The evolutionary and genetic patterns of African swine fever virus

Abstract

African swine fever (ASF) is a serious animal disease, and has spread to Africa, Europe and Asia, causing massive economic losses. African swine fever virus (ASFV) is transmitted from a reservoir host (warthog) to domestic pigs via a sylvatic cycle (transmission between warthogs and soft ticks) and a domestic cycle (transmission between domestic pigs) and survives by expressing a variety of genes related to virus–host interactions. We evaluated differences in codon usage patterns among ASFV genotypes and clades and explored the common and specific evolutionary and genetic characteristics of ASFV sequences. We analysed the evolutionary relationships, nucleotide compositions, codon usage patterns, selection pressures (mutational pressure and natural selection) and viral adaptation to host codon usage based on the coding sequences (CDS) of key functional genes of ASFV. AT bias was detected in the six genes analysed, irrespective of clade. The AT bias of genes (A224L, A179L, EP153R) encoding proteins involved in interaction with host cells after infection was high; among them, the AT bias of EP153R was the greatest at 78.3%. A large number of overrepresented codons were identified in EP153R, whereas there were no overrepresented codons with a relative synonymous codon usage (RSCU) value of ≥3 in B646L. In most genes, the pattern of selection pressure was similar for each clade, but in EP153R, diverse patterns of selection pressure were captured within the same clade and genotype. As a result of evaluating host adaptation based on the codon adaptation index (CAI), for B646L, E183L, CP204L and A179L, the codon usage patterns in all sequences were more similar to tick than domestic pig or wild boar. However, EP153R showed the lowest average CAI value of 0.52 when selecting tick as a reference set. The genes analysed in this study showed different magnitudes of selection pressure at the clade and genotype levels, which is likely to be related to the function of the encoded proteins and may determine key evolutionary traits of viruses, such as the level of genetic variation and host range. The diversity of codon adaptations at the genetic level in ASFV may account for differences in translational selection in ASFV hosts and provides insight into viral host adaptation and co-evolution.