The genomic substrate for adaptive radiation in African cichlid fish.
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ABSTRACT:
SUBMITTER: Brawand D
PROVIDER: S-EPMC4353498 | biostudies-literature | 2014 Sep
REPOSITORIES: biostudies-literature
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Project description:The African cichlid fish radiations are the most diverse extant animal radiations and provide a unique system to test predictions of speciation and adaptive radiation theory. The past few years have seen major advances in the phylogenetics, evolutionary biogeography and ecology of cichlid fish. Most of this work has concentrated on the most diverse radiations. Unfortunately, a large number of small radiations and 'non-radiations' have been overlooked, potentially limiting the contribution of the cichlid system to our understanding of speciation and adaptive radiation. I have reviewed the literature to identify 33 intralacustrine radiations and 76 failed radiations. For as many as possible I collected information on lake size, age and phylogenetic relationships. I use these data to address two questions: (i) whether the rate of speciation and the resulting species richness are related to temporal and spatial variation in ecological opportunity and (ii) whether the likelihood of undergoing adaptive radiation is similar for different African cichlid lineages. The former is a key prediction of the ecological theory of adaptive radiation that has been presumed true but remains untested for cichlid radiations. The second is based on the hypothesis that the propensity of cichlids to radiate is due to a key evolutionary innovation shared by all African cichlids. The evidence suggests that speciation rate declines through time as niches get filled up during adaptive radiation: young radiations and early stages of old radiations are characterized by high rates of speciation, whereas at least 0.5 Myr into a radiation speciation becomes a lot less frequent. The number of species in cichlid radiations increases with lake size, supporting the prediction that species diversity increases with habitat heterogeneity, but also with opportunity for isolation by distance. Finally, the data suggest that the propensity to radiate within lakes is a derived property that evolved during the evolutionary history of some African cichlids, and the appearance of which does not coincide with the appearance of proposed key innovations in morphology and life history.
| S-EPMC1635482 | biostudies-literature
Project description:The initial sequencing of five cichlid genomes revealed an accumulation of genetic variation, including extensive copy number variation in cichlid lineages particularly those that have undergone dramatic evolutionary radiation. Gene duplication has the potential to generate substantial molecular substrate for the origin of evolutionary novelty. We use array-based comparative heterologous genomic hybridization to identify copy number variation events (CNVEs) for 168 samples representing 53 cichlid species including the 5 species for which full genome sequence is available. We identify an average of 50-100 CNVEs per individual. For those species represented by multiple samples, we identify 150-200 total CNVEs suggesting a substantial amount of intraspecific variation. For these species, only ?10% of the detected CNVEs are fixed. Hierarchical clustering of species according to CNVE data recapitulates phylogenetic relationships fairly well at both the tribe and radiation level. Although CNVEs are detected on all linkage groups, they tend to cluster in "hotspots" and are likely to contain and be flanked by transposable elements. Furthermore, we show that CNVEs impact functional categories of genes with potential roles in adaptive phenotypes that could reasonably promote divergence and speciation in the cichlid clade. These data contribute to a more complete understanding of the molecular basis for adaptive natural selection, speciation, and evolutionary radiation.
| S-EPMC6795240 | biostudies-literature
Project description:BackgroundGene duplication is a source of evolutionary innovation and can contribute to the divergence of lineages; however, the relative importance of this process remains to be determined. The explosive divergence of the African cichlid adaptive radiations provides both a model for studying the general role of gene duplication in the divergence of lineages and also an exciting foray into the identification of genomic features that underlie the dramatic phenotypic and ecological diversification in this particular lineage. We present the first genome-wide study of gene duplication in African cichlid fishes, identifying gene duplicates in three species belonging to the Lake Malawi adaptive radiation (Metriaclima estherae, Protomelas similis, Rhamphochromis "chilingali") and one closely related species from a non-radiated riverine lineage (Astatotilapia tweddlei).ResultsUsing Astatotilapia burtoni as reference, microarray comparative genomic hybridization analysis of 5689 genes reveals 134 duplicated genes among the four cichlid species tested. Between 51 and 55 genes were identified as duplicated in each of the three species from the Lake Malawi radiation, representing a 38%-49% increase in number of duplicated genes relative to the non-radiated lineage (37 genes). Duplicated genes include several that are involved in immune response, ATP metabolism and detoxification.ConclusionsThese results contribute to our understanding of the abundance and type of gene duplicates present in cichlid fish lineages. The duplicated genes identified in this study provide candidates for the analysis of functional relevance with regard to phenotype and divergence. Comparative sequence analysis of gene duplicates can address the role of positive selection and adaptive evolution by gene duplication, while further study across the phylogenetic range of cichlid radiations (and more generally in other adaptive radiations) will determine whether the patterns of gene duplication seen in this study consistently accompany rapid radiation.
| S-EPMC3944005 | biostudies-literature
Project description:The mechanosensory lateral line system is used by fishes to sense hydrodynamic stimuli in their environment. It provides information about flow regimes, proximity to substrate, and the presence and identity of prey and predators and represents a means of receiving communication signals from other fish. Thus we may expect lateral line system structures to be under strong divergent selection during adaptive radiation. Here, we used X-ray micro-computed tomography scans to quantify variation in cranial lateral line canal morphology within the adaptive radiation of Lake Malawi cichlids. We report that cranial lateral line canal morphology is strongly correlated with diet and other aspects of craniofacial morphology, including the shape of oral jaws. These results indicate an adaptive role for the lateral line system in prey detection and suggest that diversification of this system has taken an important role in the spectacular evolution of Lake Malawi's cichlid fish diversity.
| S-EPMC6542376 | biostudies-literature
Project description:The adaptive radiation of cichlid fishes in East African Lake Malawi encompasses over 500 species that are believed to have evolved within the last 800,000 years from a common founder population. It has been proposed that hybridization between ancestral lineages can provide the genetic raw material to fuel such exceptionally high diversification rates, and evidence for this has recently been presented for the Lake Victoria region cichlid superflock. Here, we report that Lake Malawi cichlid genomes also show evidence of hybridization between two lineages that split 3-4 Ma, today represented by Lake Victoria cichlids and the riverine Astatotilapia sp. "ruaha blue." The two ancestries in Malawi cichlid genomes are present in large blocks of several kilobases, but there is little variation in this pattern between Malawi cichlid species, suggesting that the large-scale mosaic structure of the genomes was largely established prior to the radiation. Nevertheless, tens of thousands of polymorphic variants apparently derived from the hybridization are interspersed in the genomes. These loci show a striking excess of differentiation across ecological subgroups in the Lake Malawi cichlid assemblage, and parental alleles sort differentially into benthic and pelagic Malawi cichlid lineages, consistent with strong differential selection on these loci during species divergence. Furthermore, these loci are enriched for genes involved in immune response and vision, including opsin genes previously identified as important for speciation. Our results reinforce the role of ancestral hybridization in explosive diversification by demonstrating its significance in one of the largest recent vertebrate adaptive radiations.
| S-EPMC7086168 | biostudies-literature
Project description:Factors ranging from ecological opportunity to genome composition might explain why only some lineages form adaptive radiations. While being rare, particular systems can provide natural experiments within an identical ecological setting where species numbers and phenotypic divergence in two closely related lineages are notably different. We investigated one such natural experiment using two de novo assembled and 40 resequenced genomes and asked why two closely related Neotropical cichlid fish lineages, the Amphilophus citrinellus species complex (Midas cichlids; radiating) and Archocentrus centrarchus (Flyer cichlid; nonradiating), have resulted in such disparate evolutionary outcomes. Although both lineages inhabit many of the same Nicaraguan lakes, whole-genome inferred demography suggests that priority effects are not likely to be the cause of the dissimilarities. Also, genome-wide levels of selection, transposable element dynamics, gene family expansion, major chromosomal rearrangements and the number of genes under positive selection were not markedly different between the two lineages. To more finely investigate particular subsets of the genome that have undergone adaptive divergence in Midas cichlids, we also examined if there was evidence for 'molecular pre-adaptation' in regions identified by QTL mapping of repeatedly diverging adaptive traits. Although most of our analyses failed to pinpoint substantial genomic differences, we did identify functional categories containing many genes under positive selection that provide candidates for future studies on the propensity of Midas cichlids to radiate. Our results point to a disproportionate role of local, rather than genome-wide factors underlying the propensity for these cichlid fishes to adaptively radiate.
| S-EPMC8607476 | biostudies-literature
Project description:Ecomorphological differentiation is a key feature of adaptive radiations, with a general trend for specialization and niche expansion following divergence. Ecological opportunity afforded by invasion of a new habitat is thought to act as an ecological release, facilitating divergence, and speciation. Here, we investigate trophic adaptive morphology and ecology of an endemic clade of oreochromine cichlid fishes (Alcolapia) that radiated along a herbivorous trophic axis following colonization of an isolated lacustrine environment, and demonstrate phenotype-environment correlation. Ecological and morphological divergence of the Alcolapia species flock are examined in a phylogenomic context, to infer ecological niche occupation within the radiation. Species divergence is observed in both ecology and morphology, supporting the importance of ecological speciation within the radiation. Comparison with an outgroup taxon reveals large-scale ecomorphological divergence but shallow genomic differentiation within the Alcolapia adaptive radiation. Ancestral morphological reconstruction suggests lake colonization by a generalist oreochromine phenotype that diverged in Lake Natron to varied herbivorous morphologies akin to specialist herbivores in Lakes Tanganyika and Malawi.
| S-EPMC5132037 | biostudies-literature
Project description:African cichlid fishes are an ideal system for studying explosive rates of speciation and the origin of diversity in adaptive radiation. Within the last few million years, more than 2000 species have evolved in the Great Lakes of East Africa, the largest adaptive radiation in vertebrates. These young species show spectacular diversity in their coloration, morphology and behavior. However, little is known about the genomic basis of this astonishing diversity. Recently, five African cichlid genomes were sequenced, including that of the Nile Tilapia (Oreochromis niloticus), a basal and only relatively moderately diversified lineage, and the genomes of four representative endemic species of the adaptive radiations, Neolamprologus brichardi, Astatotilapia burtoni, Metriaclima zebra, and Pundamila nyererei. Using the Tilapia genome as a reference genome, we generated a high-resolution genomic variation map, consisting of single nucleotide polymorphisms (SNPs), short insertions and deletions (indels), inversions and deletions. In total, around 18.8, 17.7, 17.0, and 17.0 million SNPs, 2.3, 2.2, 1.4, and 1.9 million indels, 262, 306, 162, and 154 inversions, and 3509, 2705, 2710, and 2634 deletions were inferred to have evolved in N. brichardi, A. burtoni, P. nyererei, and M. zebra, respectively. Many of these variations affected the annotated gene regions in the genome. Different patterns of genetic variation were detected during the adaptive radiation of African cichlid fishes. For SNPs, the highest rate of evolution was detected in the common ancestor of N. brichardi, A. burtoni, P. nyererei, and M. zebra. However, for the evolution of inversions and deletions, we found that the rates at the terminal taxa are substantially higher than the rates at the ancestral lineages. The high-resolution map provides an ideal opportunity to understand the genomic bases of the adaptive radiation of African cichlid fishes.
| S-EPMC4042683 | biostudies-literature
Project description:Understanding why some evolutionary lineages generate exceptionally high species diversity is an important goal in evolutionary biology. Haplochromine cichlid fishes of Africa's Lake Victoria region encompass >700 diverse species that all evolved in the last 150,000 years. How this 'Lake Victoria Region Superflock' could evolve on such rapid timescales is an enduring question. Here, we demonstrate that hybridization between two divergent lineages facilitated this process by providing genetic variation that subsequently became recombined and sorted into many new species. Notably, the hybridization event generated exceptional allelic variation at an opsin gene known to be involved in adaptation and speciation. More generally, differentiation between new species is accentuated around variants that were fixed differences between the parental lineages, and that now appear in many new combinations in the radiation species. We conclude that hybridization between divergent lineages, when coincident with ecological opportunity, may facilitate rapid and extensive adaptive radiation.
| S-EPMC5309898 | biostudies-literature
Project description:Adaptive radiation (AR) is a key process in the origin of organismal diversity. However, the evolution of trait disparity in connection with ecological specialization is still poorly understood. Available models for vertebrate ARs predict that diversification occurs in the form of temporal stages driven by different selective forces. Here, we investigate the AR of cichlid fishes in East African Lake Tanganyika and use macroevolutionary model fitting to evaluate whether diversification happened in temporal stages. Six trait complexes, for which we also provide evidence of their adaptiveness, are analysed with comparative methods: body shape, pharyngeal jaw shape, gill raker traits, gut length, brain weight and body coloration. Overall, we do not find strong evidence for the 'stages model' of AR. However, our results suggest that trophic traits diversify earlier than traits implicated in macrohabitat adaptation and that sexual communication traits (i.e. coloration) diversify late in the radiation.
| S-EPMC4213606 | biostudies-literature