East African cichlid lineages (Teleostei: Cichlidae) might be older than their ancient host lakes: new divergence estimates for the east African cichlid radiation.
ABSTRACT: BACKGROUND:Cichlids are a prime model system in evolutionary research and several of the most prominent examples of adaptive radiations are found in the East African Lakes Tanganyika, Malawi and Victoria, all part of the East African cichlid radiation (EAR). In the past, great effort has been invested in reconstructing the evolutionary and biogeographic history of cichlids (Teleostei: Cichlidae). In this study, we present new divergence age estimates for the major cichlid lineages with the main focus on the EAR based on a dataset encompassing representative taxa of almost all recognized cichlid tribes and ten mitochondrial protein genes. We have thoroughly re-evaluated both fossil and geological calibration points, and we included the recently described fossil †Tugenchromis pickfordi in the cichlid divergence age estimates. RESULTS:Our results estimate the origin of the EAR to Late Eocene/Early Oligocene (28.71?Ma; 95% HPD: 24.43-33.15?Ma). More importantly divergence ages of the most recent common ancestor (MRCA) of several Tanganyika cichlid tribes were estimated to be substantially older than the oldest estimated maximum age of the Lake Tanganyika: Trematocarini (16.13?Ma, 95% HPD: 11.89-20.46?Ma), Bathybatini (20.62?Ma, 95% HPD: 16.88-25.34?Ma), Lamprologini (15.27?Ma; 95% HPD: 12.23-18.49?Ma). The divergence age of the crown haplochromine H-lineage is estimated to 22.8?Ma (95% HPD: 14.40-26.32?Ma) and of the Lake Malawi radiation to 4.07?Ma (95% HDP: 2.93-5.26?Ma). In addition, we recovered a novel lineage within the Lamprologini tribe encompassing only Lamprologus of the lower and central Congo drainage with its divergence estimated to the Late Miocene or early Pliocene. Furthermore we recovered two novel mitochondrial haplotype lineages within the Haplochromini tribe: 'Orthochromis' indermauri and 'Haplochormis' vanheusdeni. CONCLUSIONS:Divergence time estimates of the MRCA of several Tanganyika cichlid tribes predate the age of the extant Lake Tanganyika basin, and hence are in line with the recently formulated "Melting-Pot Tanganyika" hypothesis. The radiation of the 'Lower Congo Lamprologus clade' might be linked with the Pliocene origin of the modern lower Congo rapids as has been shown for other Lower Congo cichlid assemblages. Finally, the age of origin of the Lake Malawi cichlid flock agrees well with the oldest age estimate for lacustrine conditions in Lake Malawi.
Project description:The species-flocks of cichlid fishes in the East African Great Lakes Victoria, Malawi and Tanganyika constitute the most diverse extant adaptive radiations in vertebrates. Lake Tanganyika, the oldest of the lakes, harbors the morphologically and genetically most diverse assemblage of cichlids and contains the highest number of endemic cichlid genera of all African lakes. Based on morphological grounds, the Tanganyikan cichlid species have been grouped into 12-16 distinct lineages, so-called tribes. While the monophyly of most of the tribes is well established, the phylogenetic relationships among the tribes remain largely elusive. Here, we present a new tribal level phylogenetic hypothesis for the cichlid fishes of Lake Tanganyika that is based on the so far largest set of nuclear markers and a total alignment length of close to 18kb. Using next-generation amplicon sequencing with the 454 pyrosequencing technology, we compiled a dataset consisting of 42 nuclear loci in 45 East African cichlid species, which we subjected to maximum likelihood and Bayesian inference phylogenetic analyses. We analyzed the entire concatenated dataset and each marker individually, and performed a Bayesian concordance analysis and gene tree discordance tests. Overall, we find strong support for a position of the Oreochromini, Boulengerochromini, Bathybatini and Trematocarini outside of a clade combining the substrate spawning Lamprologini and the mouthbrooding tribes of the 'H-lineage', which are both strongly supported to be monophyletic. The Eretmodini are firmly placed within the 'H-lineage', as sister-group to the most species-rich tribe of cichlids, the Haplochromini. The phylogenetic relationships at the base of the 'H-lineage' received less support, which is likely due to high speciation rates in the early phase of the radiation. Discordance among gene trees and marker sets further suggests the occurrence of past hybridization and/or incomplete lineage sorting in the cichlid fishes of Lake Tanganyika.
Project description:BACKGROUND:The diversification process known as the Lake Tanganyika Radiation has given rise to the most speciose clade of African cichlids. Almost all cichlid species found in the lakes Tanganyika, Malawi and Victoria, comprising a total of 12-16 tribes, belong to this clade. Strikingly, all the species in the latter two lakes are members of the tribe Haplochromini, whose origin remains unclear. The 'out of Tanganyika' hypothesis argues that the Haplochromini emerged simultaneously with other cichlid tribes and lineages in Lake Tanganyika, presumably about 5-6?million years ago (MYA), and that their presence in the lakes Malawi and Victoria and elsewhere in Africa today is due to later migrations. In contrast, the 'melting pot Tanganyika hypothesis' postulates that Haplochromini emerged in Africa prior to the formation of Lake Tanganyika, and that their divergence could have begun about 17 MYA. Haplochromine fossils could potentially resolve this debate, but such fossils are extremely rare. RESULTS:Here we present a new fossil haplochromine from the upper Miocene site Waril (9-10 million years) in Central Kenya. Comparative morphology, supported by Micro-CT imaging, reveals that it bears a unique combination of characters relating to dentition, cranial bones, caudal skeleton and meristic traits. Its most prominent feature is the presence of exclusively unicuspid teeth, with canines in the outer tooth row. †Warilochromis unicuspidatus gen. et sp. nov. shares this combination of characters solely with members of the Haplochromini and its lacrimal morphology indicates a possible relation to the riverine genus Pseudocrenilabrus. Due to its fang-like dentition and non-fusiform body, †W. unicuspidatus gen. et sp. nov. might have employed either a sit-and-pursue or sit-and-wait hunting strategy, which has not been reported for any other fossil haplochromine cichlid. CONCLUSIONS:The age of the fossil (9-10 MYA) is incompatible with the 'out of Tanganyika' hypothesis, which postulates that the divergence of the Haplochromini began only 5-6 MYA. The presence of this fossil in an upper Miocene palaeolake in the Central Kenya Rift, as well as its predatory lifestyle, indicate that Haplochromini were already an important component of freshwater drainages in East Africa at that time.
Project description: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.
Project description:With about 250 endemic species, Lake Tanganyika contains an extraordinarily diverse cichlid fish fauna, and thus represents an ideal model system for the study of pathways and processes of speciation. The Lamprologini form the most species-rich tribe in Lake Tanganyika comprising about 100 species in seven genera, most of which are endemic to the lake. They are territorial substrate-breeders and represent a monophyletic tribe. By combined analysis of population genetics and geometric morphometric markers, we assessed gene flow among three populations of the highly specialized shrimp-feeding rock-dweller Altolamprologus compressiceps, separated by geographic distance and ecological barriers. Five highly polymorphic microsatellite markers were analyzed in conjunction with 17 landmarks in order to compare genetic differences to body shape differences among populations. Both genetic and morphological analyses revealed significant differentiation among the three studied populations. A significant, but overall relatively low degree of genetic differentiation supports a very recent divergence. Phenotypic differentiation was primarily found in the head region of A. compressiceps. In agreement with findings in other cichlid species, similar adaptations to specialized feeding mechanisms can consequently lead to marginal shape changes in the trophic apparatus.
Project description:The cichlid fishes of Lake Malawi are famously diverse. However, phylogenetic and population genetic studies of their history have been difficult because of the great amount of genetic variation that is shared between species. We apply a recently developed method for fitting the "isolation with migration" divergence model to a data set of specially designed compound loci to develop portraits of cichlid species divergence. Outgroup sequences from a cichlid from Lake Tanganyika permit model parameter estimates in units of years and effective population sizes. Estimated speciation times range from 1,000 to 17,000 years for species in the genus Tropheops. These exceptionally recent dates suggest that Malawi cichlids as a group experience a very active and dynamic diversification process. Current effective population size estimates range form 2,000 to near 40,000, and to >120,000 for estimates of ancestral population sizes. It appears that very recent speciation and gene flow are among the reasons why it has been difficult to discern the phylogenetic history of Malawi cichlids.
Project description:Cichlid fishes are famous for large, diverse and replicated adaptive radiations in the Great Lakes of East Africa. To understand the molecular mechanisms underlying cichlid phenotypic diversity, we sequenced the genomes and transcriptomes of five lineages of African cichlids: the Nile tilapia (Oreochromis niloticus), an ancestral lineage with low diversity; and four members of the East African lineage: Neolamprologus brichardi/pulcher (older radiation, Lake Tanganyika), Metriaclima zebra (recent radiation, Lake Malawi), Pundamilia nyererei (very recent radiation, Lake Victoria), and Astatotilapia burtoni (riverine species around Lake Tanganyika). We found an excess of gene duplications in the East African lineage compared to tilapia and other teleosts, an abundance of non-coding element divergence, accelerated coding sequence evolution, expression divergence associated with transposable element insertions, and regulation by novel microRNAs. In addition, we analysed sequence data from sixty individuals representing six closely related species from Lake Victoria, and show genome-wide diversifying selection on coding and regulatory variants, some of which were recruited from ancient polymorphisms. We conclude that a number of molecular mechanisms shaped East African cichlid genomes, and that amassing of standing variation during periods of relaxed purifying selection may have been important in facilitating subsequent evolutionary diversification.
Project description:Lake Tanganyika comprises a cichlid species flock with substrate-breeding and mouthbrooding lineages. While sexual selection via mate choice on male mating color is thought to boost speciation rates in mouthbrooding cichlids, this is not the case in substrate-breeding lamprologines, which mostly form stable pairs and lack sexual dichromatism. We present a comprehensive reconstruction of the evolution of the cichlid tribe Lamprologini, based upon mtDNA sequences and multilocus nuclear DNA (AFLP) markers. Twelve mtDNA clades were identified, seven of which were corroborated by the AFLP tree. The radiation is likely to have started about 5.3 MYA, contemporarily with that of the mouthbrooding C-lineage, and probably triggered by the onset of deep-water conditions in Lake Tanganyika. Neither the Congo- nor the Malagarazi River species form the most ancestral branch. Several conflicts in the mtDNA phylogeny with taxonomic assignments based upon color, eco-morphology and behavior could be resolved and complemented by the AFLP analysis. Introgressive hybridization upon secondary contact seems to be the most likely cause for paraphyly of taxa due to mtDNA capture in species involving brood-care helpers, while accidental hybridization best explains the para- or polyphyly of several gastropod shell breeders. Taxonomic error or paraphyly due to the survival of ancestral lineages appear responsible for inconsistencies in the genera Lamprologus and Neolamprologus.
Project description:Lake Tanganyika is the oldest and phenotypically most diverse of the three East African cichlid fish adaptive radiations. It is also the cradle for the younger parallel haplochromine cichlid radiations in Lakes Malawi and Victoria. Despite its evolutionary significance, the relationships among the main Lake Tanganyika lineages remained unresolved, as did the general timescale of cichlid evolution. Here, we disentangle the deep phylogenetic structure of the Lake Tanganyika radiation using anchored phylogenomics and uncover hybridization at its base, as well as early in the haplochromine radiation. This suggests that hybridization might have facilitated these speciation bursts. Time-calibrated trees support that the radiation of Tanganyika cichlids coincided with lake formation and that Gondwanan vicariance concurred with the earliest splits in the cichlid family tree. Genes linked to key innovations show signals of introgression or positive selection following colonization of lake habitats and species' dietary adaptations are revealed as major drivers of colour vision evolution. These findings shed light onto the processes shaping the evolution of adaptive radiations.
Project description:The species flocks of cichlid fishes in the East African Great Lakes are the largest vertebrate adaptive radiations in the world and illustrious textbook examples of convergent evolution between independent species assemblages. Although recent studies suggest some degrees of genetic exchange between riverine taxa and the lake faunas, not a single cichlid species is known from Lakes Tanganyika, Malawi and Victoria that is derived from the radiation associated with another of these lakes. Here, we report the discovery of a haplochromine cichlid species in Lake Tanganyika, which belongs genetically to the species flock of haplochromines of the Lake Victoria region. The new species colonized Lake Tanganyika only recently, suggesting that faunal exchange across watersheds and, hence, between isolated ichthyofaunas, is more common than previously thought.
Project description:The Lake Malawi haplochromine cichlid flock is one of the largest vertebrate adaptive radiations. The geographical source of the radiation has been assumed to be rivers to the south and east of Lake Malawi, where extant representatives of the flock are now present. Here, we provide mitochondrial DNA evidence suggesting the sister taxon to the Lake Malawi radiation is within the Great Ruaha river in Tanzania, north of Lake Malawi. Estimates of the time of divergence between the Lake Malawi flock and this riverine sister taxon range from 2.13 to 6.76 Ma, prior to origins of the current radiation 1.20-4.06 Ma. These results are congruent with evaluations of 2-3.75 Ma fossil material that suggest past faunal connections between Lake Malawi and the Ruaha. We propose that ancestors of the Malawi radiation became isolated within the catchment during Pliocene rifting that formed both Lake Malawi and the Kipengere/Livingstone mountain range, before colonizing rivers to the south and east of the lake region and radiating within the lake basin. Identification of this sister taxon allows tests of whether standing genetic diversity has predisposed Lake Malawi cichlids to rapid speciation and adaptive radiation.