Abstract
The de novo birth of functional genes from non-coding DNA as an important contributor to new gene formation is increasingly supported by evidence from diverse eukaryotic lineages. However, many uncertainties remain, including how the incipient de novo genes would continue to evolve and the molecular mechanisms underlying their evolutionary trajectory. Here we address these questions by investigating evolutionary history of the de novo antifreeze glycoprotein (AFGP) gene and gene family in gadid (codfish) lineages. We examined AFGP phenotype on a phylogenetic framework encompassing a broad sampling of gadids from freezing and non-freezing habitats. In three select species representing different AFGP-bearing clades, we analyzed all AFGP gene family members and the broader scale AFGP genomic regions in detail. Codon usage analyses suggest that motif duplication produced the intragenic AFGP tripeptide coding repeats, and rapid sequence divergence post-duplication stabilized the recombination-prone long repetitive coding region. Genomic loci analyses support AFGP originated once from a single ancestral genomic origin, and shed light on how the de novo gene proliferated into a gene family. Results also show the processes of gene duplication and gene loss are distinctive in separate clades, and both genotype and phenotype are commensurate with differential local selective pressures.
Highlights
We reconstructed the phylogenetic relationships among a broad sampling of gadid species to map the antifreeze glycoprotein (AFGP) trait and trace the evolutionary origin and history of gadid AFGP
M. tomcod has four AFGP genes (Mt_AFGP1 to 4) and the last one is a pseudogene with a long (6.5 kbp) insertion in the coding region. These results depict a gradation of gene family size and gene copy number, largest in the high Arctic B. saida, and smallest in the cold temperate (Shinnecock Bay, NY, USA) M. tomcod, correlating with the substantially greater circulatory AFGP we found in B. saida (20.5 mg/mL) than in M
Under selective pressure from marine glaciation, the primordial AFGP originated de novo once, in a common gadine ancestor (Figure 1 node A), followed by retention or degeneration of the new trait in different lineages
Summary
Evolutionary adaptation relies on the origination of new genetic elements that could fuel evolutionary innovation. A type of new gene—de novo gene, which arose from DNA sequences that were ancestrally non-genic has gained increasing recognition as widespread, paving the way for a potential paradigm shift in our understanding of how new genes evolve. Emergence of a de novo gene from a non-protein coding sequence, previously deemed as a rare event [1,2], has been proposed to be a dominant mechanism of novel gene origination in recent analyses [3]. Occurrence of de novo genes could be quite readily inferred by comparative genomic and transcriptomic sequence analyses, but elucidating the molecular mechanism of their evolutionary process, the functional properties of the proteins they encode, and the adaptive fitness they confer are far more challenging [4,5,6]
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