Abstract
Organisms from diverse phylogenetic origins can thrive within the same ecological niches. They might be induced to evolve convergent adaptations in response to a similar landscape of selective pressures. Their genomes should bear the signature of this process. The study of unrelated virus lineages infecting the same host panels guarantees a clear identification of phyletically independent convergent adaptation. Here, we investigate the evolutionary history of genes in the accessory genome shared by unrelated insect large dsDNA viruses: the entomopoxviruses (EPVs, Poxviridae) and the baculoviruses (BVs). EPVs and BVs have overlapping ecological niches and have independently evolved similar infection processes. They are, in theory, subjected to the same selective pressures from their host’s immune responses. Their accessory genomes might, therefore, bear analogous genomic signatures of convergent adaption and could point out key genomic mechanisms of adaptation hitherto undetected in viruses. We uncovered 32 homologous, yet independent acquisitions of genes originating from insect hosts, different eukaryotes, bacteria and viruses. We showed different evolutionary levels of gene acquisition convergence in these viruses, underlining a continuous evolutionary process. We found both recent and ancient gene acquisitions possibly involved to the adaptation to both specific and distantly related hosts. Multidirectional and multipartite gene exchange networks appear to constantly drive exogenous gene assimilations, bringing key adaptive innovations and shaping the life histories of large DNA viruses. This evolutionary process might lead to genome level adaptive convergence.
Highlights
All cellular and viral species are engaged in multitrophic interactions involving a wide diversity of beneficial or antagonist partners [1]
We performed a protein secondary structure alignment clustering, using the jackhmmer program of the hmmer3 package [25], in an all-against-all alignment of all protein members of Entomopoxvirinae sub-family and Baculoviridae family found in the non-redundant protein database of the NCBI, including the newly described Adoxophyes honmai EPV (AHEV), Choristoneura biennis EPV (CBEV), Choristoneura rosaceana EPV (CREV) and Mythimna separata (MySEV) predicted proteins [14]
Out of 487 viral protein clusters, we found 33 clusters of homologous genes shared by EPVs and BVs, including 26 with similarities to cellular proteins and 21 with similarities to other families of large dsDNA viruses (Table 1)
Summary
All cellular and viral species are engaged in multitrophic interactions involving a wide diversity of beneficial or antagonist partners [1]. It is not uncommon for many parasites, including viruses, of unrelated families to thrive within the same host species [2]. The strongest evidence of adaptation though is the convergent evolution in independent lineages of similar traits and genomic features [5,6]. Large dsDNA viruses with their relatively fluid genomes provide sufficient genomic information to test if adaptation towards the same hosts might have produced similar traces on their genomes, the acquisition of beneficial genes [8]. Convergence at the genomic level is rarely demonstrated because phylogenetic independence is seldom achieved
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