Animal virus ecology and evolution are shaped by the virus host-body infiltration and colonization pattern.

Abstract

The current classification of animal viruses primarily relates to the virus molecular world, the genomic architecture and the corresponding host-cell infection cycle. This virus centered perspective does not make allowance for the precept that virus fitness hinges on the virus transmission success. Virus transmission reflects the infection-shedding-transmission dynamics and, with it, the organ system involvement and other, macroscopic dimensions of the host environment. This study examines the transmission ecology of the world main livestock viruses, 36 in total, belonging to eleven different families, and a mix of RNA, DNA and retroviruses. Viruses are virtually ranked in an outer- to inner-body fashion, based on the shifting organ system involvement and associated infection-shedding-transmission dynamics. As a next step, this ranking is disentangled with the aim to contrast two main host ecologies, poultry plus pig production and ruminant plus equine husbandry, as well as to create a distinction among the RNA, DNA and retroviruses, also ranked in an outer- to inner-body fashion. Spearman correlation reveals the matches among these various virus traits, as pertaining to the two host-ecologies, four infection-shedding-transmission related variables, and the three virus genomes. The collective results reveal the outer- to inner-body shifts in the interplay of host environment, virus-host interactions, and nature of the virus. Two opposing virus evolution pathways emerge, respectively for generalist type, outer-body and for specialist type, inner-body viruses. The ecological virus classification here presented is broadly consistent with the current virus classification system and offers the advantage of bringing substance and cohesion to the interrelationships among viruses and virus families.\n\nAuthor SummaryIt remains unknown how exactly viruses fit in the tree of life. Still, there is growing awareness that viruses as biological replicators are subjected to ecological sorting and so require a viable propagation strategy. In the current analysis I depart from the precept that virus fitness hinges on the virus transmission success. I examine the transmission ecologies of the world main livestock viruses, 36 in total, a collection of pathogens well described in terms of the organ system involvement, infection course, the extent of host damage, virus shedding profile, and virus transmission modes. The viruses are on this basis ranked in an outer- to inner-body fashion, virtually. As a next step, this ranking is disentangled with a view to contrast two main host ecologies, poultry plus pig production and ruminant plus equine husbandry, as well as to create a distinction among the RNA, DNA and retrovirus in the study. The matches among these various virus traits serve to establish the outer- to inner-body shifts in the interplay of host environment, virus-host interactions, and nature of the virus. Two opposing virus evolution pathways emerge, respectively for generalist type, outer-body and for specialist, inner-body viruses.