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The African coelacanth genome provides insights into tetrapod evolution

Chris T. Amemiya

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- The discovery in 1997 of a second coelacanth species in Indonesia, Latimeria menadoensis, was surprising, as it had been assumed that living coelacanths were confined to small populations off the East African coast.
- Fascination with these fish is partly due to their prehistoric appearance—remarkably, their morphology is similar to that of fossils that date back at least 300 Myr, leading to the supposition that, among vertebrates, this lineage is markedly slow to evolve.
- The L. chalumnae genome has been reported previously to have a karyotype of 48 chromosomes.
- The Ensembl gene annotation pipeline created gene models using protein alignments from the Universal Protein Resource (Uniprot) database, limited coelacanth complementary DNA data, RNA-seq data generated from L. chalumnae muscle (18 Gb of paired-end reads were assembled using Trinity software, Supplementary Fig. 2) as well as orthology with other vertebrates.
- We found that the coelacanth genome contains a wide variety of transposableelement superfamilies and has a relatively high transposable-element content (25%); this number is probably an underestimate as this is a draft assembly (Supplementary Note 5 and Supplementary Tables 7–10).
- Analyses of chromosomal breakpoints in the coelacanth genome and tetrapod genomes reveal extensive conservation of synteny and indicate that large-scale rearrangements have occurred at a generally low rate in the coelacanth lineage. Analyses of these rearrangement classes detected several fission events published previously that are known to have occurred in tetrapod lineages, and at least 31 interchromosomal rearrangements that occurred in the coelacanth lineage or the early tetrapod lineage (0.063 fusions per 1 Myr), compared to events (0.054 fusions per 1 Myr) in the salamander lineage and events (0.057 fusions per 1 Myr) in the Xenopus lineage (Supplementary Note 7 and Supplementary Fig. 6). These analyses indicate that karyotypic evolution in the coelacanth lineage has occurred at a relatively slow rate, similar to that of non-mammalian tetrapods.
- In a separate analysis we examined the evolutionary divergence between the two species of coelacanth, L. chalumnae and L. menadoensis, found in African and Indonesian waters, respectively.
- When we compared the liver and testis transcriptomes of L. menadoensis to the L. chalumnae genome, we found an identity of 99.73% (Supplementary Note 8 and Supplementary Fig. 7), whereas alignments between 20 sequenced L. menadoensis bacterial artificial chromosomes (BACs) and the L. chalumnae genome showed an identity of 98.7% (Supplementary Table 11 and Supplementary Fig. 8).
- Over the 400 Myr that vertebrates have lived on land, some genes that are unnecessary for existence in their new environment have been eliminated. To understand this aspect of the water-to-land transition, we surveyed the Latimeria genome annotations to identify genes that were present in the last common ancestor of all bony fish but that are missing from tetrapod genomes.
- Our analysis identified 44,200 ancestral tetrapod coding elements (CNEs) that originated after the divergence of the coelacanth lineage.
- We have identified a region of the coelacanth HOX-A cluster that may have been involved in the evolution of extra-embryonic structures in tetrapods, including the eutherian placenta.
- We have confirmed that the protein-coding genes of L. chalumnae show a decreased substitution rate compared to those of other sequenced vertebrates, even though its genome as a whole does not show evidence of low genome plasticity.

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