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.
The emergence of jawed vertebrates (gnathostomes) from jawless vertebrates was accompanied by major morphological and physiological innovations, such as hinged jaws, paired fins and immunoglobulin-based adaptive immunity. Gnathostomes subsequently diverged into two groups, the cartilaginous fishes and the bony vertebrates. Here we report the whole-genome analysis of a cartilaginous fish, the elephant shark (Callorhinchus milii). We find that the C. milii genome is the slowest evolving of all known vertebrates, including the ‘living fossil’ coelacanth, and features extensive synteny conservation with tetrapod genomes, making it a good model for comparative analyses of gnathostome genomes. Our functional studies suggest that the lack of genes encoding secreted calcium-binding phosphoproteins in cartilaginous fishes explains the absence of bone in their endoskeleton. Furthermore, the adaptive immune system of cartilaginous fishes is unusual: it lacks the canonical CD4 co-receptor and most transcription factors, cytokines and cytokine receptors related to the CD4 lineage, despite the presence of polymorphic major histocompatibility complex class II molecules. It thus presents a new model for understanding the origin of adaptive immunity.
Members of the teleost family Syngnathidae (seahorses, pipefishes and seadragons) (Extended Data Fig. 1), comprising approximately 300 species, display a complex array of morphological innovations and reproductive behaviours. This includes specialized morphological phenotypes such as an elongated snout with a small terminal mouth, fused jaws, absent pelvic and caudal fins, and an extended body covered with an armour of bony plates instead of scales 1 (Fig. 1a). Syngnathids are also unique among vertebrates due to their 'male pregnancy' , whereby males nourish developing embryos in a brood pouch until hatching and parturition occurs 2,3 . In addition, members of the subfamily Hippocampinae (seahorses) exhibit other derived features such as the lack of a caudal fin, a characteristic prehensile tail, and a vertical body axis 4 (Fig. 1a). To understand the genetic basis of the specialized morphology and reproductive system of seahorses, we sequenced the genome of the tiger tail seahorse, H. comes, and carried out comparative genomic analyses with the genome sequences of other ray-finned fishes (Actinopterygii). Genome assembly and annotationThe genome of a male H. comes individual was sequenced using the Illumina HiSeq 2000 platform. After filtering low-quality and duplicate reads, 132.13 Gb (approximately 190-fold coverage of the estimated 695 Mb genome) of reads from libraries with insert sizes ranging from 170 bp to 20 kb were retained for assembly. The filtered reads were assembled using SOAPdenovo (version 2.04) to yield a 501.6 Mb assembly with an N50 contig size and N50 scaffold size of 34.7 kb and 1.8 Mb, respectively. Total RNA from combined soft tissues of H. comes was sequenced using RNA-sequencing (RNA-seq) and assembled de novo. The H. comes genome assembly is of high quality, as > 99% of the de novo assembled transcripts (76,757 out of 77,040) could be mapped to the assembly; and 243 out of 248 core eukaryotic genes mapping approach (CEGMA) genes are complete in the assembly.We predicted 23,458 genes in the genome of H. comes based on homology and by mapping the RNA-seq data of H. comes and a closely related species, the lined seahorse, Hippocampus erectus, to the genome assembly (see Methods and Supplementary Information). More than 97% of the predicted genes (22,941 genes) either have homologues in public databases (Swissprot, Trembl and the Kyoto Encyclopedia of Genes and Genomes (KEGG)) or are supported by assembled RNAseq transcripts. Analysis of gene family evolution using a maximum likelihood framework identified an expansion of 25 gene families (261 genes; 1.11%) and contraction of 54 families (96 genes; 0.41%) in the H. comes lineage (Extended Data Fig. 2 and Supplementary Tables 4.1, 4.2). Transposable elements comprise around 24.8% (124.5 Mb) of the H. comes genome, with class II DNA transposons being the most abundant class (9%; 45 Mb). Only one wave of transposable element expansion was identified, with no evidence for a recent transposable element burst (Kimura divergence ≤ 5) (Extended D...
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