Elephant shark genome provides unique insights into gnathostome evolution

Abstract

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.

The seahorse genome and the evolution of its specialized morphology

“…Mosaic mutant F0 fish were outcrossed to AB wild-type fish and embryos were batch genotyped for transmission of the mutation using PCR and T7 endonuclease. Mutant PCR products were cloned into the pGEM-T vector Gene loci for human, coelacanth and zebrafish were adapted from other publications 60,61 . sparcl1, which is the ancestral gene that gave rise to SCPP genes is shown in grey; P/Q-rich SCPP genes are shown in red; acidic SCPP genes are shown in blue.…”

Identification and expression analysis of an atypical chemokine receptor-2 (ACKR2)/CC chemokine binding protein-2 (CCBP2) in rainbow trout (Oncorhynchus mykiss)

“…ACKR1 members were also included as an out group. The predicted elephant shark ACKR2 [27] was excluded from the phylogenetic tree analysis because of the uncertainty of its N-terminal sequence. All the ACKR2 molecules were grouped together and separated from other molecules (CCR1-5,8,9, CCRL1-2 and ACKR1) with high bootstrap support (98%) in a neighbour-joining tree.…”

“…no. XM_007908256) [27], although in the latter case the N-terminal of the predicted translation is relatively large and may include upstream genomic sequence. However, to date little or no functional analysis has been performed in fish.…”

Chordate evolution and the three-phylum system

“…By contrast, cartilaginous fishes produce extensive dermal bone, such as teeth, dermal denticle and fin spine. However, they lack the ability to make endochondral bone, which is unique to bony vertebrates (adapted from Venkatesh et al [96]). (b) The neural crest GRN in vertebrates.…”

“…Endochondral ossification is established by a highly complex process unique to bony vertebrates. Recent decoding of the elephant shark genome suggests that the lack of genes encoding secreted calcium-binding phosphoproteins in cartilaginous fishes explains the absence of bone in their endoskeleton [96]. Adaptive immune system.…”