The diverse evolutionary histories of domesticated metaviral capsid genes in mammals

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Abstract

Selfish genetic elements and their remnants comprise at least half of the human genome. Active transposons duplicate by inserting copies at new sites in a host genome. Following insertion, transposons can acquire mutations that render them inactive; the accrual of additional mutations can render them unrecognizable over time. However, in rare instances, segments of transposons become useful for the host, in a process called gene domestication. Using the first complete human genome assembly and 25 additional vertebrate genomes, we analyzed the evolutionary trajectories and functional potential of genes domesticated from the capsid genes of Metaviridae , a retroviral-like retrotransposon family. Our analysis reveals four families of domesticated capsid genes in placental mammals with varied evolutionary outcomes, ranging from universal retention to lineage-specific duplications or losses and from purifying selection to lineage-specific rapid evolution. The four families of domesticated capsid genes have divergent amino-terminal domains, inherited from four distinct ancestral metaviruses. Structural predictions reveal that many domesticated genes encode a previously unrecognized RNA-binding domain retained in multiple paralogs in mammalian genomes both adjacent to and independent from the capsid domain. Collectively, our study reveals diverse outcomes of domestication of diverse metaviruses, which led to structurally and evolutionarily diverse genes that encode important, but still largely-unknown functions in placental mammals.

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  1. N-terminal regions

    If you seeded sequence- or structure-based searches with only these regions, do you ever see them fused to other known functional domains besides this family?

  2. function is not universally required in mammals

    Could it be that they had essential functions in now-extinct mammals? No idea how one would answer this, but I always wonder in these instances.

  3. 17 additional representative mammalian genomes

    Curious how these were chosen? Was it based primarily on availability or was there something specific about the particular ones you chose? Would have been cool to see more marsupials or monotremes represented, but I assume it was challenging to find high quality genomes that were amenable to your analyses?

  4. including reproduction

    I've always found this fascinating. Did ERV gene domestication happen at a particularly interesting moment in natural history for these animals with regard to reproduction? Something major that was changing in the environment that benefited from domestication events to accelerate change?