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.     

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.     

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.     

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.     

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.     

Genetic mosaic in a marine species flock

We used molecular approaches to study the status of speciation in coral reef fishes known as hamlets (Serranidae: Hypoplectrus). Several hamlet morphospecies coexist on Caribbean reefs, and mate assortatively with respect to their strikingly distinct colour patterns. We provide evidence that, genetically, the hamlets display characteristics common in species flocks on land and in freshwaters. Substitutions within two mitochondrial DNA (mtDNA) protein-coding genes place hamlets within a monophyletic group relative to members of two related genera (Serranus and Diplectrum), and establish that the hamlet radiation must have been very recent. mtDNA distances separating hamlet morphospecies were slight (0.6 +/- 0.04%), yielding a coalescent estimate for the age of the hamlet flock of approximately 430 000 years. Morphospecies did not sort into distinct mtDNA haplotype phylogroups, and alleles at five hypervariable microsatellite loci were shared broadly across species boundaries. None the less, molecular variation was not distributed at random. Analyses of mtDNA haplotype frequencies and nested clades in haplotype networks revealed significant genetic differences between geographical regions and among colour morphospecies. We also observed significant microsatellite differentiation between geographical regions and in Puerto Rico, among colour morphospecies; the latter providing evidence for reproductive isolation between colour morphospecies at this locale. In our Panama collection, however, colour morphospecies were mostly genetically indistinguishable. This mosaic pattern of DNA differentiation implies a complex interaction between population history, mating behaviour and geography and suggests that porous boundaries separate species in this flock of brilliantly coloured coral reef fishes.     

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 phyletic study on lacustrine haplochromine fishes (Perciformes, Cichlidae) of East Africa, based on scale and squamation characters

Phyletic relations within the haplochromine cichlids of East Africa were investigated using scale and squamation characters. Within the L. Victoria–Edward–Kivu species flock most of the genera proposed in Greenwood's revision could be confirmed by this approach. In addition the genera could be interrelated phylogenetically. They form two distinct superlineages comprising several genera each. The genus Astatotilapia as conceived by Greenwood is diphyletic. The fluviatile members of the genus form the sister taxon of the L. Victoria–Edward–Kivu flock, while the rest are a subgroup of that flock. The flock seems to be of monophyletic origin.     

Mitochondrial phylogeny of the Lamprologini, the major substrate spawning lineage of cichild fishes from Lake Tanganyika in eastern Africa

Lake Tanganyika harbors the oldest, morphologically and behaviorally most diverse flock of cichlid species. While the cichlids in Lakes Malawi and Victoria breed their eggs exclusively by buccal incubation (termed "mouthbrooding"), the Tanganyikan cichlid fauna comprise mouthbrooding and substrate-spawning lineages (fish spawn on rocks, and never orally incubate eggs or wrigglers). The substrate-spawning tribe Lamprologini appears to occupy a key position that might allow one to elucidate the origin of the Tanganyika flock, because five riverine (therefore nonendemic) species from the Zaire River system have been assigned to this tribe, in addition to the lake's endemic species, which make up almost 50% of all 171 species known from this lake (Poll 1986). From 16 species (18 individuals) of the tribe Lamprologini, a 402-bp segment of the mitochondrial cytochrome b gene was sequenced, and, from 25 lamprologine species (35 individuals), sequences from the mitochondrial control region were obtained. To place the Lamprologini into a larger phylogenetic framework, orthologous sequences were obtained from eight nonlamprologine Tanganyikan cichlid species (13 individuals). The Lamprologini are monophyletic, and a clade of six Tanganyikan lineages of mouthbrooders, representing five tribes (Poll 1986), appears to be their sister group. Comparisons of sequence divergences of the control region indicate that the Lamprologini may be older than the endemic Tanganyikan tribe Ectodini, and short basal branches might suggest a rapid formation of lineages at an early stage of the Tanganyika radiation. It is interesting that three analyzed riverine members of the tribe form a monophyletic group; however, they are not the most ancestral branch of the Lamprologini. This might indicate that they are derived from an endemic lamprologine ancestor that left Lake Tanganyika by entering the Zaire River system. These riverine species may not have seeded the Tanganyikan radiation, as currently thought, but may have recently recolonized the river after a long period of isolation, as soon as the lake was connected to the Zaire River again about 2 Mya. Neolamprologus moorii, endemic to Lake Tanganyika, appears to represent the most basal clade of the Lamprologini. Complex breeding behavior, involving the usage of gastropod shells and associated with dwarfism, is likely to have evolved in parallel in several lineages among the Lamprologini. The tribe Lamprologini may be in need of revision, since several genera appear to be polyphyletic.      

Genetic differentiation and reproductive isolation in a Cyprinodon fish species flock from Laguna Chichancanab, Mexico

The Cyprinodon species flock from Laguna Chichancanab, aged 8000 years, provides another potential case of sympatric speciation. The flock consists of seven morphologically distinct species, each within partially different trophic niches, and a group of specimens which cannot unequivocally be assigned to one of these species. Genetic analyses, based on mtDNA and five microsatellite loci, revealed significant genetic differentiation of one species, C. maya, from other members of the species flock, providing strong evidence for reproductive isolation. For the remaining members of the flock significant genetic structuring was detected, with some evidence of gene flow with the most abundant species C. beltrani. These analyses suggest that speciation proceeds with ongoing hybridisation, and further suggest that the morphologically unidentifiable specimens found in the lake are probably hybrids. I propose that in the Cyprinodon species flock besides disruptive selection sexual selection plays an important part in achieving and maintaining reproductive isolation.     

On the evolution of Gomphocythere (Crustacea,Ostracoda) in Lake Nyassa/ Malawi (East Africa), with the description of 5 new species

Five new species of the ostracod genus Gomphocythere are described from Lake Nyassa/ Malawi (East Africa). The morphology of the hemipenis in this genus is redescribed and the different parts are homologised with those of the Limnocytherinae and of other Timiraseviinae. The female abdominal structures are re-examined and a new terminology is proposed. Based on both valve and soft part morphology, the five new species are assumed to belong to a monophyletic cluster, which to all probability evolved within the lake itself. Indications for speciation by both natural and sexual selection are found. Natural selection could have been parapatric along a bathymetric cline; sexual selection involves at least characters related to the copulatory complex of the hemipenis. Closest congeners to the present species flock are the non-Tanganyikan, East African species, rather than those belonging to the southern African G. capensis complex.     

The microsoroid ferns: Inferring the relationships of a highly diverse lineage of Paleotropical epiphytic ferns (Polypodiaceae, Polypodiopsida)

The relationships of the microsoroid ferns were studied using a DNA sequence-based phylogenetic approach. Nucleotide sequences for up to four chloroplast genome regions were assembled for 107 samples from 87 species. Microsoroids s.l. include six lineages of which two are species rich. The results indicate that several genera are not monophyletic (e.g. Microsorum), several controversial genera are confirmed to be monophyletic (e.g. Leptochilus), and some genera new to science should be recognized (M. membranaceum clade). Unique insights were gained into the biogeographic history of this highly diverse epiphytic vascular plant lineage that is widespread in continental Asia to Australasia. Evidence was found for splits into lineages diversifying in parallel in continental Asia and Malesia. No evidence was recovered for an African radiation because all African microsoroid species either also are found in Asia or have sister species in continental Asia. In contrast, evidence for independent radiations were discovered for the Australasian region.     

A phylogenetic analysis and taxonomic revision of ricefishes,Oryzias and relatives (Beloniformes,Adrianichthyidae)

Ricefishes, known best by the model organism, the medaka, Oryzias latipes Temminck & Schlegel, 1846, comprise the family Adrianichthyidae, which ranges broadly throughout fresh and brackish waters of Central, South and Southeast Asia and the Indo‐Malay‐Philippines Archipelago as far east as Timor. Twenty‐eight Recent species are recognized here in two monophyletic genera, Adrianichthys and Oryzias. Xenopoecilus and Horaichthys are placed in synonymy of Oryzias for the first time. Adrianichthys comprises four species from Lake Poso, Sulawesi, Indonesia. Oryzias comprises 24 species that live throughout the range of the family. A fossil genus and species, ?Lithopoecilus brouweri from the Miocene of central Sulawesi, is included tentatively in the Adrianichthyidae. Evidence for the sister group relationship of adrianichthyids and exocoetoids is reviewed briefly and that relationship corroborated. Monophyly of adrianichthyids is likewise strongly supported here. Species groups within Oryzias are diagnosed as monophyletic largely based on osteology, colour pattern and meristic variation. They correspond only in part to species groups previously recognized based on chromosome constitution. Miniature species do not comprise a monophyletic group; disjunct absolute size in close relatives has evolved repeatedly. Oryzias latipes is a member of a species complex that includes O. luzonensis, O. curvinotus and the miniatures O. sinensis and O. mekongensis. A new species, Oryzias bonneorum sp. nov. , is described from Lake Lindu, Sulawesi, Indonesia. Lectotypes are designated for Haplochilus celebensis Weber, 1894 and Haplochilus timorensis Weber & de Beaufort, 1922. No claim to original US Government works. Journal compilation © 2008 The Linnean Society of London, Zoological Journal of the Linnean Society, 2008, 154 , 494–610.     

The macroecology of rapid evolutionary radiation

A long-standing debate in ecology addresses whether community composition is the result of stochastic factors or assembly rules. Non-random, over-dispersed patterns of species co-occurrence have commonly been attributed to competition--a particularly important force in adaptive radiation. We thus examined the macroecology of the recently radiated cichlid rock-fish assemblage in Lake Malawi, Africa at a spectrum of increasingly fine spatial scales (entire lake to depth within rock-reef sites). Along this range of spatial scales, we observed a signal of community structure (decreased co-occurrence of species) at the largest and smallest scales, but not in between. Evidence suggests that the lakewide signature of structure is driven by extreme endemism and micro-allopatric speciation, while patterns of reduced co-occurrence with depth are indicative of species interactions. We identified a 'core' set of rock-reef species, found in combination throughout the lake, whose depth profiles exhibited replicated positive and negative correlation. Our results provide insight into how ecological communities may be structured differently at distinct spatial scales, re-emphasize the importance of local species interactions in community assembly, and further elucidate the processes shaping speciation in this model adaptive radiation.     

Molecular phylogeny of Palearctic-African Acrocephalus and Hippolais Warblers (Aves: Sylviidae)

Phylogenetic relationships of the reed warbler group (genera Acrocephalus, Hippolais, Chloropeta; Aves: Passeriformes) and their potential relatives were studied using nucleotide sequences (1 kb) of the mitochondrial cytochrome b gene. This species-rich but morphologically poorly differentiated group of insectivorous passerines is distributed in Eurasia, Africa, and Australasia. Intergeneric relationships were poorly resolved, but monophyly of the reed warbler group (including Chloropeta) versus other Sylviidae was strongly supported. A basal polytomy within the reed warbler group consists of seven branches and may indicate a rapid early radiation. In the genus Acrocephalus three major clades were identified, which corresponded to phenotypic groups characterized by body size and plumage patterns. However, current delimitation of some subgenera (Acrocephalus, Lusciniola, Bebrornis) is at variance with our phylogeny estimate, and appropriate revisions are proposed. The genus Hippolais, which may or may not be monophyletic, consisted of two well-supported clades of four species each. Some Acrocephalus taxa whose species status had been doubted (griseldis, tangorum, orientalis, australis) proved to be highly distinct genetically. Genetic distances between members of two pairs of allopatric Hippolais taxa (caligata/rama; opaca/elaeica) were as large or larger than between other closely related warbler species. Overall, cytochrome b sequences resolved phylogenetically young relationships quite well, whereas more ancient nodes remained poorly resolved.     

Evolutionary relationships, interisland biogeography, and molecular evolution in the Hawaiian violets (Viola: Violaceae)

The endemic Hawaiian flora offers remarkable opportunities to study the patterns of plant morphological and molecular evolution. The Hawaiian violets are a monophyletic lineage of nine taxa distributed across six main islands of the Hawaiian archipelago. To describe the evolutionary relationships, biogeography, and molecular evolution rates of the Hawaiian violets, we conducted a phylogenetic study using nuclear rDNA internal transcribed spacer sequences from specimens of each species. Parsimony, maximum likelihood (ML), and Bayesian inference reconstructions of island colonization and radiation strongly suggest that the Hawaiian violets first colonized the Maui Nui Complex, quickly radiated to Kaua'i and O'ahu, and recently dispersed to Hawai'i. The lineage consists of "wet" and "dry" clades restricted to distinct precipitation regimes. The ML and Bayesian inference reconstructions of shifts in habitat, habit, and leaf shape indicate that ecologically analogous taxa have undergone parallel evolution in leaf morphology and habit. This parallel evolution correlates with shifts to specialized habitats. Relative rate tests showed that woody and herbaceous sister species possess equal molecular evolution rates. The incongruity of molecular evolution rates in taxa on younger islands suggests that these rates may not be determined by growth form (or lifespan) alone, but may be influenced by complex dispersal events.