ANRV330-EN53-24 ARI 2 November 2007 18:52 Fruit Fly (Diptera: Tephritidae) Host Status Determination: Critical Conceptual, Methodological, and Regulatory Considerations∗ Martın´ Aluja1 and Robert L. Mangan2 1Instituto de Ecologıa,´ A.C., Xalapa, Veracruz, Mexico;´ email: [email protected] 2Kika de la Garza ARC, USDA-ARS, Weslaco, Texas; email: [email protected] Annu. Rev. Entomol. 2008. 53:473–502 Key Words First published online as a Review in Advance on host plant, oviposition behavior, host range evolution, quarantine September 17, 2007 pest, risk analysis, systems approach The Annual Review of Entomology is online at ento.annualreviews.org Abstract This article’s doi: Although fruit fly host status determination/designation lies at the 10.1146/annurev.ento.53.103106.093350 heart of strategic decisions on national and international trade of Copyright c 2008 by Annual Reviews. fruit and vegetables, all attempts thus far to define host plant sta- All rights reserved tus have been contentious and as a result long-standing disputes 0066-4170/08/0107-0473$20.00 between commercial partners throughout the world have lingered ∗ by U.S. Department of Agriculture on 04/23/08. For personal use only. The U.S. Government has the right to retain a over decades. Part of the problem is that too little effort has been nonexclusive, royalty-free license in and to any devoted to understanding the underlying mechanisms involved in copyright covering this paper. host plant use by fruit flies and that instead economic and political Annu. Rev. Entomol. 2008.53:473-502. Downloaded from arjournals.annualreviews.org interests usually prevail. Here we review the most important evolu- tionary, biological, ecological, physiological, and behavioral aspects that drive host use by fruit flies, and then construct a flow diagram rooted in these fundamentals that outlines a series of steps and def- initions to determine if a particular fruit or vegetable (and cultivars thereof) is a natural host, or a conditional (potential, artificial) host, or a nonhost. Along the way, we incorporate risk analysis considera- tions and propose that the underlying complexity determining host plant utilization by fruit flies requires a flexible systems approach ca- pable of realistically dealing with fly/host/environment/geographic variability on a case-by-case basis. 473 ANRV330-EN53-24 ARI 2 November 2007 18:52 INTRODUCTION lined system designed to reach science-based decisions on fruit fly host designations. Fruit flies (Diptera: Tephritidae) are among Systems approach: the most important pests worldwide because integration of pre- of their direct economic impact (i.e., fe- EVOLUTIONARY and postharvest male oviposition and larval feeding render CONSIDERATIONS OF HOST practices, from the fruit/vegetables unmarketable) and the strict USE BY TEPHRITID FLIES production of a quarantine restrictions imposed by many commodity to its Overview of Broad Patterns Involved distribution and countries to curtail their entry (1, 31, 64). commercialization, A critical component when trying to assess The evolutionary pathway leading to special- that cumulatively the risk of introductions into a country or ized herbivory is a complex one and the fac- meet predetermined an entire region is the status of a given tors shaping host plant use are highly diverse, requirements for quarantine security fruit/vegetable species (and cultivars thereof ) with patterns spanning from extreme conser- as a host of a particular fruit fly species (3, vatism (175, 182, and references therein) to Natural host: fruit or vegetable 82). Given the underlying biological complex- extreme plasticity (57, 58). Tephritid conser- unequivocally found ity/conditionality of fruit fly host use and the vatism is exemplified by the large subfamily infested under totally economic and political impact of the issue of Tephritinae, which is almost exclusively asso- natural field host plant status determination/designation ciated with plants within the Asteraceae (52). conditions (i.e., at the international level, there is an urgent But there is also evidence for rapid host range nothing is manipulated) need for a solid conceptual and methodolog- evolution, with related insects attacking a wide ical framework that can aid scientists, regula- range of unrelated plants (7, 154). tory officials, policy makers, politicians, and In broad terms, two principal driving stakeholders throughout the world in solving forces guide host range evolution: phyto- current and future disputes over the status of chemical coevolution between plants and her- particular plants as fruit fly hosts. bivores (47) and selective pressure by gen- Here we analyze the causes of confusion eralist natural enemies (19, 22, 87, 158). and complexity involving fruit fly host de- Which selective forces played a more impor- termination and ultimately agricultural risk, tant role in the case of tephritid flies is open including, among others, (a) the evolution to debate. Ancestral tephritids most proba- of fruit fly/host plant relationships and the bly evolved from a saprophagous to a phy- behavioral mechanisms related to host find- tophagous lifestyle (43). Currently, most fruit ing and utilization; (b) conditional infestation flies specialize in flowers and fruit structures based on the physiological (motivational) state that frequently lack the plants’ characteristic of the fly; and (c) conditional infestation based secondary chemistry (112). Furthermore, it by U.S. Department of Agriculture on 04/23/08. For personal use only. on the state of the host. We propose that the has been argued that domesticated fruit were underlying complexity/conditionality that de- selected on the basis of their low toxicity to Annu. Rev. Entomol. 2008.53:473-502. Downloaded from arjournals.annualreviews.org termines host ranges requires a flexible sys- vertebrates (84) and that artificial selection tems approach capable of realistically dealing for increased human palatability also low- with fly/host/environment/geographic vari- ered the levels of chemical defenses in com- ability on a case-by-case basis. We construct mercially grown fruit (80). Additionally, Fitt a flow diagram (Figure 1) that proposes a (58) pointed out that as fruit ripen, defen- series of steps and definitions to determine sive compounds disappear. Conversely, some if a particular fruit or vegetable (and culti- fruit fly species feed on seed tissue that may vars thereof ) is a natural host, or alternatively be more toxic than the pulp, and in the case (non-natural host), if it should be considered a of pulp, there is evidence that some fruit re- conditional (potential, artificial) host or a non- main highly toxic to larvae (see below). For host. We finish by outlining promising areas example, in the case of flies within Anastrepha, of research that could help solidify a stream- primitive species such as A. cordata, A. hamata, 474 Aluja · Mangan ANRV330-EN53-24 ARI 2 November 2007 18:52 Monophagous Evolutionary background, Stenophagous life history, ecology, behavior, Oligophagous physiology, and biogeography Polyphagous Univoltine Multivoltine Monitoring of adult populations and extensive field sampling to gather evidence of natural field infestation Poor Natural host Non-natural host Good Bioassays under Field cages with entire fruit-bearing trees forced artificial Enclosed fruit-bearing branches Additional Risk analysis Quarantine conditions Laboratory cages field and systems treatment research approach Inability to Life cycle completion complete life cycle Natural factors Conditional host (potential or artificial) Nonhost Monitoring/risk analysis factors Manipulated conditions Economic/political/regulatory No quarantine Additional Risk analysis Economic, Quarantine implications action needed, field and systems political, treatment but screening research approach and Research events to detect regulatory mutations concerns Trade restrictions recommended No fertile adult development Figure 1 Flow chart indicating proposed steps for fruit fly host status determination/designation. The entire approach is rooted in the fundamentals of the system, i.e., the evolutionary background of host plant by U.S. Department of Agriculture on 04/23/08. For personal use only. associations, life-history parameters, ecology, physiology, and most importantly behavior. When quarantine systems are based on a systems approach, the entire system should be continuously evaluated by resampling and reanalyzing the components to improve security. Annu. Rev. Entomol. 2008.53:473-502. Downloaded from arjournals.annualreviews.org A. crebra, and their closely related relatives The other argument, that host ranges evolve (flies in the sister group Toxotrypana) spe- because of the selective advantages of mov- cialize on seeds or associated tissue of and ing to hosts that provide shelter from natu- attack latex-producing plants (e.g., Apocy- ral enemies, has not been formally tested, al- naceae, Asclepiadaceae, and Sapotaceae). In though Feder (53) provided evidence that, at contrast, some derived species (e.g., fratercu- least in the case of the apple maggot (Rhago- lus group) feed almost exclusively on fruit pulp letis pomonella), a shift from native hawthorns and are highly polyphagous (7, 9). Species to introduced apples did allow the frugivore such as A. ludens (also within the highly de- to gain enemy-free space. rived fraterculus group) have retained the abil- According to Zwolfer¨ (182) fruit flies arose ity to feed on both types of substrates (9). in the