In an effort to understand the molecular basis of adaptation in vertebrates, researchers sequenced the genomes and transcriptomes of five species of the African cichlid fish.
The researchers uncovered a variety of features in the cichlid genome that enabled the fishes to thrive in new habitats and ecological niches within the Great Lakes of East Africa.
In addition to helping explain the complex genomic mechanisms that give rise to incredible diversity among cichlid fishes, the findings from these ‘natural mutants’ shed new light on the molecular process of evolution in all vertebrate species.
The study was led by Director of Science at The Genome Analysis Centre (TGAC) Federica Di Palma. The research paper, done in collaboration with scientists at the Broad Institute, Eawag Swiss Federal Institute for Aquatic Sciences and Georgia Institute of Technology, in addition to international scientists in the cichlid research community, appears in the September, advance online edition of Nature.
Using the cichlid fish species as a model system gives us valuable insight into human biology and disease.
Federica Di Palma, last author of the Nature study, previously Assistant Director of Vertebrate Sequencing and Analysis at the Broad, said: “This study shows how important it is to fund underpinning biology research in non-conventional model organisms. By learning how natural populations, such as fishes, adapt and evolve under selective pressures, we can learn how these pressures affect humans in terms of health and disease.”
The African cichlid fishes are some of the most phenotypically diverse groups of organisms on the planet, with over 2,000 known species. Some lakes are home to hundreds of distinct species that evolved from a common ancestral species that left its ancient river habitat to colonise the lake. Like Darwin’s finches, the cichlids are a dramatic example of adaptive radiation, the process by which multiple species ‘radiate’ from an ancestral species through adaptation.
“Our study reveals a spectrum of methods that nature uses to allow organisms to adapt to different environments,” said senior author Kerstin Lindblad-Toh, Scientific Director of Vertebrate Genome Biology at the Broad Institute: “These mechanisms are likely to be also at work in humans and other vertebrates, and by focusing on the remarkably diverse cichlid fishes, we were able to study this process on a broad scale for the first time.”
The researchers wanted to examine the cichlid genome as a model system and determine what allowed these fishes to diversify broadly in a relatively short time. The researchers sequenced the DNA and RNA – the genome and transcriptomes (all the messenger RNA) from ten tissues – of five distinct lineages of African cichlids.
The sequenced species include the Nile tilapia, representing the ancestral lineage, and four East African species: a species that inhabits a river near Lake Tanganyika; a species from Lake Tanganyika that appeared 10-20 million years ago; a cichlid species from Lake Malawi that appeared less than 5 million years ago; and a very recent species from Lake Victoria that radiated less than 15,000 to 100,000 years ago.
After analysing the data, the researchers found a surprising number of genomic elements at play. Compared with the ancestral lineage, the East African cichlid genomes possess: an excess of gene duplications; alterations in regulatory, non-protein-coding elements in the genome; accelerated evolution of protein-coding elements, especially in genes for pigmentation; and other distinct features that affect gene expression, such as insertions of transposable elements and regulation by novel microRNAs.
“It’s not one big change in the genome of this fish, but lots of different molecular mechanisms used to achieve this amazing adaptation and speciation,” said Federica.
Some changes in the genome appear to have accumulated before the species left the rivers to colonise lakes and radiated into hundreds of species. This suggests that the cichlids were once in a period of reduced constraint. During this time, the fishes accumulated diversity through genetic mutations, and the relaxed constraint – in which all individuals thrived, not just the fittest – allowed genetic variation to accumulate. As the fish later inhabited new environmental niches within the lakes, new species could form quickly through selection. In this way, a reservoir of mutations – and resultant phenotypes – represented a ‘genomic toolkit’ that allowed quick adaptation.
More work remains to fully dissect the mechanisms and may involve the sequencing of many more cichlid species. This effort could help explain how similar forms or traits evolved in parallel in different lakes, converging on the same morphology through distinct lineages.
Ole Seehausen, senior author and Head of Fish Ecology and Evolution at Eawag Aquatic Research, said: “African cichlid fish stand out amongst fish by their incredible richness of species that evolved without geographical isolation and that now coexist within individual lakes. We were puzzled about how their genomic blueprint could accommodate all the different forms and functions. We learned that the radiation ancestors had an opportunity to amass genomic variation of many different kinds. At the time this was probably rather useless genomic variation, but has now become incredibly beneficial millions of years later when the opportunity for major adaptive radiations arose, changing the way we think about evolutionary processes.”
This work was funded in part by the National Human Genome Research Institute (NHGRI), the Swiss National Science Foundation, the German Science Foundation, Biomedical Research Council of A*STAR, Singapore, the European Research Council, and the Wellcome Trust.
The paper, titled: “The genomic substrate for adaptive radiation in African cichlid fish” is published in Nature.