Out of Tanganyika: Genesis, explosive speciation, key-innovations and phylogeography of the haplochromine cichlid fishes

Background  

The adaptive radiations of cichlid fishes in East Africa are well known for their spectacular diversity and their astonishingly fast rates of speciation. About 80% of all 2,500 cichlid species in East Africa, and virtually all cichlid species from Lakes Victoria (~500 species) and Malawi (~1,000 species) are haplochromines. Here, we present the most extensive phylogenetic and phylogeographic analysis so far that includes about 100 species and is based on about 2,000 bp of the mitochondrial DNA.     

Tempo and mode of diversification of lake Tanganyika cichlid fishes

Background

Understanding the causes of disparities in species diversity across taxonomic groups and regions is a fundamental aim in evolutionary biology. Addressing these questions is difficult because of the need for densely sampled phylogenies and suitable empirical systems.

Methodology/Principal Findings

Here we investigate the cichlid fish radiation of Lake Tanganyika and show that per lineage diversification rates have been more than six times slower than in the species flocks of Lakes Victoria and Malawi. The result holds even at peak periods of diversification in Lake Tanganyika, ruling out the age of the lake as an explanation for slow average rates, and is robust to uncertainties over the calibration of cichlid radiations in geological time. Moreover, Lake Tanganyika lineages, irrespective of different biological characteristics (e.g. sexually dichromatic versus sexually monochromatic clades), have diversified at similar rates, falling within typical estimates across a range of plant and animal clades. For example, the mostly sexually dichromatic haplochromines, which have speciated explosively in Lakes Victoria and Malawi, have displayed modest rates in Lake Tanganyika (where they are called Tropheini).

Conclusion/Significance

Our results show that either the Lake Tanganyika environment is less conducive for cichlid speciation or the remarkable diversifying abilities of the haplochromines were inhibited by the prior occupancy of older radiations. Although the results indicate a dominant role for the environment in shaping cichlid diversification, differences in the timing of diversification among the Tanganyikan tribes indicate that biological differences were still important for the dynamics of species build-up in the lake. While we cannot resolve the timing of the radiation relative to the origin of the lake, because of the lack of robust geological date calibrations for cichlids, our results are consistent with a scenario that the different clades reflect independent adaptive radiations into different broad niches in the lake.     

Mitochondrial phylogeny and phylogeography of East African squeaker catfishes (Siluriformes: Synodontis)

Background  

Squeaker catfishes (Pisces, Mochokidae, Synodontis) are widely distributed throughout Africa and inhabit a biogeographic range similar to that of the exceptionally diverse cichlid fishes, including the three East African Great Lakes and their surrounding rivers. Since squeaker catfishes also prefer the same types of habitats as many of the cichlid species, we hypothesized that the East African Synodontis species provide an excellent model group for comparative evolutionary and phylogeographic analyses.     

Nuclear markers reveal unexpected genetic variation and a Congolese-Nilotic origin of the Lake Victoria cichlid species flock

Phylogenetic analyses based on mitochondrial (mt) DNA have indicated that the cichlid species flock of the Lake Victoria region is derived from a single ancestral species found in East African rivers, closely related to the ancestor of the Lake Malawi cichlid species flock. The Lake Victoria flock contains ten times less mtDNA variation than the Lake Malawi radiation, consistent with current estimates of the ages of the lakes. We present results of a phylogenetic investigation using nuclear (amplified fragment length polymorphism) markers and a wider coverage of riverine haplochromines. We demonstrate that the Lake Victoria-Edward flock is derived from the morphologically and ecologically diverse cichlid genus Thoracochromis from the Congo and Nile, rather than from the phenotypically conservative East African Astatotilapia. This implies that the ability to express much of the morphological diversity found in the species flock may by far pre-date the origin of the flock. Our data indicate that the nuclear diversity of the Lake Victoria-Edward species flock is similar to that of the Lake Malawi flock, indicating that the genetic diversity is considerably older than the 15 000 years that have passed since the lake began to refill. Most of this variation is manifested in trans-species polymorphisms, indicating very recent cladogenesis from a genetically very diverse founder stock. Our data do not confirm strict monophyly of either of the species flocks, but raise the possibility that these flocks have arisen from hybrid swarms.     

Phylogeny of the Lake Tanganyika cichlid species flock and its relationship to the Central and East African haplochromine cichlid fish faunas

Lake Tanganyika, the oldest of the East African Great Lakes, harbors the ecologically, morphologically, and behaviorally most complex of all assemblages of cichlid fishes, consisting of about 200 described species. The evolutionary old age of the cichlid assemblage, its extreme degree of morphological differentiation, the lack of species with intermediate morphologies, and the rapidity of lineage formation have made evolutionary reconstruction difficult. The number and origin of seeding lineages, particularly the possible contribution of riverine haplochromine cichlids to endemic lacustrine lineages, remains unclear. Our phylogenetic analyses, based on mitochondrial DNA sequences of three gene segments of 49 species (25% of all described species, up to 2,400 bp each), yield robust phylogenies that provide new insights into the Lake Tanganyika adaptive radiation as well as into the origin of the Central- and East-African haplochromine faunas. Our data suggest that eight ancient African lineages may have seeded the Tanganyikan cichlid radiation. One of these seeding lineages, probably comprising substrate spawning Lamprologus-like species, diversified into six lineages that evolved mouthbrooding during the initial stage of the radiation. All analyzed haplochromines from surrounding rivers and lakes seem to have evolved within the radiating Tanganyikan lineages. Thus, our findings contradict the current hypothesis that ancestral riverine haplochromines colonized Lake Tanganyika to give rise to at least part of its spectacular endemic cichlid species assemblage. Instead, the early phases of the Tanganyikan radiation affected Central and East African rivers and lakes. The haplochromines may have evolved in the Tanganyikan basin before the lake became a hydrologically and ecologically closed system and then secondarily colonized surrounding rivers. Apparently, therefore, the current diversity of Central and East African haplochromines represents a relatively young and polyphyletic fauna that evolved from or in parallel to lineages now endemic to Lake Tanganyika.     

Mastacembelid eels support Lake Tanganyika as an evolutionary hotspot of diversification

Background  

Lake Tanganyika (LT) is the oldest of the African Rift Lakes and is one of the richest freshwater ecosystems on Earth, with high levels of faunal diversity and endemism. The endemic species flocks that occur in this lake, such as cichlid fishes, gastropods, catfish and crabs, provide unique comparative systems for the study of patterns and processes of speciation. Mastacembelid eels (Teleostei: Mastacembelidae) are a predominately riverine family of freshwater fish, occurring across Africa and Asia, but which also form a small species flock in LT.     

Phylogeography and speciation in the <Emphasis Type="Italic">Pseudocrenilabrus philander</Emphasis> species complex in Zambian Rivers

Haplochromine cichlids form the most species-rich lineage of cichlid fishes that both colonized almost all river systems in Africa and radiated to species flocks in several East African lakes. The enormous diversity of lakes is contrasted by a relatively poor albeit biogeographically clearly structured species diversity in rivers. The present study analyzed the genetic structure and phylogeographic history of species and populations of the genus Pseudocrenilabrus in Zambian rivers that span two major African drainage systems, the Congo- and the Zambezi-system. The mtDNA phylogeny identifies four major lineages, three of which occur in the Congo-system and one in the Zambezi system. Two of the Congo-clades (Lake Mweru and Lunzua River) comprise distinct albeit yet undescribed species, while the fish of the third Congo-drainage clade (Chambeshi River and Bangweulu swamps), together with the fish of the Zambezi clade (Zambezi and Kafue River) are assigned to Pseudocrenilabrus philander. Concerning the intraspecific genetic diversity observed in the sampled rivers, most populations are highly uniform in comparison to lacustrine haplochromines, suggesting severe founder effects and/or bottlenecking during their history. Two bursts of diversification are reflected in the structure of the linearized tree. The first locates at about 3.9% mean sequence divergence and points to an almost simultaneous colonization of the sampled river systems. Subsequent regional diversification (with about 1% mean sequence divergence) occurred contemporaneously within the Kafue River and the Zambezi River. The clear-cut genetic biogeographic structure points to the dominance of geographic speciation in this lineage of riverine cichlid fishes, contrasting the importance of in situ diversification observed in lake cichlids.     

The root of the East African cichlid radiations

Background  

For decades cichlid fishes (Perciformes: Cichlidae) of the East African cichlid radiations (Teleostei: Cichlidae) have served as natural experimental subjects for the study of speciation processes and the search for potential speciation key factors. Despite numerous phylogenetic studies dealing with their intragroup relationships, surprisingly little is known about the phylogenetic placement and time of origin of this enigmatic group. We used multilocus DNA-sequence data from five nuclear and four mitochondrial genes and refined divergence time estimates to fill this knowledge gap.     

Pliocene isolation of a north‐west Saharan cichlid fish

The evolutionary origin of the only north‐west Saharan haplochromine cichlid, Astatotilapia desfontainii, was explored using mitochondrial DNA sequences. Phylogenetic analyses revealed that this species belonged to the main East African–Nilotic haplochromine clade, but was a distinct lineage that diverged from modern haplochromines in the Pliocene. The results suggest that A. desfontainii is a relict haplochromine lineage that has endured major climate fluctuations in North Africa.     

Explosive speciation in cichlid fishes of the African Great Lakes: a dynamic model of adaptive radiation

In the African cichlid species flocks several corresponding ecotypes and species communities have evolved independently in each of the lakes. These flocks can be viewed as reiterations of a process, induced by the same type of external event (the formation of a lake) and seeded by the same group of organisms, equipped with the same innovative potential. The East African lakes differ in their ages, so that different stages of adaptive radiation of a single group of fishes can be studied simultaneously. This review combines findings on various African cichlid species flocks and derives a generalized model of cichlid adaptive radiation. The model constitutes four stages, defined by the most influential habitat characteristics and interactions among members of the species community at each phase. It is an attempt to provide an explicit hypothesis for a dynamic evolutionary process, as a basis to future studies.     

Age and spread of the haplochromine cichlid fishes in Africa

The Haplochromini are by far the most species-rich cichlid fish tribe that originated along with the so-called primary radiation of the Lake Tanganyika cichlid species flock, i.e. at the same time during which the majority of the endemic Lake Tanganyika cichlid tribes emerged. Unlike the other tribes, the haplochromines are not restricted to Lake Tanganyika but distributed throughout Africa, except for the northwestern part of the continent. Haplochromine cichlids seeded the adaptive radiation of cichlid fishes in Lakes Malawi, Kivu, Victoria, Turkana, as well as in the now extinct paleo-Lake Makgadikgadi. Here we present a comprehensive phylogenetic and phylogeographic analysis of haplochromine cichlids that is based upon DNA sequences of two mitochondrial gene segments of riverine taxa covering all major African biogeographic regions where haplochromines are found. Our analysis revealed that six lineages of haplochromines originated within a short period of time, about 5.3-4.4 MYA. These haplochromine lineages show a highly complex phylogeographic pattern, probably severely influenced by climate- and/or geology-induced changes of the environment, with river capture events most likely playing an important role for species dispersal.     

Genetic isolation and morphological divergence mediated by high-energy rapids in two cichlid genera from the lower Congo rapids

Background  

It is hypothesized that one of the mechanisms promoting diversification in cichlid fishes in the African Great Lakes has been the well-documented pattern of philopatry along shoreline habitats leading to high levels of genetic isolation among populations. However lake habitats are not the only centers of cichlid biodiversity - certain African rivers also contain large numbers of narrowly endemic species. Patterns of isolation and divergence in these systems have tended to be overlooked and are not well understood.     

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.     

Phylogenetic analysis of cichlid fishes using nuclear DNA markers

The recent explosive adaptive radiation of cichlids in the great lakes of Africa has attracted the attention of both morphologists and molecular biologists. To decipher the phylogenetic relationships among the various taxa within the family Cichlidae is a prerequisite for answering some fundamental questions about the nature of the speciation process. In the present study, we used the random amplification of polymorphic DNA (RAPD) technique to obtain sequence differences between selected cichlid species. We then designed specific primers based on these sequences and used them to amplify template DNA from a large number of species by the polymerase chain reaction (PCR). We sequenced the amplified products and searched the sequences for indels and shared substitutions. We identified a number of such characters at three loci-- DXTU1, DXTU2, and DXTU3--and used them for phylogenetic and cladistic analysis of the relationships among the various cichlid groups. Our studies assign an outgroup position to Neotropical cichlids in relation to African cichlids, provide evidence for a sister-group relationship of tilapiines to the haplochromines, group Cyphotilapia frontosa with the lamprologines of Lake Tanganyika, place Astatoreochromis alluaudi to an outgroup position with respect to other haplochromines of Lakes Victoria and Malawi, and provide additional support for the monophyly of the remaining Lake Victoria haplochromines and the Lake Malawi haplochromines. The described approach holds great promise for further resolution of cichlid phylogeny.      

Rapid speciation in a newly opened postglacial marine environment, the Baltic Sea

Background  

Theory predicts that speciation can be quite rapid. Previous examples comprise a wide range of organisms such as sockeye salmon, polyploid hybrid plants, fruit flies and cichlid fishes. However, few studies have shown natural examples of rapid evolution giving rise to new species in marine environments.     

Phylogenetic Relationships Among East African Haplochromine Fish as Revealed by Short Interspersed Elements (SINEs)

Genomic DNA libraries were prepared from two endemic species of Lake Victoria haplochromine (cichlid) fish and used to isolate and characterize a set of short interspersed elements (SINEs). The distribution and sequences of the SINEs were used to infer phylogenetic relationships among East African haplochromines. The SINE-based classification divides the fish into four groups, which, in order of their divergence from a stem lineage, are the endemic Lake Tanganyika flock (group 1); fish of the nonendemic, monotypic, widely distributed genus Astatoreochromis (group 2); the endemic Lake Malawi flock (group 3); and group 4, which contains fish from widely dispersed East African localities including Lakes Victoria, Edward, George, Albert, and Rukwa, as well as many rivers. The group 4 haplochromines are characterized by a subset of polymorphic SINEs, each of which is present in some individuals and absent in others of the same population at a given locality, the same morphologically defined species, and the same mtDNA-defined haplogroup. SINE-defined group 4 contains six of the seven previously described mtDNA haplogroups. One of the polymorphic SINEs appears to be fixed in the endemic Lake Victoria flock; four others display the presence-or-absence polymorphism within the species of this flock. These findings have implications for the origin of Lake Victoria cichlids and for their founding population sizes.     

Effects of Nile perch (Lates niloticus) introduction into Lake Victoria,East Africa,on the diet of Pied Kingfishers (Ceryle rudis)

In recent years the ichthyofauna of Lake Victoria, the world's largest tropical lake, has gone through dramatic changes. The population of Nile perch, a large predator which has been introduced into the lake by man, increased explosively at the expense of many haplochromine cichlid species. At the same time, numbers of a small cyprinid (dagaa) rose sharply.

Previously Pied Kingfishers on Lake Victoria fed mainly on haplochromines. Only the youngest nestlings depended on dagaa as primary food. The current diet of adult birds clearly reflects the changes which have occurred in the fish community. Pellet analysis reveals a shift towards a diet composed of almost 100% dagaa.

The change in prey species composition has increased the number of fish a kingfisher needs to catch daily in order to meet its energetic demands, because:

1. (1)

   the mean size of haplochromines is larger than that of dagaa;

2. (2)

   (2) the mean size of dagaa has decreased since the increase in Nile perch;

3. (3)

   (3) the weight of dagaa is lower than that of haplochromines of equal size;

4. (4)

   (4) mainly juvenile dagaa and adults in poor condition are accessible to kingfishers.

     

Occurrence of haemolytic Mannheimia spp. in apparently healthy sheep in Norway

Background  

The occurrence of Mannheimia species in healthy sheep has only been investigated to a very limited extend since the genus and its five named species were established. The aim of the present study was to evaluate the occurrence of haemolytic Mannheimia species in apparently healthy sheep originating from four sheep flocks in South-Western Norway.     

Linkage Relationships and Haplotype Variation of the Major Histocompatibility Complex Class I <Emphasis Type="BoldItalic">A</Emphasis> Genes in the Cichlid Fish <Emphasis Type="BoldItalic">Oreochromis niloticus</Emphasis>

: The haplochromine cichlid species flocks of the East African Great Lakes are one of the best examples of adaptive radiation. Analysis of genetic variation among these species provides valuable information on species relationships and timing of speciation events. Although the haplochromine cichlids generally display little genetic variation, the major histocompatibility complex (Mhc) genes have been found to be highly variable. A study of the linkage relationships of the Mhc class I A genes in the cichlid fish Oreochromis niloticus was therefore undertaken. Class I loci were identified, and their segregation in seven mothers and their haploid embryos was determined. In total, 56 class I A sequences were found among the seven families. A strong concordance of segregation was observed in five haplotypes among the embryos, indicating a close linkage of all loci. The number of loci per haplotype varied from 11 to 17, while the total number of distinct loci found among all families was 22. These findings show that all class I A loci are linked in a single genetic cluster in O. niloticus.     

Fast adaptive responses in the oral jaw of Lake Victoria cichlids

Rapid morphological changes in response to fluctuating natural environments are a common phenomenon in species that undergo adaptive radiation. The dramatic ecological changes in Lake Victoria provide a unique opportunity to study environmental effects on cichlid morphology. This study shows how four haplochromine cichlids adapted their premaxilla to a changed diet over the past 30 years. Directly after the diet change toward larger and faster prey in the late 1980s, the premaxilla (upper jaw) changed in a way that is in agreement with a more food manipulating feeding style. During the 2000s, two zooplanktivorous species showed a reversal of morphological changes after returning to their original diet, whereas two other species showed no reversal of diet and morphology. These rapid changes indicate a potential for extremely fast adaptive responses to environmental fluctuations, which are likely inflicted by competition release and increase, and might have a bearing on the ability of haplochromines to cope with environmental changes. These responses could be due to rapid genetic change or phenotypic plasticity, for which there is ample evidence in cichlid fish structures associated with food capture and processing. These versatile adaptive responses are likely to have contributed to the fast adaptive radiation of haplochromines.