Dataset Information

The genomic substrate for adaptive radiation in African cichlid fish.

ABSTRACT: 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.

SUBMITTER: Brawand D

PROVIDER: S-EPMC4353498 | biostudies-literature | 2014 Sep

REPOSITORIES: biostudies-literature

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The genomic substrate for adaptive radiation in African cichlid fish.

Brawand David D Wagner Catherine E CE Li Yang I YI Malinsky Milan M Keller Irene I Fan Shaohua S Simakov Oleg O Ng Alvin Y AY Lim Zhi Wei ZW Bezault Etienne E Turner-Maier Jason J Johnson Jeremy J Alcazar Rosa R Noh Hyun Ji HJ Russell Pamela P Aken Bronwen B Alföldi Jessica J Amemiya Chris C Azzouzi Naoual N Baroiller Jean-François JF Barloy-Hubler Frederique F Berlin Aaron A Bloomquist Ryan R Carleton Karen L KL Conte Matthew A MA D'Cotta Helena H Eshel Orly O Gaffney Leslie L Galibert Francis F Gante Hugo F HF Gnerre Sante S Greuter Lucie L Guyon Richard R Haddad Natalie S NS Haerty Wilfried W Harris Rayna M RM Hofmann Hans A HA Hourlier Thibaut T Hulata Gideon G Jaffe David B DB Lara Marcia M Lee Alison P AP MacCallum Iain I Mwaiko Salome S Nikaido Masato M Nishihara Hidenori H Ozouf-Costaz Catherine C Penman David J DJ Przybylski Dariusz D Rakotomanga Michaelle M Renn Suzy C P SCP Ribeiro Filipe J FJ Ron Micha M Salzburger Walter W Sanchez-Pulido Luis L Santos M Emilia ME Searle Steve S Sharpe Ted T Swofford Ross R Tan Frederick J FJ Williams Louise L Young Sarah S Yin Shuangye S Okada Norihiro N Kocher Thomas D TD Miska Eric A EA Lander Eric S ES Venkatesh Byrappa B Fernald Russell D RD Meyer Axel A Ponting Chris P CP Streelman J Todd JT Lindblad-Toh Kerstin K Seehausen Ole O Di Palma Federica F

Nature 20140903 7518

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 ...[more]

PMID: 25186727

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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.

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.

Dataset Information

The genomic substrate for adaptive radiation in African cichlid fish.

Publications

The genomic substrate for adaptive radiation in African cichlid fish.

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