Review Article |
Corresponding author: Alvin Hee ( alvinhee@upm.edu.my ) Academic editor: Anthony Clarke
© 2015 Alvin Hee, Suk-Ling Wee, Ritsuo Nishida, Hajime Ono, Jorge Hendrichs, David S Haymer, Keng-Hong Tan.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Hee AKW, Wee SL, Nishida R, Ono H, Hendrichs J, Haymer DS, Tan KH (2015) Historical perspective on the synonymization of the four major pest species belonging to the Bactrocera dorsalis species complex (Diptera, Tephritidae).In: De Meyer M, Clarke AR, Vera MT, Hendrichs J (Eds) Resolution of Cryptic Species Complexes of Tephritid Pests to Enhance SIT Application and Facilitate International Trade. ZooKeys 540: 323–338. https://doi.org/10.3897/zookeys.540.6028
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An FAO/IAEA-sponsored coordinated research project on integrative taxonomy, involving close to 50 researchers from at least 20 countries, culminated in a significant breakthrough in the recognition that four major pest species, Bactrocera dorsalis, B. philippinensis, B. papayae and B. invadens, belong to the same biological species, B. dorsalis. The successful conclusion of this initiative is expected to significantly facilitate global agricultural trade, primarily through the lifting of quarantine restrictions that have long affected many countries, especially those in regions such as Asia and Africa that have large potential for fresh fruit and vegetable commodity exports. This work stems from two taxonomic studies: a revision in 1994 that significantly increased the number of described species in the Bactrocera dorsalis species complex; and the description in 2005 of B. invadens, then newly incursive in Africa. While taxonomically valid species, many biologists considered that these were different names for one biological species. Many disagreements confounded attempts to develop a solution for resolving this taxonomic issue, before the FAO/IAEA project commenced. Crucial to understanding the success of that initiative is an accounting of the historical events and perspectives leading up to the international, multidisciplinary collaborative efforts that successfully achieved the final synonymization. This review highlights the 21 year journey taken to achieve this outcome.
Bactrocera dorsalis species complex, B. philippinensis , B. papayae , B. invadens , synonymization, integrative taxonomy
The genus Bactrocera Macquart of true fruit flies belongs to the Dacinae - a subfamily of Tephritidae (
Within Bactrocera, the B. dorsalis species complex contains almost 100 species that are morphologically similar and occur in the tropics and subtropics where fruit growing areas are extensive (
The existence of a complex of closely related, morphologically similar species to B. dorsalis, had been recognized for over 40 years (
The extensive similarities between B. dorsaliss.s and the three putative species established, B. invadens, B. papayae and B. philippinensis, has led to much debate on the delimitation of these species, particularly in terms of seeking congruence between the biological and taxonomic status of these entities (
To address and resolve the longstanding issue of species delimitation in the key pest species of the B. dorsalis complex, a multidisciplinary approach was adopted by an international team of more than fifty researchers from over twenty different countries. Under the auspices of the Joint FAO/IAEA Division on Nuclear Techniques in Food and Agriculture, a 5-year Coordinated Research Project (CRP) on ‘Resolution of Cryptic Species Complexes of Tephritid Pests to Overcome Constraints to SIT Application and International Trade’ was established in 2010. The aim of the project was to define the species limits of pest species complexes within the Tephritidae, with the B. dorsalis complex identified as a priority. Studies that had been independently developed in the past, including morphometric, cytogenetic, molecular, behavioural and chemoecological datasets were re-examined, and gaps crucial for answering questions of how taxonomic species could be reconciled as biological species were filled. This project has led to the synonymization of B. papayae, B. philippinensis and B. invadens with B. dorsalis, based on the conclusion that there is insufficient evidence to maintain the former three taxa as biological species distinct from B. dorsalis (
It is not the aim of this paper to again provide the evidence for the synonymization of the four major pest species, as this has already been provided (
Before describing some of the biological insights which led to the questioning of taxonomic validity of these species, this section details the taxonomic history of the taxa of concern.
Prior to the taxonomic revision of the B. dorsalis complex by
The concern over the destructive potential of B. papayae also underscored the importance of another closely related species, B. carambolae Drew & Hancock, which itself had formerly been referred to as Malaysian A (
Additional to ‘species near B. dorsalis (A) and (B), was a third taxon, designated as ‘sp. near B. dorsalis (C) (
As for the South-east Asian pest species of the B. dorsalis complex, confusion also existed for B. invadens in Africa, a devastating pest species now widespread in Africa, which has largely displaced other long established pests such as Mediterranean fruit fly, Ceratitis capitata (Wiedemann) (
Efforts of fruit fly workers over two decades to resolve the biological species status of B. papayae, B. philippinensis, B. invadens and B. dorsalis started with the question from one of us (Keng-Hong Tan) on why males of certain fly species, such as B. dorsalis, are so strongly attracted to methyl eugenol (ME). This research effort was partly in response to a challenge posed by N. Tanaka of the USDA Hawaiian Fruit Flies Investigations Laboratory in 1980 to figure out the role of ME in the biology of male tephritid flies. Whilst ME was first discovered a century ago as attracting male fruit flies (
While Tan and colleagues searched for the reason as to why male Bactrocera respond to ME, significant insights were also gained as to the likely biological relationships between B. dorsalis and B. papayae (especially). This section describes the history of that process.
In the early 1980s work was undertaken using ME for field ecological surveys and population dynamics of Dacus species. This work demonstrated for the first time that temporary habituation of the male flies to ME is possible (
In 1986, the research collaboration of Keng-Hong Tan and Ritsuo Nishida of Kyoto University on the ecological significance of male fruit fly attractants took off after the introduction of Nishida by Professor S. Takahashi also of Kyoto University to Tan. This research collaboration resulted in the detection of the phenylpropanoids, (E)-coniferyl alcohol (CF) and 2-allyl-4,5-dimethoxyphenol (DMP), as sex pheromone components of male B. dorsalis (samples from Malaysia later known as ‘Malaysian B’ and then B. papayae - see next paragraph) following ME consumption (
During that time, B. dorsalis in Malaysia had been taxonomically split into two sibling species, Malaysian A and Malaysian B in 1991, and subsequently in 1994 described as B. carambolae and B. papayae, respectively. These sibling species, together with B. dorsaliss.s., were morphologically very similar to each other, particularly for male flies, and much work was concentrated on attempts to differentiate these species. In 1994, results from a primary chemotaxonomic diagnostic tool were presented in the 4th International Symposium of Fruit Flies of Economic Importance held in Tampa, Florida, demonstrating that CF and DMP were detected in both B. dorsalis (ex-Hawaii) and B. papayae, and with improved male mating competitiveness, following males’ consumption of ME (
The discovery that both B. dorsalis and B. papayae, having very similar morphological characters, also possessed identical pheromone components and mated readily under semi-natural conditions and producing viable offspring over generations provided the first strong evidence that the two species deserved to be considered as a single biological species. These are the basic criteria for species delimitation of Mayr’s ‘Biological Species Concept’ (
Following the revision of the B. dorsalis complex in 1994, differences in male genitalia length was used as the sole morphological basis of separating B. papayae from B. dorsalis (
The development of DNA-based markers meant that a broader range of molecular tools were available to researchers in clarifying the status of species. Using ribosomal DNA markers, for example, had shown in tephritids that it was possible to differentiate distinct species within and between genera of flies, but not within a complex of closely related species (
Additional molecular work on species in the B. dorsalis complex began with the analysis of the actin gene family in B. dorsalis (He and Haymer 1994). Specifically, intron sequences from these genes were used for the analysis of genetic variation in populations of B. dorsalis and its sibling species in the B. dorsalis complex (
Following this, samples of Bactrocera flies were sent to Alfred Handler (USDA, Gainesville, Florida) from Keng-Hong Tan. The analysis of insertions of the piggyBac transposable element in these specimens revealed that the gene was inserted at identical loci in both B. dorsalis and B. papayae, but at different loci in other clearly distinct species (
That B. dorsalis and B. papayae were not distinct species was consistent with earlier observations that interbreeding between B. papayae, B. carambolae and B. dorsalis results in viable offspring/hybrids (unpublished data c/f
While some authors have refuted this line of argument supporting the view that B. dorsalis and B. papayae are the same species, noting that hybridization between Bactrocera species is easy to achieve in laboratory cages even when using species from different subgenera (
The failure to discover robust diagnostics markers to separate the species within the complex, and indeed the accumulating evidence that supported the idea that at least B. dorsalis and B. papayae were populations of the same species, prompted further studies by
As soon as the paper by
Furthermore, it must also be pointed out that at the same time of this fierce debate, evidence was being accumulated showing the devastation caused by another species, B. invadens as it invaded and spread rapidly across the continent of Africa in the early 2000s, together with the establishment of quarantine barriers by countries that did not harbour B. invadens, even though they harboured B. dorsalis.
The detection of an unknown pest fruit fly in Kenya, 2003, first reported as an unknown species suspected to be of Asian origin and related to the Oriental fruit fly (
One major reason for the need to resolve the taxonomic status of this new pest was to confirm or reject the validity of the quarantine barriers which were established following the B. invadens incursion between importing countries (for example in Asia) where B. dorsalis was endemic and exporting African nations. In addition, an effective fruit fly management programme requires correct identification of the target pest species. In the case of B. invadens, while copious amounts of work have been done in understanding its ecology and biology, its true taxonomic status remained confused despite the availability of an array of modern analytical tools to aid in the identification of the species. For example, using piggyBac gene insertions,
In conjunction with the alarming spread of B. invadens in Africa and doubts cast over its taxonomic status, as well the ongoing failure to resolve the species status of the Asian species, a clear need and opportunity arose for the international fruit fly research community to address the question of species boundaries in the B. dorsalis complex, involving not only B. invadens but also B. dorsalis, B. papayae, B. philippinensis and B. carambolae, all of which rank among the world’s most destructive and highly invasive alien pest species. At the request from member states, the Joint FAO/IAEA Division took on an instrumental role in establishing in 2010 a six-year Coordinated Research Project (CRP) on ‘Resolution of Cryptic Species Complexes of Tephritid Flies to Overcome Constraints to SIT Application and International Trade’. While the first meeting of researchers to coordinate the research programme of this CRP took place in Vienna in 2010, it must be noted that it was during the FAO/IAEA consultants meeting in 2009 (that included Jorge Hendrichs and Keng-Hong Tan) that the CRP was designed.
The objectives of the CRP were not only to resolve the species issues within the B. dorsalis complex but also of other tephritid genera where close species relationships were an issue, including Anastrepha and Ceratitis pest populations or species. Research coordination meetings were held in Vienna, Austria (2010), Brisbane, Australia, (2012), Tucuman, Argentina (2013), and La Reunion, France (2015), where research progress was critically evaluated and follow-up research work-plans developed. A multidisciplinary consensus was finally reached that while there was sufficient evidence confirming the separate species status for B. carambolae, the four species B. dorsalis, B. invadens, B. papayae and B. philippinensis constituted only a single biological species. This culminated in the synonymization of the later three species with B. dorsalis (
The authors would like to thank everyone in the Bactrocera dorsalis complex group in the CRP for the valuable discussions. We are also grateful to Alfred M. Handler (USDA, Gainsville, Florida) for his interest and invaluable assistance in conducting the piggyBac studies on B. papayae. The assistance of technical staff and interest of colleagues (Sai-Tee Tan) in the School of Biological Sciences, Universiti Sains Malaysia (1981–1999) are appreciated. Also thanks to Russell H. Messing (University of Hawaii) for providing the initial stock of the B. dorsaliss.s. to Keng-Hong Tan. The financial support from FAO/IAEA offered to Alvin K.W. Hee through IAEA research contract no. 16066 and Keng-Hong Tan, IAEA research contract no. 16160 is gratefully acknowledged.