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Tracking the changes in virus taxonomy

Abstract

A database and website (http://www.ictvonline.org/taxonomyReleases.asp) have been established where the history of changes in virus taxonomy from 1971 to the present day can easily be traced. Each change is linked to a source document confirming the change or, for most changes since 2002, to the taxonomic proposal approved by the International Committee on Taxonomy of Viruses (ICTV).

Introduction

The attempt to create a universal taxonomic scheme for all viruses began in earnest at the IXth Congress of the International Association of Microbiological Societies (IAMS), held in Moscow in 1966. Meetings at the congress formally established what was termed the International Committee on Nomenclature of Viruses (ICNV). The Committee was so constituted that, wherever practicable, each country was represented by at least one member nominated by the microbiological society of that country. The first Executive Committee (EC) was also appointed with Professor Peter Wildy as its President. Members of the EC were appointed to chair subcommittees to develop taxonomy for the viruses of bacteriophage, invertebrates, plants and vertebrates, all of which would need the approval of the EC and of the entire ICNV.

While there have been some changes, this pattern of operation has largely continued to the present day. The ICNV was renamed the International Committee on Taxonomy of Viruses (ICTV) in 1974 and is today a committee of the Virology Division of the International Union of Microbiological Societies (IUMS).

Virus taxonomy differs from other types of biological classification because the ICTV not only regulates a Code of Nomenclature but also considers and approves the creation of virus taxa (currently orders, families, subfamilies, genera and species). Priority of publication is not the determining factor. The names of all recognized taxa are nowadays written in italics with an initial capital letter. All changes in taxonomy must first be approved by the EC and then by the entire voting membership of the ICTV. In the early years, the final vote was taken at an ICTV plenary session at an International Congress of Virology. These congresses have generally been held every three years, and the original intention was then to publish a report setting out the revised taxonomy following the Congress. With the passage of time, the ICTV reports developed into large reference works, requiring major efforts in editing and publication, and it has become impractical to publish them every three years. In addition, the explosion in virus discovery has meant that taxonomic changes need to be made more frequently. The current pattern is for annual changes, with the final ratification vote being conducted by e-mail.

The first formal report on virus classification was published in 1971 [25]. This report, which laid the foundation for viral taxonomy, covers the period from the formation of the ICNV in 1966 until 1970. Since then, there have been 27 occasions on which official taxonomy has changed. These changes may be traced by consulting the published reports of the ICTV and various articles (most of them in Archives of Virology) that have summarised the changes agreed by voting at virology congresses or by postal or e-mail ballots (Table 1). To make this information readily accessible, we have now developed a database and website where the entire history of taxonomic changes from 1971 to the present day can easily be traced. Each change is linked to a source document confirming the change or, for most changes since 2002, to the taxonomic proposal approved by the ICTV.

Table 1 Time points and references for changes in virus taxonomy

Preliminary considerations

Because the taxonomic categories recognised by the ICTV have changed over the years, some approximations or conventions have been adopted to ensure that all changes can be tracked.

The early published reports consisted of brief summaries of the genera officially recognized by the ICTV (and a small number of families), with lists of viruses that were considered ‘members’, ‘probable members’ and ‘possible members’ of these genera. One of the member viruses was identified as the ‘type member’ or ‘type species’. Plant viruses were presented in ‘groups’ until more data were available to determine whether these groups corresponded to genera or families. All such groups had disappeared by 1993, most of them being recognised and renamed as genera. Before about 1996, there were not usually specific proposals and ballots of ICTV members to establish new member viruses (or species) and the lists were revised (sometimes extensively) by the relevant study groups when each ICTV Report was published. Until this stage in the history of the ICTV, there had been no agreement on the need for, or definition of, virus species, but species were systematically introduced for the Seventh Report [24]. In many cases, these species lists corresponded to the viruses listed earlier as genus members, but in some genera closely related viruses were classified into a single species. Possible or probable members of genera and families were then listed as ‘tentative species’.

For the purpose of the database, the viruses listed as genus ‘members’ from 1971-1995 are treated as species. The ‘groups’ are usually treated as genera. No attempt has been made to list ‘possible members’, ‘probable members’ or ‘tentative species’. Where changes to taxonomy occurred, links are provided to proposal documents or other records (e.g. minutes recording the results of ICTV ballots) where available. As explained above, the recognition of new member viruses (or species) before 1996 can usually only be traced to the publication of a particular report. It is helpful to remember that while the taxonomic levels of orders, families, subfamilies, genera and species are recognised in virus taxonomy, not all these levels are necessarily used. Each species is a member of a higher taxon; this is usually a genus, but sometimes a species may be placed within a family or subfamily but not assigned to any current genus. Most genera, but not all, are placed in families. Many families are not currently assigned to an order, and few of them are divided into subfamilies.

Using the web site

The ICTV web site (Fig. 1, http://www.ictvonline.org) provides access to a wide variety of information pertinent to ICTV activities. This information includes copies of the ICTV Statutes and Code of Virus Classification (“The ICTV” menu); both approved and pending taxonomy proposals as well as downloadable copies of the complete virus taxonomy—the Master Species List (“ICTV Files” menu); and lists of Executive Committee, Subcommittee, and Study Group members (“ICTV Directory” menu). The current, and all past, releases of the virus taxonomy can be accessed from the ICTV taxonomic database and displayed from web links provided by the “Taxonomy” menu. The current taxonomy release (Fig. 2, http://www.ictvonline.org/virusTaxonomy.asp) displays a list of the complete taxonomic hierarchy organized alphabetically according to taxonomic rank. Each rank displayed within this taxonomy tree can be expanded by clicking on the + sign to the left of the taxon name. A list of historical ICTV releases is also available (Fig. 3, http://www.ictvonline.org/taxonomyReleases.asp). This list displays the year that the release was approved by the EC, the release number and location of the EC meeting during which the release was compiled, and statistics detailing the number of entries for each taxon rank. Clicking on the release year will open a web page that provides access to the corresponding taxon list. Release numbers are composed of up to three items: a MSL number that corresponds to the release number of the Master Species List, an EC number that corresponds to the Executive Committee meeting at which the proposals were discussed and approved, and an ICTV Report number that corresponds to the volume number of the ICTV Report’s publication for that MSL release.

Fig. 1
figure1

Screen shot of the ICTV web site home page, http://www.ictvonline.org

Fig. 2
figure2

Screen shot of the ICTV web site current taxonomy release, http://www.ictvonline.org/virusTaxonomy.asp

Fig. 3
figure3

Screen shot of the ICTV web site historical taxonomy releases, http://www.ictvonline.org/taxonomyReleases.asp

To search for a particular taxon across all taxonomy releases, a taxon name (or partial name) can be entered into the search box at the top of any taxonomy release page (Fig. 4). For example, entering the search term “bee” will result in a list of all taxon names that include the characters “bee” as a part of the name. The result set provides a list of these taxa, along with the year of each release in which each taxon name appears. Clicking on the “View” button to the left of the taxon will expand the taxonomy tree for that particular release, and highlight the taxon name in yellow (Fig. 4). To the right of each taxon name is a “history” link. A left and right arrow brackets the history link. If these arrows are colored, this provides an indication that the taxon has been updated from the previous release (red left arrow) and/or was updated in the next release (green right arrow). The “history” link opens a web page that provides the complete history of the taxon (Fig. 5) that summarizes all of the changes to the taxon over the years during which that taxon has existed. The terminology used to describe changes to a taxon’s history is provided in Table 2.

Fig. 4
figure4

Screen shot of the ICTV web site taxonomy search page

Fig. 5
figure5

Screen shot of the ICTV web site taxon history web page

Table 2 Terminology used to describe taxon changes

Conclusions

Compilation of these data has provided a thorough check of the ICTV records. A small number of mistakes, mostly in the spelling of species names, that became incorporated into Reports have been identified and corrected. Such corrections have been the subject of formal proposals to maintain comprehensive records. With very few exceptions, all taxonomic changes involving genera or higher taxa have been traced to published records. Procedures for presenting, reviewing and approving taxonomic proposals have developed over time but have become increasingly detailed and transparent in the last 10-15 years. The proposals of the last 10 years have all been assembled and linked to the database, providing a detailed justification for the changes made. Since 1971, the numbers of genera have risen from 43 to 455 and families from 2 to 103 (Fig. 6). This reflects a huge amount of work in virus discovery and characterization as well as the effort involved in making and evaluating taxonomic proposals. The speed of change will likely increase in the years ahead, and it is intended that this database will provide an ongoing and updated record of those changes.

Fig. 6
figure6

Graph showing changes to the numbers of genera, families, subfamilies and orders recognised by the ICTV, 1971-2014

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Acknowledgments

We thank past and present members of the Executive Committee of ICTV for their interest. We particularly thank Drs L. A. Ball, E. B. Carstens, A. M. Q. King and H. J. Vetten for their enthusiastic help in tracing ICTV documents included in this project and Dr. A. E. Gorbalenya for constructive suggestions.

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Correspondence to M. J. Adams.

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Adams, M.J., Hendrickson, R.C., Dempsey, D.M. et al. Tracking the changes in virus taxonomy. Arch Virol 160, 1375–1383 (2015). https://doi.org/10.1007/s00705-015-2376-4

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Keywords

  • Executive Committee
  • Virus Discovery
  • Taxonomic Change
  • Microbiological Society
  • Virus Taxonomy