Research Article Received: 5 September 2013

Revised: 12 October 2013

Accepted article published: 14 December 2013

Published online in Wiley Online Library:

(wileyonlinelibrary.com) DOI 10.1002/ps.3709

Bemisia tabaci nomenclature: lessons learned Laura M Boykin∗ Abstract BACKGROUND: The nomenclature used within the whitefly research community for different putative species within Bemisia tabaci (sensu Russell) remains highly variable and confused. This was evident by the many different naming schemes researchers were using in their presentations at the 1st International Whitefly Symposium in Kolymbari, Crete, Greece (20–24 May 2013). I wanted to try to document how we, as a community, have arrived at such a state of confused nomenclature. This also included an investigation of the nomenclature used in the literature (from 2002 to 2012) by means of two online search tools (Web of Science and Scirus). RESULTS: Nomenclatural data were collected at the 1st International Whitefly Symposium, based on oral presentations and posters. There were 17 different names used for the MED species and 12 different names used for the MEAM1 species of the B. tabaci species complex. Investigation of the literature revealed limited uptake of the intermediate names. CONCLUSION: The intermediate names for the various species in the B. tabaci species complex – MED, MEAM1, New World, etc. – are not being used by the wider whitefly community. To move forwarrd as a community, we must work towards a formal revision of the B. tabaci complex. c 2013 Society of Chemical Industry  Keywords: whitefly, integrative taxonomy, Bemisia argentifolii, MED, MEAM1 and species complex

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MOTIVATION

The personal style in which this paper is written was inspired by T Dobzhansky and his paper synthesising what he observed at the American Biology Teachers’ conference in 1973.1 I decided to document and synthesise what I observed at the 1st International Whitefly Symposium in Kolymbari, Crete, Greece (20–24 May 2013) in the present paper. While in Greece, I quickly realised that the nomenclature used within the whitefly research community for the different putative species within Bemisia tabaci (sensu Russell2 ) remains highly variable and confused. This was evident by the many different naming schemes individual researchers were using in their presentations and also in recent publications involving B. tabaci. I wanted to try to document how we, as a community, have arrived at such a state of inconsistent nomenclature. I became involved in the whitefly community in 2006, and at that time everyone was using the ‘biotype’ nomenclature. There had been a few attempts to ‘overthrow’ the biotype nomenclature by Perring et al.3 with Bemisia argentifolii and De Barro et al.4 with the ‘race’ concept, but neither entities were embraced by the whitefly community. In 2007, we took a global perspective and documented considerable amounts of genetic variation (in the mtCOI region) in the clades recovered in the B. tabaci phylogeny.5 At the time (2007) we conservatively called them ‘genetic groups’ because of the global biosecurity implications of describing new species of B. tabaci.6 Following this work, pivotal mating experiments between the genetic groups7 – 9 led to a series of further studies that revealed a consistent pattern of limited mating between the different groups.10 – 12 In 2010, a threshold for ‘species’ was hypothesised,13 and in 2012 we used several species delimitation measures to define the species in the B. tabaci species complex.6 I was certain all the work on species delimitation in the B. tabaci species Pest Manag Sci (2014)

complex over the last 6 years would have made communication easier within the whitefly community, but it appears to have complicated the situation (from the data collected in Greece and subsequent literature searches). The purpose of this paper is to look into the history of the B. tabaci nomenclature, to document the lessons learned and to suggest a route map for creating a robust nomenclature that can be easily adopted by the whole community.

2 HISTORY OF THE B. tabaci BINOMIAL AND BIOTYPE The literature surrounding the B. tabaci species complex nomenclature has been controversial for many decades.2 – 6,14 – 16 Beginning in 1889, P Gennadius described a new species of whitefly from Greece that infested tobacco, which he named Aleurodes tabaci Gennadius.17 Since the original description of A. tabaci there have been many nomenclatural modifications to the entity initially called A. tabaci, including biotype, race, genetic group, putative species, species and haplotype group (Fig. 1a). Many papers have documented the early history of the naming of B. tabaci.15,16,18 The genus Bemisia was first described in 1914.19 In 1936, Takahashi20 moved A. tabaci to Bemisia and renamed it Bemisia tabaci, this marking the beginning of one



Correspondence to: Laura M Boykin, ARC Centre of Excellence in Plant Energy Biology,M316,TheUniversityofWesternAustralia,35StirlingHighway,Crawley, 6009 Western Australia, Australia. E-mail: [email protected] ARC Centre of Excellence in Plant Energy Biology, The University of Western Australia, Crawley, Western Australia, Australia

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Figure 1. (a) The major nomenclatural changes for the Bemisia tabaci species complex from 1889 to the present, and (b) the nomenclatural changes for the high-profile species (MED and MEAM1) and the species that have been matched to historical voucher specimens.

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of the most controversial names in invasive insect history. Many other whitefly species were synonymised with B. tabaci in 1957,2 creating much debate. In 1991, the biotype nomenclature was introduced to the B. tabaci nomenclature, and these designations were based on esterase patterns.21 With the advent of first RAPDS and then sequencing, esterase profiles have fallen into disuse, but the biotype nomenclature still persists in the literature (Fig 2). Referring to these species as biotypes should be discontinued because esterase profiling is no longer used to identify B. tabaci entities.

B. tabaci based on the unresolved position of B. argentifolii in both the nuclear internal transcribed spacer (ITS) and mtCOI gene trees. This paper identified six major races: Asia, Bali, Australia, sub-Saharan Africa, Mediterranean/Asia Minor/Africa and the New World. De Barro et al.4 suggested the following nomenclature for the various races: B. tabaci (Asia), B. tabaci (Bali), B. tabaci (Australia), B. tabaci (sub-Saharan Africa), B. tabaci (Mediterranean/Asia Minor/Africa) and B. tabaci (New World). This was the first attempt at a global phylogenetic analysis of the various members of the complex, and the results suggested that all members be treated at the same taxonomic rank.

3 B. argentifolii, MATING GROUPS AND RACES OF B. tabaci

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The most heated period in the debate regarding B. tabaci nomenclature (until recently) was a series of papers starting in 1993 in which Perring et al.3,22 took a bold step and raised the B. tabaci biotype B to species status by naming it Bemisia argentifolii.22 This was met with much controversy and divided the whitefly community.3,15,22 – 25 In 2004,7,26 mating experiments were conducted on allopatric and sympatric populations of B. tabaci in Africa and India found on several hosts, and three incompatible mating groups were found. These findings, coupled with mtCOI phylogenies (generated using parsimony and neighbour joining) led the researchers to hypothesise that these entities were possibly different species or ‘mating groups’. This was the first paper to correlate mating studies with phylogenetic relationships for the various entities in the B. tabaci species complex. The debate continued in the literature when De Barro et al.4 stated that B. argentifolii was not a separate species but a race of

GENETIC GROUPS OF B. tabaci

In 2007, the first published large-scale global phylogeny of all B. tabaci records in GenBank showed that the various clades recovered in the Bayesian phylogenies were quite distinct and well resolved,5 suggesting the presence of multiple species. At this time, we took a conservative approach and called the various distinct clades ‘genetic groups’, to avoid confusion, and based the names on the races described in De Barro et al.4 Mating studies that had been carried out in the past7,27,28 and new mating studies8,10 – 12 were now cast in a new context; individuals within the different genetic groups interbred successfully with one another, but crosses between individuals from different groups were predominantly unsuccessful. This linking of phylogenetically defined species (on a global scale) with mating studies marked a transition from the arbitrary, inconsistent and unquantifiable thinking behind the biotype nomenclature to viewing the genetic groups as species. Scrius

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Figure 2. Web of Science (http://thomsonreuters.com/web-of-science/) was used to search the literature search, and Scirus (http://www.scirus.com) was used to search all scientific items for the following keywords: Bemisia tabaci, Bemisia, Bemisia tabaci biotype, Bemisia argentifolii, Bemisia tabaci taxonomy, Bemisia MEAM1, Bemisia ‘genetic group’ and Bemisia species complex.

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B. tabaci PUTATIVE SPECIES al.,5

Continuing on from the work of Boykin et a refined global phylogeny was produced and ‘putative species’ were proposed on the basis of a 3.5% difference threshold of mtCOI sequences.13 It has been well documented that the ‘barcoding gap’, such as the 3.5% threshold hypothesised in Dinsdale et al.,13 can often mislead the identification and delimitation of species.29 To address this, a more robust approach to species delimitation was necessary to determine whether the 3.5% used by Dinsdale et al.13 was a good rule of thumb. A systematic approach that considered all hierarchical relations in turn was therefore taken to unravel the complexities of the B. tabaci species complex.6 It turns out, based on published data, that the B. tabaci species complex is not as complex as previously thought. The data tell us a very clear story – these putative species are different species supported by five independent species delimitation measures. In the context of species delimitation measures, obtaining consistent measures across the different metrics is not often achieved. When this is achieved, it makes a very clear statement – these groups are significantly different from one another; the most parsimonious explanation is that they are different species. The next steps are to assign names to the species16 by following the rules of the International Code of Zoological Nomenclature (ICZN) (http://iczn.org/iczn/index.jsp). The first step in naming the members of the B. tabaci species complex, according to Chapter 23, Section 23.1 of the ICZN, is the precedence of previously published binomials. Therefore, a valid name for a taxon is the oldest available name. Tay et al.16 have begun matching previously published binomials to the species of the B. tabaci species complex.

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THE PURPOSES OF THIS PAPER

The purposes of this paper are: (1) to document the evolution of the B. tabaci species complex nomenclature;2 – 7,13,17,21,30 (2) to assess the impact of nomenclatural changes by quantifying uptake of the new nomenclature at the most recent 1st International Whitefly Meeting and also in the literature; (3) to reflect upon the lessons learned throughout the process of naming the putative species of the B. tabaci species complex.

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for the MED species and 12 different names used for the MEAM1 species of the B. tabaci species complex. Clearly the thinking in the whitefly community has shifted away from treating these entities as biotypes, but a consistent nomenclature is yet to be defined.

9 NOMENCLATURAL DATA COLLECTED FROM THE LITERATURE (2002–2012) An investigation into the nomenclature used in the literature (from 2002 to 2012) was undertaken after observing the diversity of nomenclature that exists in the whitefly community (Table 1). Two online search tools were queried (see below for keywords): (1) Web of Science (http://thomsonreuters.com/web-of-science/) for the literature search; (2) Scirus (http://www.scirus.com), which searches all scientific items. The keywords searched were: Bemisia tabaci, Bemisia, Bemisia tabaci biotype, Bemisia argentifolii, Bemisia tabaci taxonomy, Bemisia MEAM1, Bemisia ‘genetic group’ and Bemisia species complex. Bemisia tabaci and Bemisia were chosen to assess overall interest in Bemisia over time. It is clear that the numbers of both scientific literature and scientific items – which includes web pages, courseware, preprint material, patents and institutional website information and journals (Fig. 2) – involving Bemisia and Bemisia tabaci have increased at an exponential rate over the last 10 years. The keywords Bemisia tabaci biotype, Bemisia argentifolii and Bemisia tabaci taxonomy were used to track older nomenclature. The literature shows a recent (2011–2012) decrease in the use of biotype, whereas the scientific items show an increase (Fig. 2). The keywords Bemisia MEAM1, Bemisia ‘genetic group’ and Bemisia species complex were chosen to assess whether these new terms are being used (see below for discussion).

Table 1. Diversity of nomenclature used for the MED and MEAM1 species at the 1st International Whitefly Symposium in Kolymbari, Crete, Greece (20–24 May 2013). Data collected from either oral presentations or the abstract book MED

MEAM1

Biotype Q

Biotype B

7 NOMENCLATURAL HISTORY OF THE MOST HIGH-PROFILE SPECIES

Q haplotype

B haplotype

Q1, Q2, Q3

MEAM1 species

Figure 1a shows the name changes through time (from 1889 to the present) of the two most notorious ‘entities’ of the B. tabaci species complex – MED and MEAM1. The binomial B. tabaci is equivalent to the putative species MED or the outdated biotype Q, as supported by the mtCOI sequencing of Gennadius’s original collection in 1889.16 In addition, Fig. 1b also documents the history of two additional species that have been recently identified using type specimens and mtCOI matching – B. inconspicua (New World 2) and B. gossypiperda (AsiaII8).31

Q1 cryptotype

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B. tabaci MED

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Q strain

Middle East Asia Minor 1 (B) species

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B-like biotype

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B. tabaci (MED, biotype Q)

‘B’ biotype

8 NOMENCLATURAL DATA COLLECTED AT THE GREECE MEETINGS, MAY 2013

MED

Nomenclatural data were collected at the 1st International Whitefly Symposium in Kolymbari, Crete, Greece (20–24 May 2013), based on oral presentations and the abstract book provided to all attendees. Table 1 shows that there were 17 different names used

MED species

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MED genetic group Mediterranean species ‘Q’ biotype

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2012. One explanation for this increase in scientific items is the transition in thinking from biotypes to species. Instead of one species, B. tabaci, there are many species in the B. tabaci species complex,6 opening up many new avenues of research. This new species framework has added many new areas of research, including providing a new insight into the virus transmission specificity of the species in the B. tabaci species complex,30 as well as genomic studies of the B. tabaci species and associated endosymbionts.33 – 40 Mating studies are also increasing within the new species framework.41,42

LESSONS LEARNED

10.1 Intermediate names have not been well received by the community The intermediate names MED, MEAM1, New World, etc.,6,18 are not being used by the wider whitefly community (Table 1; Fig. 2). Four possible reasons for this are as follows: (1) the intermediate names are awkward; (2) there has not been an official publication describing the species in accordance with the International Code of Zoological Nomenclature; (3) many are not convinced that we have yet found the species boundaries level; (4) a new naming scheme will never be accepted. Nomenclatural changes are difficult, as communication becomes clouded, but in the case of the B. tabaci species complex it has been a necessary step to propose these intermediate names because elevating the entities to species has important downstream implications.6 Adding to the confusion is the new nomenclature for the subclades of the MED species Q1, Q2 and Q3.32 Further work is necessary to clarify these new designations. 10.2 Adhere to the International Code of Zoological Nomenclature The rich history of nomenclature surrounding the various Bemisia entities15,18 has made matching older names more difficult, as many synonyms exist for the same entity. Matching older specimens is challenging because obtaining voucher specimens for DNA studies is controversial as some of the historic material is sacrificed. However, it is critical that a binomial name that has been formally described for a member of the B. tabaci species complex be used. Official descriptions of the putative species are forthcoming as matching older specimens continues. 10.3 B. argentifolii may rise again As it stands now, if no older named voucher specimen is identified to match the MEAM1 clade, B. argentifolii will be the official name for the MEAM1 putative species (Fig. 1b). The controversy surrounding B. argentifolii is 20 years old,3,23 – 25 but Fig. 2, which tracks all scientific items, shows no decrease in the utilisation of the name B. argentifolii. However, the usage of B. argentifolii is declining in the literature, which could be related to increase (Fig. 2) in the usage of the terms Bemisia species complex, Bemisia ‘genetic group’ and Bemisia MEAM1 – keywords that indicate the shift in thinking from biotype to species. 10.4 Nomenclatural changes have downstream implications Nomenclatural changes in high-profile species such as B. tabaci have downstream implications.6 Every country has protocols in place for handling B. tabaci; creating more species names would force the generation of additional protocols and strategies for handling the new species and trade documentation would need to be modified. Chemical companies that manufacture and market pesticides for use against B. tabaci would also be affected, as they would need to confirm effectiveness against every species. Regardless of these downstream implications, the data have driven the decision to propose elevation of biotypes to species for the B. tabaci species complex. 10.5 The new B. tabaci species framework has opened new avenues of research Clearly there was a significant increase in the scientific literature and scientific items (Fig. 2) involving B. tabaci from 2002 to Pest Manag Sci (2014)

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CONCLUDING REMARKS

Based on all the available data, including mating compatibility,10 – 12 mtCOI5,6,13,16 and genomes,37,43 these entities in the B. tabaci species complex appear to be different species. The sequence divergence between the MED and MEAM1 genomes is greater than the genetic differences between humans and chimps.43 The sooner the whitefly community transitions from thinking of these entities as biotypes to species the sooner we can standardise the nomenclature and move the research forward. This lack of effective communication within the community is and has been slowing down research; we spend so much time, energy and money debating what to call these ‘entities’. On a positive note, the fact that there were so many alternative names used at the Greece meetings (Table 1) indicates that we are moving our thinking beyond the biotype, but the uptake in the literature is slower. Clearly, a formal revision of the B. tabaci complex is needed, with official descriptions of the putative species. In addition, the whitefly community would benefit from a whitefly database to keep the community informed of nomenclatural changes as well as to store data.44 FlyBase45 has been successful for over 20 years and should be used as a guide for WhiteFlyBase.

ACKNOWLEDGEMENTS Two anonymous reviewers greatly improved the manuscript. I would like to thank Dr Paul De Barro (CSIRO Ecosystem Sciences) for years of support and collaboration. Dr Ian Small (Australian Research Council Centre of Excellence in Plant Energy Biology at The University of Western Australia) provided funds and support for my trip to the 1st International Whitefly Symposium in Greece. Dr Shu-Sheng Liu, Dr Xiao-Wei Wang and Hua-Ling Wang inspired me while I was visiting their lab at Zhejiang University in October 2012 as part of the New Zealand–China Scientist Exchange Programme.

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27 De Barro PJ and Hart PJ, Mating interactions between two biotypes of the whitefly, Bemisia tabaci (Hemiptera: Aleyrodidae), in Australia. B Entomol Res 90:103–112 (2000). 28 Perring TM and Symmes EJ, Courtship behavior of Bemisia argentifolii (Hemiptera: Aleyrodidae) and whitefly mate recognition. Ann Entomol Soc Am 99:598–606 (2006). 29 Meier R, Zhang GY and Ali F, The use of mean instead of smallest interspecific distances exaggerates the size of the ‘barcoding gap’ and leads to misidentification. Syst Biol 57:809–813 (2008). 30 Polston JE, De Barro PJ and Boykin LM, Transmission specificities of plant viruses with the newly identified species of the Bemisia tabaci species complex Pest Manag Sci in press (2013). 31 Tay WT, Evans GA, Boykin LM and De Barro PJ, Demonstrating the value of the voucher specimens to help resolve modern whitefly taxonomy. Proc 1st International Whitefly Symposium, Kolymbari, Crete, Greece, pp. 71 (2013). 32 Gueguen G, Vavre F, Gnankine O, Peterschmitt M, Charif D, Chiel E et al., Endosymbiont metacommunities, mtDNA diversity and the evolution of the Bemisia tabaci (Hemiptera: Aleyrodidae) species complex. Mol Ecol 19:4365–4378 (2010). 33 Bing XL, Ruan YM, Rao Q, Wang XW and Liu SS, Diversity of secondary endosymbionts among different putative species of the whitefly Bemisia tabaci. Insect Sci 20:194–206 (2013). 34 Bing XL, Yang J, Zchori-Fein E, Wang XW and Liu SS, Characterization of a newly discovered symbiont of the whitefly Bemisia tabaci (Hemiptera: Aleyrodidae). Appl Environ Microbiol 79:569–575 (2013). 35 Liu B, Preisser EL, Chu D, Pan H, Xie W, Wang S et al., Multiple forms of vector manipulation by a plant-infecting virus: Bemisia tabaci and tomato yellow leaf curl virus. J Virol 87:4929–4937 (2013). 36 Su Y, He WB, Wang J, Li JM, Liu SS and Wang XW, Selection of endogenous reference genes for gene expression analysis in the Mediterranean species of the Bemisia tabaci (Hemiptera: Aleyrodidae) complex. J Econ Entomol 106:1446–1455 (2013). 37 Wang HL, Yang J, Boykin LM, Zhao QY, Li Q, Wang XW et al., The characteristics and expression profiles of the mitochondrial genome for the Mediterranean species of the Bemisia tabaci complex. BMC Genom 14:401 (2013). 38 Wang ZZ, Shi M, Ye XQ, Chen MY and Chen XX, Identification, characterization and expression of a defensin-like antifungal peptide from the whitefly Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae). Insect Mol Biol 22:297–305 (2013). 39 Rao Q, Wang S, Zhu DT, Wang XW and Liu SS, Draft genome sequence of Rickettsia sp. strain MEAM1, isolated from the whitefly Bemisia tabaci. J Bacteriol 194:4741–4742 (2012). 40 Rao Q, Wang S, Su YL, Bing XL, Liu SS and Wang XW, Draft genome sequence of ‘Candidatus Hamiltonella defensa’, an endosymbiont of the whitefly Bemisia tabaci. J Bacteriol 194:3558 (2012) DOI: 10.1128/JB.00069-12. 41 Luan J and Liu S, Differences in mating behavior lead to asymmetric mating interactions and consequential changes in sex ratio between an invasive and an indigenous whitefly. Integr Zool 7:1–15 (2012). 42 Wang P, Crowder DW and Liu SS, Roles of mating behavioural interactions and life history traits in the competition between alien and indigenous whiteflies. B Entomol Res 102:1–11 (2012). 43 Wang XW, Luan JB, Li JM, Su YL, Xia J and Liu SS, Transcriptome analysis and comparison reveal divergence between two invasive whitefly cryptic species. BMC Genom 12:458 (2011). 44 Boykin LM, Armstrong K, Kubatko L and De Barro P, DNA barcoding invasive insects: database roadblocks. Invert Syst 26:506–514 (2012). 45 Marygold SJ, Leyland PC, Seal RL, Goodman JL, Thurmond JR, Strelets VB et al., The FlyBase Consortium. Nucleic Acids Res 41(D1):D751–D757 (2013).

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Bemisia tabaci nomenclature: lessons learned.

The nomenclature used within the whitefly research community for different putative species within Bemisia tabaci (sensu Russell) remains highly varia...
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