Biological species in the viral world

Abstract

Due to their dependence on cellular organisms for metabolism and replication, viruses are typically named and assigned to species according to their genome structure and the original host that they infect. But because viruses often infect multiple hosts and the numbers of distinct lineages within a host can be vast, their delineation into species is often dictated by arbitrary sequence thresholds, which are highly inconsistent across lineages. Here we apply an approach to determine the boundaries of viral species based on the detection of gene flow within populations, thereby defining viral species according to the biological species concept (BSC). Despite the potential for gene transfer between highly divergent genomes, viruses, like the cellular organisms they infect, assort into reproductively isolated groups and can be organized into biological species. This approach revealed that BSC-defined viral species are often congruent with the taxonomic partitioning based on shared gene contents and host tropism, and that bacteriophages can similarly be classified in biological species. These results open the possibility to use a single, universal definition of species that is applicable across cellular and acellular lifeforms.

Keywords: asexuality; biological species concept; gene flow; recombination; speciation.

Fig. 1.

Recognizing biological species. In each set of genomes comprising n strains, nonredundant combinations of i strains (ranging from 4 to n − 2 strains) were subsampled 100 times for each value of i. At each iteration of subsampling, the h/m ratio—the ratio of polymorphisms attributable to homoplasy relative to those attributable to mutation—was calculated for the concatenated alignment of genes common to all strains. Within the bivariate plots, black dots are medians and the gray-shaded region is the SD of the indicated number of subsampled combinations of strains. Red dots and pink-shaded regions denote median h/m values and SD for simulations in which all homoplasies are introduced by convergent mutations, as described in the text. Differences between the distributions of observed and simulated h/m values indicate the extent to which homoplasies are introduced by recombination. Top shows the three possible outcomes of these analyses: when there are no barriers to gene flow among strains (Left); when a discontinuity is produced by inclusion of a strain that does not participate in gene exchange (Center); and when there is clonal evolution or an absence of gene flow (Right). Lower displays results obtained for dsDNA and ssRNA viruses.

Fig. 2.

Maximum sequence divergence between members of viral and bacteriophage species. Shown are average nucleotide sequence identity values for orthologous genes shared by the two maximally divergent strains within each biological species.

Fig. 3.

Prevalence of sex and related mechanisms in cellular and acellular taxa. Frequency of sexual species was compiled by ref. for animals, seed plants, ferns, and fungi and by ref. for bacteria (n = 91) and in the present study for animal viruses (n = 8) and bacteriophages (n = 17). Values reported for Rhizaria (n = 15) and Amoebozoa (n = 15) refer to the frequency of lineages containing sexual species reported in ref. .