutes the first known case of this behaviour among the Basommatophora. Protancylus live exclusively as epizoans on those pachychilid gastropods of the viviparous genus Tylomelania, also a Sulawesi endemic species, that inhabit mostly soft substrates. We found that the two known species Protancylus pileolus from Lake Poso and P. adhaerens from the Malili lake system both retain gelatinous egg strings underneath their outer mantle, where up to 15 (mostly eight or nine) shelled juveniles are brooded. Nourishment is provided within the egg capsule only. Thus, brood care in Protancylus resembles the reproductive strategy found recently among pachychilid gastropods Jagora from the Philippines, but differs from euviviparous (i.e. matrotrophic) incubation among thiarid gastropods possessing a brood pouch with juveniles being nourished via a ‘pseudoplacenta’ in several taxa.     

Ancient lakes as hotspots of diversity: a morphological review of an endemic species flock of <Emphasis Type="Italic">Tylomelania</Emphasis> (Gastropoda: Cerithioidea: Pachychilidae) in the Malili lake system on Sulawesi,Indonesia

The viviparous freshwater gastropod Tylomelania (Caenogastropoda: Cerithioidea: Pachychilidae) endemic to the Indonesian island Sulawesi has radiated extensively in two ancient lake systems. We here present the first systematic species-level review of taxa in the five lakes of the Malili lake system, which contains the most diverse and best studied freshwater fauna on Sulawesi. Our results indicate a significantly higher diversity of Tylomelania in these lakes than previously perceived based on morphological evidence for delimiting the taxa. We describe nine new species, thus increasing the number of taxa known from the Malili lakes to 25. Tylomelania species are inhabiting all available substrates in the lakes, and the diversity of habitats is reflected in an unparalleled range of radula types in this closely related group. Several species show a high intraspecific variability in some characters, and their closer investigation will probably lead to the discovery of more cryptic species. As it is, this species flock on Sulawesi is among the largest freshwater mollusc radiations known. Since the Malili lake system also contains other large endemic species flocks of e.g. crustaceans and fishes, it is a major hotspot of freshwater biodiversity in Asia to become a conservation priority. Handling editor: K. Martens     

The species flocks of lacustrine gastropods: <Emphasis Type="Italic">Tylomelania</Emphasis> on Sulawesi as models in speciation and adaptive radiation

Endemic radiations provide splendid opportunities for studies in evolutionary biology. Species flocks in ancient lakes, such as in Tanganyika, Malawi or Baikal, have featured prominently in evolutionary biology, viewing these “evolutionary theatres” as hotspots of diversification. However, following a century of neglect, the endemic evolution of limnic cerithioidean gastropods in the two central lake systems on the Indonesian island of Sulawesi (i.e. Lake Poso and the lakes of the Malili system, e.g. Danau Matano, Mahalona and Towuti) also provide instructive model cases for the study of speciation mechanisms, adaptive radiation and annidation (i.e. niche exploitation). We here discuss the evolutionary and taxonomic implications of the lacustrine species flocks in Tylomelania from these lakes in Sulawesi as an exceptional endemic assemblage of morphologically distinct viviparous pachychilid gastropods. This first comprehensive compilation of data on both ancient lake systems, Poso and Malili, offers a new perspective on ecological differentiation in this radiation. Presented here within the framework of the theory of evolutionary ecology it provides a research program for acquiring a synthetical perspective that includes morphology, molecular genetics, ecology and biogeography. In this context, it will be possible to compare the species flocks of these truly “Darwinian snails” on Sulawesi with the long enigmatic, so-called thalassoid (i.e. marine-like) gastropod radiation in East African’s Lake Tanganyika.     

Rapid evolution of sessility in an endemic species flock of the freshwater bivalve Corbicula from ancient lakes on Sulawesi, Indonesia

The fauna of ancient lakes frequently contains taxa with highly derived morphologies that resulted from in situ radiation of lacustrine lineages with high antiquity. We employed a molecular mtDNA phylogeny to investigate this claim for corbiculid freshwater bivalves in two ancient lake systems on the Indonesian island Sulawesi. Among the otherwise mobile corbiculid species flock, only one taxon, Posostrea anomioides, in the ancient Lake Poso exhibits a unique habit, i.e. cementing one valve to the substrate. Our data show that Corbicula on Sulawesi is polyphyletic, with the endemic riverine taxa in terminal position, and the lacustrine species flock being paraphyletic. Surprisingly, Posostrea is not confirmed as a genus distinct from Corbicula and genetic distances suggest a rather recent origin from the only other corbiculid species endemic to Lake Poso, the non-cementing Corbicula possoensis. While the cementing anomioides, despite its unique behavioural and morphological characteristics, clusters together with non-sessile Corbicula species, the latter exhibit strong genetic distances in the absence of morphological disparity and fall into several genetically rather distinct clades. These findings suggest that developmental plasticity of animals in ancient lakes rather than the antiquity of lineages might account for the unique morphology of some species.     

The birth of an endemic species flock: demographic history of the Bellamya group (Gastropoda,Viviparidae) in Lake Malawi

Changes in habitat stability may significantly shape evolutionary patterns and processes in ancient lakes. In the present study, we use a hierarchical combination of molecular phylogenetic and coalescent approaches to investigate the evolutionary history of the endemic species of the gastropod genus Bellamya in the African rift‐lake Malawi. By integrating our findings with reported palaeontological and palaeolimnological data, we demonstrate that all but one evolutionary lineage of the Pliocene Bellamya fauna in Lake Malawi became extinct. Coalescent analyses indicate that the modern radiation underwent both a sudden demographic and a spatial expansion after a genetic bottleneck. We argue that a reflooding of the lake after severe Pleistocene low stands offers a straightforward explanation for this pattern and may have triggered speciation processes in the modern endemic Bellamya radiation in Lake Malawi. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 102 , 130–143.     

Biodiversity and distribution of epibiontic communities on Caridina ensifera (Crustacea,Decapoda, Atyidae) from Lake Poso: comparison with another ancient lake system of Sulawesi (Indonesia)

Fernandez‐Leborans, G. and von Rintelen, K. 2010. Biodiversity and distribution of epibiontic communities on Caridina ensifera (Crustacea, Decapoda, Atyidae) from Lake Poso: comparison with another ancient lake system of Sulawesi (Indonesia). — Acta Zoologica (Stockholm) 91 : 163–175 The epibiont communities of the shrimp Caridina ensifera, endemic to Lake Poso (Sulawesi, Indonesia), were analysed. Most of the epibiont species were ciliated protozoa belonging to three suctorian genera (Acineta, Podophrya and Spelaeophrya), three peritrich genera (Zoothamnium, Vorticella and Cothurnia), and a haptorid genus (Amphileptus). There was also a rotifer epibiont of the genus Embata. Epibionts were identified to species level. There were 14 to 1114 epibionts per shrimp. The distribution of the epibiont species on the surface of the basibiont was recorded, calculating the number on the different colonized individuals of C. ensifera. The most abundant species, Zoothamnium intermedium and Acineta sulawesiensis, were also the most widely distributed. There was a significant difference between the spatial distributions of the different epibiont species. The analysis of the number of the epibiont species throughout the anteroposterior axis of the shrimp showed a gradient from the anterior to the posterior end of the body. Data from Lake Poso were compared with those of the Malili lake system (Sulawesi), obtained from its endemic shrimp, Caridina lanceolata. Lake Poso had the highest mean diversity, while Lake Mahalona showed the highest maximum diversity. All lakes were correlated with respect to the mean number of epibionts on the anatomical units of the shrimp, which showed a similar general distribution. The distributions of the different epibiont species were compared between the lakes. The possible adaptations of the epibionts as well as the colonization patterns were discussed. From the statistical results and the analysis of the distributions, we propose that in these communities epibiont species have a pattern of colonization in which they follow a behaviour as a whole; each species has a differential distribution, with the species occupying the available substratum with the particular requirements of each functional group, but there is a trend towards maintaining an equilibrium among species and groups, compensating for diversity and number of individuals. In all lakes there was an epibiont distribution model comprising the maintenance of an anteroposterior axis gradient, which was supported by the fluctuation in diversity and number of individuals of the different functional groups of epibiont species. The functional role of the different groups of species seems to tend towards sustainability with little global variation among the lakes.     

Prey preferences in captivity of the freshwater crab Potamonautes lirrangensis from Lake Malawi with special emphasis on molluscivory

Freshwater crabs play an important role for the diversification of shell morphologies in freshwater gastropods. For example, the radiation of the freshwater crab genus Platythelphusa in Lake Tanganyika is thought to have driven shell diversification of the lake’s snail fauna, promoting the evolution of thalassoid shells. No comparable thalassoid snails are known from Lake Malawi. Accordingly, it was hypothesized that the lake’s only freshwater crab, Potamonautes lirrangensis, is not a snail predator. We tested this hypothesis using feeding experiments with specimens caught in the southern part of Lake Malawi. Individual crabs were held in experimental containers offshore and were presented with various food items overnight, after which ingestion frequency was recorded. Potamonautes lirrangensis can be characterized as a scavenger that is opportunistically carnivorous. A preference for fish and snail flesh could be observed, indicating a bias toward carnivory. We observed occasional cracking of the shell in different snail species, with frequent ingestion of artificially crushed specimens, suggesting that crabs do attempt to feed on snails. However, the investigated Lake Malawi gastropods appear to be partly protected against crab predation through thick-walled and low-spired shells (especially Lanistes and Bellamya), obviating the evolution of thalassoid shells carrying rims, ridges, or spines.     

Oligochaeta and Aphanoneura in ancient lakes: a review

By their antiquity, history, rarity, great depth in many instances and the presence of highly diverse faunas with many endemics, ancient lakes constitute ecosystems of a special nature, clearly apart from the large majority of extant lakes. While the fauna of these lakes is becoming better and better known for various animals groups, the Oligochaeta are still poorly known. Tubificidae and Naididae are found in each ancient lake. On the other hand, some families are restricted to only one lake, such as Aeolosomatidae and Proppapidae in Lake Baikal or Eudrilidae and Ocnerodrilidae (megadriles) in Lake Tanganyika, but such a distribution is probably due to a lack of knowledge or sampling biases. All ancient lakes have an endemic oligochaete fauna except Lake Kinneret (Israël). The oldest, Lake Baikal (20–25 Ma), holds the most abundant and diverse oligochaete fauna, in which species flocks are even recognizable or suspected. In contrast, the oligochaete fauna of the slightly younger Lake Tanganyika is very scarce. This is partly due to an obvious lack of studies, as the oligochaete fauna of other great African lakes is virtually unknown, but this might be the result of an environment in these lakes less favourable to oligochaetes. Some factors likely to interact with speciation in oligochaetes are discussed but nothing can be concluded to date. A recent interest in African great lakes revealed a more diverse oligochaete fauna than previously assumed but a better study of this fauna is still badly needed.     

A tale of time and depth: intralacustrine radiation in endemic Gammarus species flock from the ancient Lake Ohrid

Tentatively dated, the Plio‐/Pleistocene origin of the ancient Lake Ohrid on the Balkan Peninsula makes it the oldest ancient lake in Europe. Given the surface area of the lake and the adjusted endemicity rate, it may be also defined as the most diverse of all the ancient lakes in the world. From all the animal groups endemic to this lake, gammarids are amongst the most scarcely known in terms of their diversity and phylogenetic relationships. Partial DNA sequences of two mitochondrial genes, cytochrome oxidase subunit I (cox1) and 16S ribosomal RNA (16S rRNA) of eight known endemic Gammarus species from the Lake Ohrid valley were analysed. Phylogenetic analyses showed that endemic Gammarus species comprise an ancient species flock, with Gammarus sketi from the feeder springs being their sister taxon outside the lake. Amongst the species inhabiting the lake, Gammarus solidus and Gammarus salemaai are morphologically and molecularly well defined. By contrast, Gammarus ochridensis, Gammarus parechiniformis, Gammarus lychnidensis, and Gammarus stankokaramani revealed high discrepancy between morphological and genetic data. None of these morphospecies form a monophyletic clade and a significant degree of apparent gene flow occurs between them. This could be caused by incomplete lineage sorting and/or hybridization events. Two novel mtDNA lineages were found within the lake, possibly constituting two new species (Gammarus sp. 1 and Gammarus sp. 2). Molecular clock analysis showed that the split between G. sketi and the Gammarus species flock from the lake occurred approximately 5–7 Mya, whereas within the flock there were at least two intralacustrine radiations: one estimated at 2–3 Mya and the second at less than 1 Mya. The first one could be associated with the origin of the lake and the second with the lake water‐level fluctuations during Pleistocene. © 2013 The Linnean Society of London     

ADAPTIVE RADIATION AND ECOLOGICAL DIVERSIFICATION OF SULAWESI'S ANCIENT LAKE SHRIMPS

Ancient lakes are natural laboratories for the study of adaptive radiation. Recently, two lake systems on the Indonesian island Sulawesi have emerged as promising new model systems. A species flock of atyid freshwater shrimps in the Malili lake system comprises 15 colorful endemic taxa. Mitochondrial DNA data suggest two independent colonizations by riverine ancestors. Only one colonization event led to subsequent radiation into 14 species, while the second clade comprises just one species. The vast majority of species (n= 12) are habitat specialists, which are confined to the larger Malili clade and include all taxa with species‐specific color patterns and a restricted distribution within the five connected Malili lakes. Morphological, genetic, and ecological data are consistent with the existence of an adaptive radiation in the Malili lakes, involving the habitat‐specific diversification of trophic morphology. In addition to testing criteria for the recognition of an adaptive radiation, an ancestral state reconstruction reveals an equal probability for either a riverine generalist or a lacustrine specialist as ancestor of the large Malili clade, which is interpreted as indicative of an early stage of habitat specialization within this radiation. Finally, our results suggest that species diversification may have been primarily driven by ecological specialization and allopatric speciation.     

The endemic molluscs of the Late Miocene Lake Pannon: their origin, evolution, and family-level taxonomy

Long-lived lakes are often sites of spectacular endemic radiations. During the Oligocene to recent history of the Paratethys, large, long-lived (more than a million years) lakes with endemic faunas formed three times, in three different basins: the first in the Pannonian basin, the second in the Euxinian (Black Sea) basin, and the third in the Caspian basin. Because the Euxinian lake inherited much of the fauna of Lake Pannon, the three lakes together hosted two endemic radiations of molluscs. The most long-lived lake in the region was Lake Pannon, which persisted approximately seven million years from the late Middle Miocene to the Early Pliocene. Lake Pannon was formed by isolation from the sea. Changes in hydrological regime and/or water chemistry in addition to the relative lowstand which accompanied (or caused) the isolation almost completely exterminated the restricted marine fauna of the basin. A few highly euryhaline and marginal marine cardiids, dreissenids, and hydrobiids survived this environmental change. As in other fossil and extant long-lived lakes, the originally low-diversity fauna radiated into a high number of related endemic species (‘species flocks’) and genera in the expanding and ecologically vacated lake. Many originally freshwater taxa (unionids, sphaeriids, viviparids, valvatids, melanopsids, lymnaeids, planorbids) entered the lake as well, and some of them also gave rise to endemic clades. Evolution in both relict and freshwater immigrant groups led to the appearance of highly unusual shell shapes. Many lineages exhibit gradual morphological changes over one to several million years. More than 900 endemic mollusc species have been described from Lake Pannon, although this number includes junior synonyms, invalid species names, and highly similar chronospecies. Applying a conservative taxonomy, all these species belong to four bivalve and eight gastropod families. The high degree of endemism, however, is reflected by proposals of some authors to establish as many as five new families based on Lake Pannon endemics.     

Nematodes from saline and freshwater lakes of the Vestfold Hills,East Antarctica,including the description of <Emphasis Type="Italic">Hypodontolaimus antarcticus</Emphasis> sp. n.

The invertebrate fauna of many Antarctic ice-free areas, even those close to permanent research stations, can be poorly known. Here we describe some nematodes from freshwater and saline, marine-derived lakes of the Vestfold Hills, East Antarctica. The freshwater lakes contained the widespread East Antarctic endemic species, Plectus frigophilus Kirjanova, 1958. The saline lakes were inhabited by two recently described species, Halomonhystera halophila Andrássy, 2006 and Halomonhystera continentalis Andrássy, 2006, and by a new species described in this report, Hypodontolaimus antarcticus sp. n. Originally marine but now brackish Highway Lake contained a nematode fauna with both freshwater and marine-derived components. The nematode fauna of Antarctica now consists of 54 named species, 22 of which are found in East Antarctica.     

The neglected side of speciation in ancient lakes: phylogeography of an inconspicuous mollusc taxon in lakes Ohrid and Prespa

The morphologically remarkable endemic fauna within ancient lakes has received much attention in the literature. More inconspicuous taxa, however, often lack detailed molecular and morphometrical examination, although their proportion of the endemic fauna of an ancient lake must not be underestimated. Consequently, a better understanding of evolutionary patterns and processes within these lakes requires more knowledge about the often-neglected inconspicuous taxa. In the present study, we focus on the notoriously cryptic pea clam genus Pisidium (Bivalvia: Sphaeriidae). Though the genus is widely distributed, most endemic species are reported only from ancient lakes, including the European ancient sister lake system of Ohrid and Prespa on the Balkan Peninsula. Here we test for the first time hypotheses on the evolution of the endemic pea clams in this European biodiversity hotspot by molecular means. Combining a broad 16S phylogeny (comprising most European pea clam species), network analyses and morphometrical analyses, we found interesting biogeographical patterns and provide evidence for cryptic species in both lakes. Furthermore, we confirmed the proposed sister-species relationship of the endemics P. edlaueri in Lake Ohrid and P. maasseni in Lake Prespa, and we suggest scenarios of the endemic pea clam evolution within both lakes. The patterns of speciation found in the genus Pisidium are compared to patterns in morphologically distinct molluscan groups in lakes Ohrid und Prespa.     

Testing two contrasting evolutionary patterns in ancient lakes: species flock versus species scatter in valvatid gastropods of Lake Ohrid

Ancient lakes have long been recognized as “hot spots of evolution” and “evolutionary theatres” and they have significantly contributed to a better understanding of speciation and radiation processes in space and time. Yet, phylogenetic relationships of many ancient lake taxa, particularly invertebrate groups, are still unresolved. Also, the lack of robust morphological, anatomical, and phylogeographical data has largely prevented a rigorous testing of evolutionary hypotheses. For the freshwater gastropod genus Valvata—a group with a high degree of endemism in several ancient lakes—different evolutionary scenarios are suggested for different ancient lakes. Lake Baikal, for example, is inhabited by several endemic Valvata taxa that presumably do not form a monophyletic group. For such an evolutionary pattern, the term ancient lake species scatter is introduced here. In contrast, for the Balkan Lake Ohrid, workers previously suggested the presence of a monophyletic group of endemic Valvata species, that is, an ancient lake species flock. Sequence data of the mitochondrial cytochrome oxidase c subunit I gene (COI) from worldwide taxa, with a strong emphasis on Balkan species, are here used to test whether the putative Ohrid Valvata endemics represent an ancient lake species flock and to study patterns of speciation both on the Ohrid and the Balkan scale. The study reveals three distinct clades of endemic Valvata in Lake Ohrid. Monophyly of these taxa, however, is rejected, and they therefore do not represent an ancient lake species flock, but rather an ancient lake species scatter. Also, in contrast to many other gastropod groups in Lake Ohrid, the valvatids apparently did not radiate. Many Valvata taxa in ancient lakes are characterized by enhanced levels of shell complexity. However, it remains unclear whether these patterns are associated with ancient lake environments per se. It is here suggested that similarities in shell structure between North American and Balkan taxa might simply be due to convergent evolution.     

Rapid evolution of an ancient lake species flock: Freshwater limpets (Gastropoda: Ancylidae) in the Balkan Lake Ohrid

Ancient lakes have long been recognized as evolutionary theatres and hot spots of endemism; the evolution of their morphologically often highly diverse species flocks has received much attention. However, as each ancient lake has its own geological and evolutionary history, modes of speciation may differ from system to system. Ancient lakes can act as evolutionary reservoirs that assure the survival of relict species, but at the same time extant species may evolve through intralacustrine speciation. Other aspects of interest are the actual rates of immigration, diversification or extinction as well as the temporal framework of morphological change. Many of these questions have been addressed in the African (e.g. Lake Tanganyika) and Asian (e.g. Lake Baikal) ancient lakes. For an European ancient lakes (e.g. Lakes Ohrid and Prespa), such studies are largely missing. In the present paper, extraordinarily shaped endemic freshwater limpets of the genus Ancylus from the Balkan Lake Ohrid are used in a phylogeographic and phylogenetic context to test whether they represent an ancient lake species flock, to study the mode of speciation, and to assess the timing of morphological change. Based on DNA data from two mitochondrial genes (COI, LSU rDNA), it has been found that the Lake Ohrid Ancylus species form an endemic monophyletic group. In addition, the lake's feeder springs are inhabited by another, undescribed Ancylus species. All other studied waterbodies within the watershed do not support their own Ancylus lineages but are inhabited by a widespread Mediterranean taxon. The split between the species endemic to the lake and its sister taxon is dated to 1.4±0.6 million years ago. The study presents the first genetic confirmation for the existence of a species flock in a European ancient lake. Contrary to the prevailing opinion it shows that, concerning Ancylus, Lake Ohrid represents a site of intralacustrine speciation rather than an evolutionary reservoir. Moreover, it provides the first evidence for rapid morphological change in an European ancient lake species flock. See also Electronic Supplement at: http://www.senckenberg.de/odes/06-12.htm.     

Role of ancient lakes in genetic and phenotypic diversification of freshwater snails

Endemic organisms of ancient lakes have been studied as models to understand processes of speciation and adaptive radiation. However, it remains unclear how ancient lakes play roles in genetic and phenotypic diversity of freshwater mollusks. In the present study, we focus on viviparid freshwater snails in the ancient lakes of East and Southeast Asia (Japan and China) to address this question. Using molecular phylogenetic analyses based on mitochondrial (COI, 16S) and nuclear genes (18S, 28S, H3), we show that patterns of species diversification in viviparid lineages. Colonization to ancient lakes occurred independently in China and Japan at least four times, with subsequent diversification into more than two species within each lake group. Morphological analyses of fossil related viviparids suggest parallel phenotypic evolution occurred in the different lakes and ages. Each lake contained a single lineage which was phenotypically diversified relative to those from other sites. Using genome‐wide SNPs obtained by MIG‐seq, we also examined the genetic structure of three Japanese viviparids, including two endemic species of ancient Lake Biwa. The results suggest that these two species diversified from the population of the third species living in wetlands surrounding the lake. These findings suggest that rapid diversification of lineages and phenotypic divergence can occur in ancient lakes compared to other habitats. Formation of large lakes probably promotes speciation and phenotypic divergence as a result of adaptation into different microhabitats. High numbers of ancient lakes could be a driver of species diversity in Asian viviparid snails.     

Ancient Lake Ohrid: biodiversity and evolution

Worldwide ancient lakes have been a major focal point of geological, biological, and ecological research, and key concepts in, for example, evolutionary biology are partly based on ancient lake studies. Ancient lakes can be found on most continents and climate zones with most actual or putative ancient lakes in Europe being restricted to the Balkan Region. The arguably most outstanding of them is the oligotrophic and karstic Lake Ohrid, a steep-sided graben of rift formation origin situated in the central Balkans. Here, an attempt is made to summarize current knowledge of the geological, limnological, and faunal history of Lake Ohrid. Additionally, existing data on biodiversity and endemism in Lake Ohrid are updated and evaluated, and patterns and processes of speciation are reviewed in the context of the Ohrid watershed, including its sister lake, Lake Prespa. Whereas the geological history of the Ohrid Graben is relatively well studied, there is little knowledge about the limnological and biotic history of the actual lake (e.g., the age of the extant lake or from where the lake first received its water, along with its first biota). Most workers agree on a time frame of origin for Lake Ohrid of 2–5 million years ago (Mya). However, until now, the exact limnological origin and the origin of faunal or floral elements of Lake Ohrid remain uncertain. Two largely contrasting opinions either favour the theory of de novo formation of Lake Ohrid in a dry polje with a spring or river hydrography or a palaeogeographical connection of Lake Ohrid to brackish waters on the Balkan Peninsula. Whereas neither theory can be rejected at this point, the data summarized in the current review support the de novo hypothesis. An assessment of the fauna and flora of Lake Ohrid confirms that the lake harbours an incredible endemic biodiversity. Despite the fact that some biotic groups are poorly studied or not studied at all, approximately 1,200 native species are known from the lake, including 586 animals, and at least 212 species are endemic, including 182 animals. The adjusted rate of endemicity is estimated at 36% for all taxa and 34% for Animalia. In terms of endemic biodiversity, Lake Ohrid is with these 212 known endemic species and a surface area of 358 km² probably the most diverse lake in the world, taking surface area into account. Preliminary phylogeographical analyses of endemic Lake Ohrid taxa indicate that the vast majority of respective sister taxa occurs in the Balkans and that therefore the most recent common ancestors of Ohrid- and non-Ohrid species likely resided in the region when Lake Ohrid came into existence. These data also indicate that there is relatively little faunal exchange and overlap between Lake Ohrid and its sister lake, Lake Prespa, despite the fact that the latter lake is a major water supplier for Lake Ohrid. Studies on selected species flocks and scatters, mostly in molluscs, point towards the assumption that only few lineages originally colonized Lake Ohrid from the Balkans and that the majority of endemic species seen today probably started to evolve within the lake during the early Pleistocene. Within the Ohrid watershed, endemism occurs at different spatial and taxonomic scales, ranging from species endemic to certain parts of Lake Ohrid to species endemic to the whole watershed and from subspecies to genus level and possibly beyond. Modes of speciation in the Ohrid watershed are largely affected by its degree of isolation. Observational evidence points towards both allopatric (peripatric) and parapatric speciation. Though sympatric speciation within a habitat is conceivable, so far there are no known examples. Today, the lake suffers from increasing anthropogenic pressure and a “creeping biodiversity crisis”. Some endemic species presumably have already gone extinct, and there are also indications of invasive species penetrating Lake Ohrid. The comparatively small size of Lake Ohrid and the extremely small range of many endemic species, together with increasing human pressure make its fauna particularly vulnerable. It is thus hoped that this review will encourage future research on the ecology and evolutionary biology of the lake’s taxa, the knowledge of which would ultimately help protecting this unique European biodiversity hot spot. Guest editors: T. Wilke, R. V?in?l? & F. Riedel Patterns and Processes of Speciation in Ancient Lakes: Proceedings of the Fourth Symposium on Speciation in Ancient Lakes, Berlin, Germany, September 4–8, 2006     

A conservation assessment of the freshwater crabs of southern Africa (Brachyura: Potamonautidae)

Recent taxonomic revisions of the freshwater crabs of southern Africa (Angola, Botswana, Lesotho, Mozambique, Namibia, South Africa, Swaziland, Zambia and Zimbabwe) allow accurate depictions of their diversity, distribution patterns and conservation status. The southern African region is home to nineteen species of freshwater crabs all belonging to the genus Potamonautes (family Potamonautidae). These crabs show high levels of species endemism (84%) to the southern African region and to the country of South Africa (74%). The conservation status of each species is assessed using the IUCN (2003) Red List criteria, based on detailed compilations of the majority of known specimens. The results indicate that one species should be considered vulnerable, fifteen species least concern and three species data deficient. The results have been utilized by the IUCN for Red Lists, and may prove useful when developing a conservation strategy for southern Africa’s endemic freshwater crab fauna.