Old fossils–young species: evolutionary history of an endemic gastropod assemblage in Lake Malawi

Studies on environmental changes provide important insights into modes of speciation, into the (adaptive) reoccupation of ecological niches and into species turnover. Against this background, we here examine the history of the gastropod genus Lanistes in the African Rift Lake Malawi, guided by four general evolutionary scenarios, and compare it with patterns reported from other endemic Malawian rift taxa. Based on an integrated approach using a mitochondrial DNA phylogeny and a trait-specific molecular clock in combination with insights from the fossil record and palaeoenvironmental data, we demonstrate that the accumulation of extant molecular diversity in the endemic group did not start before approximately 600 000 years ago from a single lineage. Fossils of the genus from the Malawi Rift, however, are over one million years older. We argue that severe drops in the lake level of Lake Malawi in the Pleistocene offer a potential explanation for this pattern. Our results also challenge previously established phylogenetic relationships within the genus by revealing parallel evolution and providing evidence that the endemic Lanistes species are not restricted to the lake proper but are present throughout the Malawi Rift.     

Allozyme and morphology evolution in European Viviparidae (Mollusca: Gastropoda: Architaenioglossa)

The paper describes morphometric and allozymic differences among four European species of the family Viviparidae: Viviparus contectus (Millet, 1813), V. viviparus (Linnaeus, 1758), V. acerosus Bourguignat, 1862, and V. ater (Cristofori et Jan, 1832). Fourteen continuous biometrical characters were measured. Incremental discriminant-function analysis, principal-component analysis, and non-metric multidimensional scaling were applied to analysis of the morphometric differences. All the techniques confirmed a similar picture: a slight morphometric differentiation, with the variability ranges of the species overlapping. On the other hand, the allozymic differentiation, studied at 12 loci, eight of them intra and/or interspecific polymorphic, is much better marked, the intraspecific Nei's distances among the four V. contectus populations ranging from 0.0014 to 0.0397, mean 0.0166, and interspecific distances ranging from 0.2306 (V. ater–V. acerosus) to 0.9888 (V. contectus 2 and V. viviparus), mean 0.6871. The allele frequencies and genetic distances (Nei's distance and Cavalli-Sforza and Edwards’chord distance) were used to compute maximum likelihood, additive Fitch–Margoliash and ultrametric Fitch–Margoliash trees. All the trees presented a similar pattern, but the maximum-likelihood and additive trees, based on Cavalli-Sforza and Edwards’distance, seem to reflect the phylogeny best. The results are compared with the most parsimonious phylogenies inferred for radular, soft-part morphology and anatomy, and opercular data from other papers by us, and the inferred phylogenies are also compared. Although the inferred molecular and morphological phylogenies are little different in topology, the amount of evolution along the corresponding branches (measured as the number of changes averaged over all reconstructions) is very different, the value of correlation coefficient between the two phylogenies being statistically insignificant. The occurrence of interspecific hybrids is discussed, and the isolation-by-competition mechanism is postulated. The probable origin of V. viviparus from a founder population extremely restricted in number is stressed. The possible history of the group is briefly discussed. The species is suggested to have originated in an unusual habitat of melt water at a glacier foreland that could have promoted genotypic differentiation and sympatric speciation.     

Shallow genetic divergence and species delineations in the endemic Labeobarbus species flock of Lake Tana,Ethiopia

To assess whether the species distinctions of Lake Tana's Labeobarbus spp. are supported by genetic information, microsatellite markers were used. A total of 376 Labeobarbus spp., belonging to 24 populations of 11 species from three regions of the lake (north, south and east), were sampled. Eight microsatellite markers were analysed. In general, differences between conspecific populations were smaller than differences between populations of different species. For six species, conspecific populations from different regions in the lake were consistently more similar than populations of other species from the same region. For four species this was not the case, while for one species two populations were similar, but different from the third population. River‐spawning species appeared to be more distinct than presumed lake spawners. On the species level, there was a significant correlation between genetic and morphological differentiation, especially in morphological aspects associated with ecological functioning. This suggests that genetic differentiation arose together with adaptive radiation, although the overall genetic differentiation among the Lake Tana Labeobarbus spp. is small.     

Phylogenomics of pike cichlids (Cichlidae: Crenicichla): the rapid ecological speciation of an incipient species flock

The rapid rise of phenotypic and ecological diversity in independent lake‐dwelling groups of cichlids is emblematic of the East African Great Lakes. In this study, we show that similar ecologically based diversification has occurred in pike cichlids (Crenicichla) throughout the Uruguay River drainage of South America. We collected genomic data from nearly 500 ultraconserved element (UCEs) loci and >260 000 base pairs across 33 species, to obtain a phylogenetic hypothesis for the major species groups and to evaluate the relationships and genetic structure among five closely related, endemic, co‐occurring species (the Uruguay River species flock; URSF). Additionally, we evaluated ecological divergence of the URSF based on body and lower pharyngeal jaw (LPJ) shape and gut contents. Across the genus, we recovered novel relationships among the species groups. We found strong support for the monophyly of the URSF; however, relationships among these species remain problematic, likely because of the rapid and recent evolution of this clade. Clustered co‐ancestry analysis recovered most species as well delimited genetic groups. The URSF species exhibit species‐specific body and LPJ shapes associated with specialized trophic roles. Collectively, our results suggest that the URSF consists of incipient species that arose via ecological speciation associated with the exploration of novel trophic roles.     

Evidence for parallel ecological speciation in scincid lizards of the Eumeces skiltonianus species group (Squamata: Scincidae)

We identify instances of parallel morphological evolution in North American scincid lizards of the Eumeces skiltonianus species group and provide evidence that this system is consistent with a model of ecological speciation. The group consists of three putative species divided among two morphotypes, the small-bodied and striped E. skiltonianus and E. lagunensis versus the large-bodied and typically uniform-colored E. gilberti. Members of the group pass through markedly similar phenotypic stages during early development, but differ with respect to where terminal morphology occurs along the developmental sequence. The morphotypes also differ in habitat preference, with the large-bodied gilberti form generally inhabiting lower elevations and drier environments than the smaller, striped morphs. We inferred the phylogenetic relationships of 53 skiltonianus group populations using mtDNA sequence data from the ND4 protein-coding gene and three flanking tRNAs (900 bp total). Sampling encompassed nearly the entire geographic range of the group, and all currently recognized species and subspecies were included. Our results provide strong evidence for parallel origins of three clades characterized by the gilberti morphotype, two of which are nested within the more geographically widespread E. skiltonianus. Eumeces lagunensis was also nested among populations of E. skiltonianus. Comparative analyses using independent contrasts show that evolutionary changes in body size are correlated with differences in adult color pattern. The independently derived association of gilberti morphology with warm, arid environments suggests that phenotypic divergence is the result of adaptation to contrasting selection regimes. We provide evidence that body size was likely the target of natural selection, and that divergences in color pattern and mate recognition are probable secondary consequences of evolving large body size.     

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.     

A new species of freshwater snail Tchangmargarya (Gastropoda: Viviparidae) endemic to a vanished small lake in Yunnan,China

Habitat loss poses a grave threat to endemic species with narrow distributions. Some species become extinct even before scientific identification due to habitat destruction. Here, a probable example is reported based on some recent and subfossil shells from an almost disappeared wetland lake in Yunnan Province, China. A new ornamented freshwater snail species, Tchangmargarya ziyi n. sp., is recognised and described based on morphological comparison with the other Tchangmargarya species. The subfossil specimens of the new species show a great similarity to Tchangmargrya yangtsunghaiensis (Tchang & Tsi, 1949), indicating their potentially close relationship. The discovery of the new species demonstrates that the plateau lakes of Yunnan, even the small ones, have a high biodiversity and endemism. Furthermore, it enriches the knowledge of the distribution of Tchangmargarya and provides further evidence that the Liangwang Mountains are a significant biogeographic barrier to three endemic viviparid genera (Margarya, Anularya and Tchangmargarya) of Yunnan. Since the only known habitat of this species has been mostly landfilled due to the construction of a golf course and villas, this species possibly has already gone extinct. In order to implement conservation measures more efficiently, more comprehensive surveys should be conducted in all plateau lakes of Yunnan, including those that might seem insignificant.     

An example of intralacustrine evolution at an early stage: the freshwater ostracods of the Miocene crater lake of Steinheim (Germany)

I present the findings of two detailed studies on Steinheim lake ostracods carried out over the last eight years. The 178 samples studied cover a combined section about 30 m thick, comprising the whole sequence of seven planorbid beds. Of the 53 species found, 44 occur in the basic sediment layers, the kleinibeds. In contrast, all of the subsequent beds contain 16 species, and only seven species withstood the extinction at the kleini–steinheimensis boundary.This may be mainly due to the loss of littoral habitats brought about by a constantly increasing lake level, as the majority of the species in the kleinibeds were shallow water dwellers. Long-term lake level fluctuations are considered the most important external factor of the post-kleini period. Density fluctuations of the ostracods Pseudocandona steinheimensis and Potamocypris gracilis broadly reflect these water level fluctuations. At the beginning of the sulcatusperiod, when the lake level was very high, some species show morphological changes in their carapaces. During this time Leucocythere immigrata split into the daughter species L. sieberi and L. esphigmena. In the following trochiformis period, when the water level was lowest, the most curious carapace sculptures appear. The morphological changes detected, however, cannot simply be interpreted as ecophenotypic. The speciation event in Leucocythere, the non-recolonization with ubiquitous species during the low water level stage (trochiformis period), as well as the types of morphological changes indicate mainly evolutionary processes, as also the planorbid molluscs prove. Moreover, ostracods and planorbids show convergent evolutionary patterns. Compared with data on ostracod speciation in ancient lakes, the ostracod assemblage of Lake Steinheim seems to be a good palaeontological example of intralacustrine evolution at an early stage.     

Sexual selection,reproductive behavior,and speciation in the mbuna species flock of Lake Malawi (Pisces: Cichlidae)

Synopsis The cichlid species flocks of the African Great Lakes represent the most extreme case of adaptive radiation among vertebrates. Recently, attention has focused on the potential for sexual selection to drive or accelerate speciation in these fishes. Cichlids as a whole are social in nature and display complex behavior, particularly during courtship and spawning; however, the extent to which changes in species recognition cues may account for species diversity among haplochromine lineages has remained speculative. Our investigations have indicated that oral incubating haplochromines show a reduction in diversity and extent of courtship relative to substrate brooding cichlids, and apparently retain aspects of a primitive specific mate recognition system. Laboratory observations of courtship in the Malawian endemicPseudotropheus zebra suggest that organization of the spawning bout is loose, and lacking in any well defined stimulus-response chain. Interspecific comparisons of in situ courtship behavior among male mbuna, lithophilous haplochromines of Lake Malawi, revealed only one potential example of species-specific behavior, and indicated that mate choice occurred prior to the onset of intense courtship. Courtship display by male mbuna does not appear critical to species recognition and may represent an evolutionary relict. Alternatively, male courtship display may have an indirect effect on successful reproduction or may be maintained through pleiotropic effects. The mbuna display no evidence of behavioral innovation and show limited interspecific differentiation in behavioral expression. More generally, there is no evidence at present to suggest that epigamic sexual selection, acting on courtship behavior, has been a major mechanism in the diversification of the haplochromine species flocks.     

Molecular phylogenetics of the Macaronesian-endemic genus Bystropogon (Lamiaceae): palaeo-islands, ecological shifts and interisland colonizations

Abstract A molecular phylogenetic study of Bystropogon L'Her. (Lamiaceae) is presented. We performed a cladistic analysis of nucleotide sequences of the internal transcribed spacers (ITS), of the nuclear ribosomal DNA, and of the trnL gene and trnL-trnF intergenic spacer of the chloroplast DNA. Bystropogon odoratissimus is the only species endemic to the Canary Islands that occurs in the three palaeo-islands of Tenerife. This species is not part of an early diverging lineage of Bystropogon and we suggest that it has a recent origin. This phylogenetic pattern is followed by most of the species endemic to the palaeo-islands of Tenerife. The two sections currently recognized in Bystropogon form two monophyletic groups. Taxa belonging to the section Bystropogon clade show interisland colonization limited to the Canary Islands with ecological shifts among three ecological zones. Taxa from the section Canariense clade show interisland colonization both within the Canary Islands and between the Canary Islands and Madeira. Speciation events within this clade are mostly limited to the laurel forest. The genus has followed a colonization route from the Canaries towards Madeira. This route has also been followed by at least five other plant genera with species endemic to Macaronesia. Major incongruences were found between the current infrasectional classification and the molecular phylogeny, because the varieties of Bystropogon origanifolius and Bystropogon canariensis do not form two monophyletic groups. The widespread B. origanifolius appears as progenitor of the other species in section Bystropogon with a more restricted distribution.     

The late Cenozoic Viviparidae (Mollusca, Gastropoda) of the Albertine Rift Valley (Uganda—Congo)

During late Cenozoic pre-rift times the viviparid genus Bellamya was probably confined to eastern Africa while in the Congo Basin occurred the genera Neothauma and Kaya (a new genus described herein). During the Pliocene, Kaya became extinct and Neothauma became a relict in Lake Tanganyika. All African rift lakes formed during or after the Pliocene were colonised by populations of Bellamya, which evolved into lacustrine endemics. The changes in shell morphology in Bellamya, such as ornamentation functioning as protection against predators, are modest and repetitive in time and space. After the initial adaptations stasis followed, and there is no indication of an arms race between prey and predator in this genus. In the lakes of the western rift that were formed prior to the Pliocene, namely Lake Tanganyika and Palaeolake Obweruka, Neothauma instead of Bellamya was the coloniser. Initially morphological inertia also occurred in this genus both in Tanganyika and, during the first four million years of its existence, in Palaeolake Obweruka, although from the outset this lake contained abundant highly specialised molluscivorous fishes. About 4.5 Ma a major extinction event occurred in the Obweruka Basin which led to the extermination of 50% of the molluscan species but none of the molluscivores. Among the viviparids, only one of the Neothauma species survived, its populations isolated and highly reduced in numbers. Immediately after this crisis a conchological quantum change occurred, the surviving lineage changing into a strongly ornamented thalassoid form. The dramatic morphological change is deemed to have been due to focussed selection by the predators on isolated and small prey populations. A radiative event immediately followed, producing still more strongly ornamented forms. The morphological changes that occurred in the Obwerukan Neothauma, in comparison to the modest and repeated patterns of evolution that can be observed in viviparids from other lakes, provides an example of true or quantum evolutionary change and yields evidence as to how it may have occurred. The fossil record of the fresh water molluscs of the Albertine Basin, thanks to its duration (ca. 12 million years), its relatively fine resolution (0.5–1.0 million years) and its sound chronostratigraphic framework, is a unique resource for understanding the tempo and mode of macroevolution. This revised version was published online in July 2006 with corrections to the Cover Date.     

Trophic differentiation in the phylogenetically young Cyprinodon species flock (Cyprinodontidae, Teleostei) from Laguna Chichancanab (Mexico)

Analysis of the gut contents of six syntopic Cyprinodon species from Laguna Chichancanab, Mexico, shows that the supposed basal form, C. beltrani , feeds on detritus and has the longest gut. All other species have significantly shorter guts. Whereas C. simus exclusively ingests detritus despite short gut length, all other species additionally rely on different benthic invertebrates. Each species has developed specific preferences: C. labiosus (amphipods), C. verecundus (bivalves), C. maya (ostracods and gastropods) and C. esconditus (ostracods and chironomid larvae). However, all of them ingest a minimum of c. 40% detritus. According to Schoener's index, pairwise niche overlap varies from c. 40% to over 95% in the species flock. Contrary to this, there is almost no overlap between the members of the flock and the only other native fish species, Gambusia sexradiata , which feeds nearly exclusively on terrestrial arthropods dropping on the water surface. Recently, the cichlid genus Oreochromis and the characid Astyanax fasciatus gained access to the lake. The cichlids show moderate to high niche overlap, whereas in A. fasciatus it is low. © 2005 The Linnean Society of London, Biological Journal of the Linnean Society , 2005, 85 , 125–134.     

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     

Phylogeographic history of the genus Tropheus,a lineage of rock-dwelling cichlid fishes endemic to Lake Tanganyika

Lake Tanganyika contains the oldest and most complex flock of cichlid fishes counting about 200 endemic species. It is comprised of 16 ecologically, morphologically and genetically highly distinct tribes. Many species are further subdivided into arrays of geographic morphs, each colonizing particular sections of the shore line. The genus Tropheus represents the most spectacular and best studied example for this phenomenon, counting more than 100 distinctly colored populations and sister species, some living in sympatry. Their present distribution and genetic structure was shaped by a series of lake level fluctuations which caused cycles of isolation and secondary admixis. The present study extends previous work on the phylogeography of Tropheus and aims at the fine-scale reconstruction of the origin and spread of lineages in the central and southern basin of the lake. The previously defined mtDNA lineages were evaluated on the basis of statistical parsimony networks. Haplotype networks were created for each lineage and related to their centers of diversity in terms of present distribution. A linearized tree analysis and a mismatch distribution analysis corroborate two of the three radiation waves suggested in earlier works, but the new data suggest a different primary colonization scenario for the southern basin.     

Evolution of distribution and habitat patterns in endemic millipedes of the genus Dolichoiulus (Diplopoda: Julidae) on the Canary Islands, with notes on distribution patterns of other Ganarian species swarms

Forty-six species of the genus Dolichoiulus , all endemic, occur on the Canary Islands The highest number of species occur on the largest, highest island (Tenerife); fewest occur on Lanzarote, Fuerteventura (low, xeric), El Hierro and La Palma (small, remote). Most of the Dolichoiulus species live on one island only, as in other endemic Canarian species swarms. The scarcity of pluri-insular Dolichoiulus species, in connection with information on phylogeny, suggests that speciation has mainly taken place within individual islands. Distribution patterns are partly governed by habitat differences between species, but vicariance patterns between species living in the same kind of habitat are evident on La Gomera and Tenerife. Dolichoiulus species occur in all kinds of natural habitats. Laurisilva and cave species are generally paler than other species. In the laurisilva of eastern Tenerife, microhabitat differentiation between species is pronounced. In some, but far from all, cases, species coexisting in the same microhabitat are of different sizes. The ancestral colonizing species of Dolichoiulus is/are hypothesized to have been small and to have lived in coastal habitats. Colonization of higher altitudes was usually accompanied by an increase in body size. Invasion of the laurisilva was usually accompanied by a habitat shift from the ground layer to logs.     

A new freshwater snail genus (Hydrobiidae,Gastropoda) from Montenegro,with a discussion on gastropod diversity and endemism in Skadar Lake

Karucia sublacustrina a new species of freshwater snails (Hydrobiidae, Gastropoda) is described based on material collected from Skadar Lake (Montenegro, Albania). The new species belongs to monotypic genus Karuciagen. n. The shell morphology and body shape of the new genus resembles Radomaniola Szarowska, 2006 and Grossuana Radoman, 1973, from which it differs in the larger shells with relatively slim and a slightly, but clearly shouldered body whorl. The number of gastropods from Skadar Lake basin tallies now 50 species. The adjusted rate of gastropod endemicity for Skadar Lake basin is estimated to be 38%. By compiling faunal and taxonomic data we also aim to provide information of relevance as to conservation efforts.