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This review argues that the three popular concepts of design, rationality and reductionism, which guided vaccine research for many years, actually contributed to the inability of vaccinologists to develop an effective HIV vaccine. The strong goal-directed intentionality inherent in the concept of design together with excessive confidence in the power of rational thinking convinced investigators that the accumulated structural knowledge on HIV epitopes, derived from crystallographic studies of complexes of neutralizing antibodies bound to HIV Env epitopes, would allow them to rationally design complementary immunogens capable of inducing anti-HIV protective antibodies. This strategy failed because it was not appreciated that the structures observed in epitope-paratope crystallographic complexes result from mutually induced fit between the two partners and do not represent structures present in the free disordered molecules before they had interacted. In addition, reductionist thinking led investigators to accept that biology could be reduced to chemistry, and this made them neglect the fundamental difference between chemical antigenicity and biological immunogenicity. As a result, they did not investigate which inherent constituents of immune systems controlled the induction of protective antibodies and focused instead only on the steric complementarity that exists between bound epitopes and paratopes.

Properties useful for defining virus species are phenotypic properties of viruses that can be altered by a few mutations. Such properties include the natural host range, cell and tissue tropism, symptomatology, pathogenicity and mode of transmission. All these properties are not necessarily present in identical form in all the members of a species; therefore, a virus species is a polythetic class of viruses defined by a variable combination of several properties rather than by a single conserved property present in all the members of the species. This review will discuss current controversies about what virus species actually are as well as which names should be given to them. It will be emphasized that most species-defining properties are so-called relational properties that arise because viruses necessarily interact with biological partners such as vectors, hosts and immune systems. Although these relational properties are of utmost importance to laboratory and clinical virologists, they remain unknown if only the viral genome is available and the relational partners of the virus have not yet been identified. Since the International Committee on Taxonomy of Viruses (ICTV) in 2013 ratified a new definition of virus species, which no longer accepts that species are polythetic classes but instead are monophyletic groups, the implications of this new definition for viral taxonomy and nomenclature will be analyzed. In my private capacity, I also make the following recommendations regarding current debates on proposed new names for virus species as well as on the feasibility of assigning viral sequences found in metagenomic databases to individual species taxa in the current ICTV classification. 1) The ICTV should abandon the current rule that the names of virus species (for instance Measles virus) should differ from the virus name (measles virus) only by typography. 2) Non-Latinized binomial species names based on familiar virus and genus names should become the norm. This would obviate the need to create about 5000 hard-to-memorize Latinized species names. 3) Virus species are defined not by the intrinsic properties of virions and viral genomes but by the relational properties of viruses that arise from their interactions with host and vector partners. Since the hosts and vectors associated with nearly all viral sequences found in metagenomic databases are unknown, the phenotypic properties of the putative viruses also remain unknown, and these viral sequences cannot be allocated to established species in the ICTV classification.

A common logical confusion is prevalent in the whole of biology, namely that biological species are viewed both as an abstract category in an hierarchical classification and as a concrete kind of organism. This is partly due to the fact that the vast majority of living organisms do not have common names that differ from the Latin name of the species to which the organism belongs. However, it is somewhat astonishing that the same confusion exists in virology since every virus has a common name, different from the species name to which the virus belongs, which could be used to refer to the infectious viral entity as a concrete material object. The original 1991 ICTV definition of virus species stated that a virus species is a polythetic class of viruses and thus that a species is a class, namely a conceptual construction of the mind and not a physical, real object located in space and time. In 2013, the ICTV redefined a virus species no longer as a class but as a material object consisting of a monophyletic group of viruses that were all physically part of the species. This new definition is reminiscent of an earlier school of thought known as bionominalism which considered species to be concrete individuals rather than classes. Both bionominalism and the new ICTV definition are based on the logical fallacy of reification which treats abstractions such as classes as if they were concrete physical entities. The implications of this new ontology of virus species for virus taxonomy and for the possibility of incorporating nucleotide metagenomic sequences in the current ICTV classification is discussed.