Coelacanth genomes reveal signatures for evolutionary transition from water to land

Abstract

Coelacanths are known as ''living fossils,'' as they show remarkable morphological resemblance to the fossil record and belong to the most primitive lineage of living Sarcopterygii (lobe-finned fishes and tetrapods). Coelacanths may be key to elucidating the tempo and mode of evolution from fish to tetrapods. Here, we report the genome sequences of five coelacanths, including four Latimeria chalumnae individuals (three specimens from Tanzania and one from Comoros) and one L. menadoensis individual from Indonesia. These sequences cover two African breeding populations and two known extant coelacanth species. The genome is~2.74 Gbp and contains a high proportion (~60%) of repetitive elements. The genetic diversity among the individuals was extremely low, suggesting a small population size and/or a slow rate of evolution. We found a substantial number of genes that encode olfactory and pheromone receptors with features characteristic of tetrapod receptors for the detection of airborne ligands. We also found that limb enhancers of bmp7 and gli3, both of which are essential for limb formation, are conserved between coelacanth and tetrapods, but not ray-finned fishes. We expect that some tetrapod-like genes may have existed early in the evolution of primitive Sarcopterygii and were later co-opted to adapt to terrestrial environments. These coelacanth genomes will provide a cornerstone for studies to elucidate how ancestral aquatic vertebrates evolved into terrestrial animals.

Next-generation sequencing detects repetitive elements expansion in giant genomes of annual killifish genus Austrolebias (Cyprinodontiformes, Rivulidae)

“…This fraction is very similar to that observed in C. melanotaenia (present work) and they were considerably greater than that of tetraodon (3.4 %), stickleback (4.5 %), and medaka (13.6 %) and inferior than that of zebrafish (35.4 %). Recently, a high proportion (*60 %) of repetitive elements has also been reported in the large genome (Nikaido et al 2013). However, the repetitive fraction of the A. charrua genome (45 %) reported here, in a total haploid genome of *3.0 Gb, surpasses all the values previously reported for diploid model and non-model ray-finned fish group (Actinopterygii).…”

“…In this sense, studies in the related aplocheloidei species N. furzeri revealed that among all TEs characterized, approximately 6.3 % are retrotransposons and 1.5 % DNA transposons (Reichwald et al 2009). However, in the genus Latimeria, 23 % of the genome is made up of DNA transposons, and 26 % is made up of retroposons comprising SINEs (13.6 %), LINEs (10.6 %), and LTR retrotransposons (2.2 %) (Nikaido et al 2013). Similar results could be observed in the parallel RepeatExplorer cluster simulation using approximately 1 % from the retrieved D. rerio genome, in which both types of TEs seem to be represented in the same proportion (See Electronic Supplementary Materials).…”

The life aquatic: advances in marine vertebrate genomics

“…Surprisingly, the homeobox (HOX) genes, which are known to have a role in the developmental stages of the body plan and limb formation 23,24 , remain largely conserved between the coelacanth and the tetra pods, as well as in comparisons of marine and terrestrial mammals 7-9 . However, candidate regu latory elements that are absent in teleosts are shared between the coelacanth and the tetrapods 19 , including a known cis-regulatory region proximal to the HoxD cluster 13 . Expression of the coelacanth HoxD cis-regulatory region in a transgenic mouse resulted in the expression of a reporter gene in forming limb buds, strongly indicating that this developmental enhancer region had a role in lobe-fin formation that may have been co-opted as a distal limb enhancer in tetrapods 13 (FIG.…”

“…Strikingly similar functional categories of protein-coding genes and regulatory regions -associated with the immune system, nitrogen excretion, limb formation and sensory adaptation -have undergone rapid evolution along the phylogenetic lineages to marine mammals, compared with their respective terrestrial ancestors 16 , and along the lineage to the tetrapods from the shared coelacanthtetrapod ancestor 13 . For example, the most enriched gene ontology categories for inferred regulatory elements that originated in tetrapods after their divergence from the coelacanth lineage were those associ ated with the sense of airborne smells 13,19 . By contrast, the gene family involved in olfactory receptor activity was the most decreased gene orthologue cluster in the genome of the Yangtze River dolphin, Lipotes vexillifer (known as the Baiji) 9 , and olfactory and taste receptors were under-represented in the genome of the minke whale, …”

Evolutionary conservation of a molecular machinery for export and expression of mRNAs with retained introns

“…Recently, sequencing of the genome of Latimeria chalumnae (a coelacanth, also known as "living fossil" fish) was completed and deposited in Ensembl and other genome browsers (Nikaido et al 2013). The coelacanths are lobefinned fish that appear to be more closely related to lungfish, reptiles, and mammals than to the common ray-finned fishes.…”