Evolution of a cichlid fish in a Lake Malawi satellite lake

Allopatric divergence in peripheral habitats may lead to rapid evolution of populations with novel phenotypes. In this study we provide the first evidence that isolation in peripheral habitats may have played a critical role in generation of Lake Malawi's cichlid fish diversity. We show that Lake Chilingali, a satellite lake 11.5 km from the shore of Lake Malawi, contains a breeding population of Rhamphochromis, a predatory genus previously thought to be restricted to Lake Malawi and permanently connected water bodies. The Lake Chilingali population is the smallest known Rhamphochromis, has a unique male nuptial colour pattern and has significant differentiation in mitochondrial DNA from Lake Malawi species. In laboratory mate choice trials with a candidate sister population from Lake Malawi, females showed a strong tendency to mate assortatively indicating that they are incipient biological species. These data support the hypothesis that isolation and reconnection of peripheral habitats due to lake level changes have contributed to the generation of cichlid diversity within African lakes. Such cycles of habitat isolation and reconnection may also have been important in evolutionary diversification of numerous other abundant and wide-ranging aquatic organisms, such as marine fishes and invertebrates.     

Resistance of an invasive gastropod to an indigenous trematode parasite in Lake Malawi

Successful establishment and spread of biological invaders may be promoted by the absence of population-regulating enemies such as pathogens, parasites or predators. This may come about when introduced taxa are missing enemies from their native habitats, or through immunity to enemies within invaded habitats. Here we provide field evidence that trematode parasites are absent in a highly invasive morph of the gastropod Melanoides tuberculata in Lake Malawi, and that the invasive morph is resistant to indigenous trematodes that castrate and induce gigantism in native M. tuberculata. Since helminth infections can strongly influence host population abundances in other host-parasite systems, this enemy release may have provided an advantage to the invasive morph in terms of reproductive capacity and survivorship.     

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.     

Axes of differentiation in the bower-building cichlids of Lake Malawi

The 500-1000 cichlid species endemic to Lake Malawi constitute one of the most rapid and extensive radiations of vertebrates known. There is a growing debate over the role natural and sexual selection have played in creating this remarkable assemblage of species. Phylogenetic analysis of the Lake Malawi species flock has been confounded by the lack of appropriate morphological characters and an exceptional rate of speciation, which has allowed ancestral molecular polymorphisms to persist within species. To overcome this problem we used amplified fragment length polymorphism (AFLP) to reconstruct the evolution of species within three genera of Lake Malawi sand-dwelling cichlids that construct elaborate male display platforms, or bowers. Sister taxa with distinct bower morphologies, and that exist in discrete leks separated by only 1-2 m of depth, are divergent in both sexually selected and ecological traits. Our phylogeny suggests that the forces of sexual and ecological selection are intertwined during the speciation of this group and that specific bower characteristics and trophic morphologies have evolved repeatedly. These results suggest that trophic morphology and bower form may be inappropriate characters for delineating taxonomic lineages. Specifically the morphological characters used to describe the genera Lethrinops and Tramitichromis do not define monophyletic clades. Using a combination of behavioural and genetic characters, we were able to identify several cryptic cichlid species on a single beach, which suggests that sand dweller species richness has been severely underestimated.     

Age of cichlids: new dates for ancient lake fish radiations

Timing divergence events allow us to infer the conditions under which biodiversity has evolved and gain important insights into the mechanisms driving evolution. Cichlid fishes are a model system for studying speciation and adaptive radiation, yet, we have lacked reliable timescales for their evolution. Phylogenetic reconstructions are consistent with cichlid origins prior to Gondwanan landmass fragmentation 121-165 MYA, considerably earlier than the first known fossil cichlids (Eocene). We examined the timing of cichlid evolution using a relaxed molecular clock calibrated with geological estimates for the ages of 1) Gondwanan fragmentation and 2) cichlid fossils. Timescales of cichlid evolution derived from fossil-dated phylogenies of other bony fishes most closely matched those suggested by Gondwanan breakup calibrations, suggesting the Eocene origins and marine dispersal implied by the cichlid fossil record may be due to its incompleteness. Using Gondwanan calibrations, we found accumulation of genetic diversity within the radiating lineages of the African Lakes Malawi, Victoria and Barombi Mbo, and Palaeolake Makgadikgadi began around or after the time of lake basin formation. These calibrations also suggest Lake Tanganyika was colonized independently by the major radiating cichlid tribes that then began to accumulate genetic diversity thereafter. These results contrast with the widely accepted theory that diversification into major lineages took place within the Tanganyika basin. Together, this evidence suggests that ancient lake habitats have played a key role in generating and maintaining diversity within radiating lineages and also that lakes may have captured preexisting cichlid diversity from multiple sources from which adaptive radiations have evolved.     

Cryptic speciation in two widespread subterranean amphipod genera reflects historical drainage patterns in an ancient landscape

The landscape of the Pilbara region of Western Australia has been relatively unchanged for 100 million years. The ancient river systems of this region might be expected to be sources of isolation and divergence for aquatic species. Hence, the occurrence of widespread groundwater taxa in this landscape offers the opportunity to examine associations between genetic diversity and drainage patterns. Pilbarus and Chydaekata are two widespread genera of subterranean amphipods endemic to the Pilbara, each occupying multiple tributaries. We used molecular data to examine the roles of drainage patterns in structuring genetic diversity. Gene flow within a tributary may be facilitated by the occasional occurrence of these amphipods in springs, which results in their downstream dispersal during episodic flooding. However, tributary boundaries may form hydrological barriers to gene flow, resulting in localised isolation of populations and divergence. Samples of both genera, collected throughout three river basins, were examined for sequence divergence in the cytochrome c oxidase I mitochondrial gene. There was no evidence of contemporary gene flow among populations of either genus, and each tributary contained highly divergent lineages, which were not associated with similar morphological differentiation. This suggests cryptic speciation has occurred, and similar phylogenetic signals in both taxa imply similar evolutionary histories. Surface populations may have been driven into subterranean refugia by the cessation of flow in the rivers, associated with Tertiary climate change, while morphological evolution may have been constrained by stabilising selection. The lack of congruence between molecular diversity and morphology raises important practical issues for conservation.     

Ancient hybridization and phenotypic novelty within Lake Malawi's cichlid fish radiation

Does hybridization play a broad innovative role in evolution? Many studies have shown hybrid origins of individual species, particularly in major adaptive radiations, but this may be a consequence, rather than a cause, of the existence of many closely related species. Cases of hybridization in the early stages of major adaptive radiations are comparatively rare. Here, we report phylogenetic evidence for ancient introgression between distinct lineages of the species-rich Lake Malawi haplochromine cichlid fishes. Mitochondrial DNA (mtDNA) sequences indicated surprisingly close relationships between the shallow-water rocky habitat "Mbuna" species and a group of dark-adapted "Deep-Benthic" species specialized for feeding in low-light conditions (dawn/dusk, under overhangs, and deep water). By contrast, analyses of nuclear amplified fragment length polymorphism data demonstrated that these Deep-Benthic cichlids were more closely related to shallow water "Shallow-Benthic" soft-sediment feeders, a group that shares similar head and body morphology. A coalescent-based computer simulation indicated that the mtDNA similarity of rocky habitat Mbuna species and dark-adapted Deep-Benthic species was due to hybridization rather than incomplete lineage sorting. Comparisons of morphology indicated that some Deep-Benthic species possessed novel morphology not present in other Lake Malawi species groups. Thus, these analyses support the hypothesis that ancient hybridization occurred within the Lake Malawi cichlid radiation, that the event occurred before the radiation of a species group adapted to low-light benthic habitats, and that this group went on to dominate the deep-water regions of Lake Malawi. The results of this study contribute to a growing literature consistent with a creative role of hybridization in the evolution of species diversity and adaptive radiations.     

Phylogenetic tree of vascular plants reveals the origins of aquatic angiosperms

Although aquatic plants are discussed as a unified biological group, they are phylogenetically well dispersed across the angiosperms. In this study, we annotated the aquatic taxa on the tree of vascular plants, and extracted the topology of these aquatic lineages to construct the tree of aquatic angiosperms. We also reconstructed the ancestral areas of aquatic families. We found that aquatic angiosperms could be divided into two different categories: the four aquatic orders and the aquatic taxa in terrestrial orders. Aquatic lineages evolved early in the radiation of angiosperms, both in the orders Nymphaeales and Ceratophyllales and among basal monocots (Acorales and Alismatales). These aquatic orders do not have any extant terrestrial relatives. They originated from aquatic habitats during the Early Cretaceous. Asia would have been one of the centers for early diversification of aquatic angiosperms. The aquatic families within terrestrial orders may originate from other areas besides Asia, such as America or Australia. The lineages leading to extant angiosperms diversified early in underexploited freshwater habitats. The four extant aquatic orders were relicts of an early radiation of angiosperm in aquatic environments. Their extinct ancestors might be aquatic early angiosperms.     

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.     

The effect of habitat on modern shark diversification

Sharks occupy marine habitats ranging from shallow, inshore environments to pelagic, and deepwaters, and thus provide a model system for testing how gross habitat differences have shaped vertebrate macroevolution. Palaeontological studies have shown that onshore lineages diversify more quickly than offshore taxa. Among onshore habitats, coral reef‐association has been shown to increase speciation rates in several groups of fishes and invertebrates. In this study, we investigated whether speciation rates are habitat dependent by generating the first comprehensive molecular timescale for shark divergence. Using phylogenetic comparative methods, we rejected the hypothesis that shelf (i.e. onshore) lineages have higher speciation rates compared to those occupying deepwater and oceanic (i.e. offshore) habitats. Our results, however, support the hypothesis of increased speciation rates in coral reef‐associated lineages within the Carcharhinidae. Our new timetree suggests that the two major shark lineages leading to the extant shark diversity began diversifying mostly after the end‐Permian mass extinction: the squalimorphs into deepwater and the galeomorphs into shelf habitats. We suggest that the breakdown of the onshore–offshore speciation rate pattern in sharks is mediated by success in deepwater environments through ecological partitioning, and in some cases, the evolution of morphological novelty.     

Marine invasions by non-sea snakes, with thoughts on terrestrial-aquatic-marine transitions

Few species of snakes show extensive adaptations to aquatic environments and even fewer exploit the oceans. A survey of morphology, lifestyles, and habitats of 2552 alethenophidian snakes revealed 362 (14%) that use aquatic environments, are semi-aquatic, or aquatic; about 70 (2.7%) of these are sea snakes (Hydrophiinae and Laticaudinae). The ancient and aquatic family Acrochordidae contains three extant species, all of which have populations inhabiting brackish or marine environments, as well as freshwater. The Homalopsidae have the most ecologically diverse representatives in coastal habitats. Other families containing species exploiting saline waters with populations in freshwater environments include: the Dipsadidae of the western hemisphere, the cosmopolitan Natricidae, the African Grayinae, and probably a few Colubridae. Species with aquatic and semi-aquatic lifestyles are compared with more terrestrial (fossorial, cryptozoic, and arboreal) species for morphological traits and life histories that are convergent with those found in sea snakes; this may provide clues to the evolution of marine snakes and increase our understanding of snake diversity.     

Endemic ranid (Amphibia: Anura) genera in southern mountain ranges of the Indian subcontinent represent ancient frog lineages: evidence from molecular data

The geological history of the Indian subcontinent is marked by successive episodes of extensive isolation, which have provided ideal settings for the development of a unique floral and faunal diversity. By molecular phylogenetic analysis of a large set of ranid frog taxa from the Oriental realm, we show that four genera, now restricted to torrential habitats in the Western Ghats of India and the central highlands of Sri Lanka, represent remnants of ancient divergences. None of three other biodiversity hotspots in the Oriental mainland were found to harbour an equivalent level of long-term evolutionary history in this frog group. By unceasingly providing favourable humid conditions, the subcontinent's southern mountain ranges have served as refugia for old lineages, and hence constitute a unique reservoir of ancient ranid endemism.     

Modelling of essential fish habitat based on remote sensing,spatial analysis and GIS

Lake Tanganyika is not the most species-rich of the Great East African Lakes, but comprises the greatest diversity of cichlid fishes in terms of morphology, ecology, and breeding styles. The lake contains a polyphyletic assemblage of cichlid lineages, which evolved from several ancient species that colonized the emerging lake some 9–12 million years ago. Based on morphological characteristics, the Tanganyikan cichlids have been classified into 12, or, more recently, 16 tribes, which are largely supported by molecular data. The radiations of East African cichlids are believed to be driven by complex interactions between extrinsic factors, such as climatic changes and geological processes, and intrinsic biological characteristics of the involved organisms. Diversification within different lineages occurred simultaneously in response to drastic habitat changes such as the establishment of lacustrine deep-water conditions 5–6 MYA and subsequent major lake-level fluctuations. This seems particularly true for the mouthbrooding lineages whereas the substrate breeders underwent a more gradual process of diversification. This review presents an account of the taxonomy and phylogeny of the Lake Tanganyika cichlid species assemblage, its relationship to the African cichlid fauna, key factors leading to the astonishing diversity and discusses recently proposed alternative age estimates for the Lake Tanganyika cichlid species assemblage.     

Mitochondrial genome primers for Lake Malawi cichlids

Resolving the evolutionary history of rapidly diversifying lineages like the Lake Malawi Cichlid Flock demands powerful phylogenetic tools. Although this clade of over 500 species of fish likely diversified in less than two million years, the availability of extensive sequence data sets, such as complete mitochondrial genomes, could help resolve evolutionary patterns in this group. Using a large number of newly developed primers, we generated whole mitochondrial genome sequences for 14 Lake Malawi cichlids. We compared sequence divergence across protein‐coding regions of the mitochondrial genome and also compared divergence in the mitochondrial loci to divergence at two nuclear protein‐coding loci, Mitfb and Dlx2. Despite the widespread sharing of haplotypes of identical sequences at individual loci, the combined use of all protein‐coding mitochondrial loci provided a bifurcating phylogenetic hypothesis for the exemplars of major lineages within the Lake Malawi cichlid radiation. The primers presented here could have substantial utility for evolutionary analyses of mitochondrial evolution and hybridization within this diverse clade.     

Aggression in closely related Malawi cichlids varies inversely with habitat complexity

Within the past 2 million years, the cichlids of Lake Malawi have diversified into well over 500 species resulting in one of the worlds largest lacustrine fish radiations. As a result, many of the habitats within the lake support a high diversity of species. In these highly species rich communities, male cichlids must acquire and defend a territory to successfully reproduce. Within the rock-dwelling cichlids of Lake Malawi (mbuna), this has resulted in the formation of polyspecific leks on the heterogeneous rocky benthos. Aggression is fairly common in these leks and has been tied not only to individual reproduction but to the larger phenomenon of community assembly and the maintenance of biological diversity. In this study, I examined the patterns of aggressive acts of four species within the mbuna genus Maylandia at two locations in the southern Lake Malawi. The number of aggressive acts of two sympatric species was examined at each location. At each site, one species defends territories over bedrock and the other over cobble. The number of aggressive acts across the four species was compared. The influence of habitat type on male aggression was examined and the targets of male aggression were identified to evaluate several hypotheses concerning the evolution of male aggression. The results show that aggression quantitatively varied among species, was largely directed towards heterospecifics, and was strongly influenced by habitat type. The aggressive behavior of one sympatric species pair, Maylandia benetos and Maylandia zebra, was observed under controlled laboratory conditions. Laboratory results support field observations: the bedrock associated species performed more aggressive acts and aggressive acts were directed equally at con- and heterospecifics. The results of this study suggest that habitat complexity plays a larger role in shaping aggressive behavior than other suggested factors such as competition for resources.     

Fate of glacier surface snow-originating bacteria in the glacier-fed hydrologic continuums

Glaciers represent important biomes of Earth and are recognized as key species pools for downstream aquatic environments. Worldwide, rapidly receding glaciers are driving shifts in hydrology, species distributions and threatening microbial diversity in glacier-fed aquatic ecosystems. However, the impact of glacier surface snow-originating taxa on the microbial diversity in downstream aquatic environments has been little explored. To elucidate the contribution of glacier surface snow-originating taxa to bacterial diversity in downstream aquatic environments, we collected samples from glacier surface snows, downstream streams and lakes along three glacier-fed hydrologic continuums on the Tibetan Plateau. Our results showed that glacier stream acts as recipients and vectors of bacteria originating from the glacier environments. The contributions of glacier surface snow-originating taxa to downstream bacterial communities decrease from the streams to lakes, which was consistently observed in three geographically separated glacier-fed ecosystems. Our results also revealed that some rare snow-originating bacteria can thrive along the hydrologic continuums and become dominant in downstream habitats. Finally, our results indicated that the dispersal patterns of bacterial communities are largely determined by mass effects and increasingly subjected to local sorting of species along the glacier-fed hydrologic continuums. Collectively, this study provides insights into the fate of bacterial assemblages in glacier surface snow following snow melt and how bacterial communities in aquatic environments are affected by the influx of glacier snow-originating bacteria.     

Global diversity of craneflies (Insecta,Diptera: Tipulidea or Tipulidae <Emphasis Type="Italic">sensu lato</Emphasis>) in freshwater

The Tipulidae s.l.—craneflies—are one of the largest groups of the Diptera containing over 15,270 valid species and subspecies. The immatures of the majority of species live in aquatic or semiaquatic habitats. Some aquatic species live entirely submerged and lack functional spiracles, others come to the surface to take oxygen by using spiracles positioned at the end of the abdomen. Semiaquatic species occur in a wide range of habitats. The semiterrestrial and terrestrial larvae live in environments that are moist or at least humous. All adult craneflies are terrestrial. Conflicting hypotheses on the phylogenetic position of the Tipuloidea within the Diptera continue to exist: some authors consider them to represent one of the oldest lineages of the Diptera, others suppose a close relationship to the Brachycera, the true flies. Current systematic knowledge of the Tipuloidea indicates that the Palaearctic region contains the highest number of genus-group taxa, while the Neotropical region has the highest number of species and subspecies. The Afrotropical and Australasian regions are relatively poor respectively in genera and subgenera and in species and subspecies. The oldest fossils that represent the Tipuloidea date back to the Lower Triassic at about 240 million years. Present-day general distribution patterns of many higher taxa of Tipuloidea probably have a Pangean or Gondwanan origin. Electronic supplementary material The online version of this article (doi:) contains supplementary material, which is available to authorized users. Guest editors: E. V. Balian, C. Lévêque, H. Segers & K. Martens Freshwater Animal Diversity Assessment.     

Lake Malawi cichlid evolution along a benthic/limnetic axis

Divergence along a benthic to limnetic habitat axis is ubiquitous in aquatic systems. However, this type of habitat divergence has largely been examined in low diversity, high latitude lake systems. In this study, we examined the importance of benthic and limnetic divergence within the incredibly species‐rich radiation of Lake Malawi cichlid fishes. Using novel phylogenetic reconstructions, we provided a series of hypotheses regarding the evolutionary relationships among 24 benthic and limnetic species that suggests divergence along this axis has occurred multiple times within Lake Malawi cichlids. Because pectoral fin morphology is often associated with divergence along this habitat axis in other fish groups, we investigated divergence in pectoral fin muscles in these benthic and limnetic cichlid species. We showed that the eight pectoral fin muscles and fin area generally tended to evolve in a tightly correlated manner in the Lake Malawi cichlids. Additionally, we found that larger pectoral fin muscles are strongly associated with the independent evolution of the benthic feeding habit across this group of fish. Evolutionary specialization along a benthic/limnetic axis has occurred multiple times within this tropical lake radiation and has produced repeated convergent matching between exploitation of water column habitats and locomotory morphology.     

Major issues in the origins of ray‐finned fish (Actinopterygii) biodiversity

Ray‐finned fishes (Actinopterygii) dominate modern aquatic ecosystems and are represented by over 32000 extant species. The vast majority of living actinopterygians are teleosts; their success is often attributed to a genome duplication event or morphological novelties. The remainder are ‘living fossils’ belonging to a few depauperate lineages with long‐retained ecomorphologies: Polypteriformes (bichirs), Holostei (bowfin and gar) and Chondrostei (paddlefish and sturgeon). Despite over a century of systematic work, the circumstances surrounding the origins of these clades, as well as their basic interrelationships and diagnoses, have been largely mired in uncertainty. Here, I review the systematics and characteristics of these major ray‐finned fish clades, and the early fossil record of Actinopterygii, in order to gauge the sources of doubt. Recent relaxed molecular clock studies have pushed the origins of actinopterygian crown clades to the mid‐late Palaeozoic [Silurian–Carboniferous; 420 to 298 million years ago (Ma)], despite a diagnostic body fossil record extending only to the later Mesozoic (251 to 66 Ma). This disjunct, recently termed the ‘Teleost Gap’ (although it affects all crown lineages), is based partly on calibrations from potential Palaeozoic stem‐taxa and thus has been attributed to poor fossil sampling. Actinopterygian fossils of appropriate ages are usually abundant and well preserved, yet long‐term neglect of this record in both taxonomic and systematic studies has exacerbated the gaps and obscured potential synapomorphies. At the moment, it is possible that later Palaeozoic‐age teleost, holostean, chondrostean and/or polypteriform crown taxa sit unrecognized in museum drawers. However, it is equally likely that the ‘Teleost Gap’ is an artifact of incorrect attributions to extant lineages, overwriting both a post‐Palaeozoic crown actinopterygian radiation and the ecomorphological diversity of stem‐taxa.     

Why are there so few fish in the sea?

The most dramatic gradient in global biodiversity is between marine and terrestrial environments. Terrestrial environments contain approximately 75-85% of all estimated species, but occupy only 30 per cent of the Earth's surface (and only approx. 1-10% by volume), whereas marine environments occupy a larger area and volume, but have a smaller fraction of Earth's estimated diversity. Many hypotheses have been proposed to explain this disparity, but there have been few large-scale quantitative tests. Here, we analyse patterns of diversity in actinopterygian (ray-finned) fishes, the most species-rich clade of marine vertebrates, containing 96 per cent of fish species. Despite the much greater area and productivity of marine environments, actinopterygian richness is similar in freshwater and marine habitats (15 150 versus 14 740 species). Net diversification rates (speciation-extinction) are similar in predominantly freshwater and saltwater clades. Both habitats are dominated by two hyperdiverse but relatively recent clades (Ostariophysi and Percomorpha). Remarkably, trait reconstructions (for both living and fossil taxa) suggest that all extant marine actinopterygians were derived from a freshwater ancestor, indicating a role for ancient extinction in explaining low marine richness. Finally, by analysing an entirely aquatic group, we are able to better sort among potential hypotheses for explaining the paradoxically low diversity of marine environments.