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Do mothers really know best? Complexities in testing the preference-performance hypothesis in polyphagous frugivorous fruit flies

Published online by Cambridge University Press:  04 December 2017

A. Birke  and
M. Aluja
A. Birke*
Affiliation:
Clúster Científico y Tecnológico BioMimic®, Instituto de Ecología A.C., Apartado Postal 63, 91070 Xalapa, Veracruz, Mexico
M. Aluja
Affiliation:
Clúster Científico y Tecnológico BioMimic®, Instituto de Ecología A.C., Apartado Postal 63, 91070 Xalapa, Veracruz, Mexico
*
*Author for correspondence Phone: +52-228-8421841, +52-228-8421800 Ext. 4151 Fax: +52-228-8421841 E-mail: andrea.birke@inecol.mx
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Abstract

The preference-performance hypothesis (PPH) has widely been used to explain host exploitation patterns by phytophagous insects. However, this hypothesis often fails in the case of polyphagous species when compared with specialists. One explanation, validated by the information-processing hypothesis (IPH), considers that polyphagous insects are unable to process a large array of cues, which hinders females from distinguishing between high- and low- quality hosts. Here we analyzed Anastrepha ludens female host preference and offspring performance, and tested if neuronal limitations could possibly play a role in the incapacity of the polyphagous A. ludens to make ‘accurate decisions’ and therefore partially explain mismatches related to PPH. Results testing the PPH by correlating female preference to six naturally occurring hosts and its offspring outcomes show that A. ludens females oviposited greater proportions of eggs on fruit according to hierarchical preferences. Infestation level was low in white sapote, the preferential and seemingly putative ancestral host, likely due to sapote defence mechanisms. Pupal weight and adult size were lower when A. ludens larvae developed in guava (conditional host that was artificially infested) and peach, a lower ranked host compared with ‘Marsh’ grapefruit, white sapote, and ‘Manila’ mango (three preferred hosts). Larvae reared in ‘Manzano’ pepper, a low-ranked host, performed better than in peach and guava. Results testing the IPH, show that polyphagous A. ludens females were less accurate when discerning between a non natural host (guava) when compared with a preferred, natural host (grapefruit): error rate was significantly higher, number of oviposited fruit in a 6-h period was extremely low, time searching and ovipositing took longer, and pupae recovery was extremely low. Our findings indicate that both hypotheses tested are complementary and help better understand host use by A. ludens. However, we also discuss the complexity of polyphagy considering other factors such as plant resistance/defence mechanisms which are not fully addressed in both theories tested.

Keywords

frugivorypreference-performance hypothesisneuronal constraints hypothesisplant resistance/defenceDiptera: Tephritidae
Type
Research Papers
Information
Bulletin of Entomological Research , Volume 108 , Issue 5 , October 2018 , pp. 674 - 684
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Copyright
Copyright © Cambridge University Press 2017 

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References

Aluja, M. & Mangan, R. (2008) Fruit fly (Diptera: Tephritidae) host status determination: critical conceptual, methodological, and regulatory considerations. Annual Review of Entomology 53, 473–502.Google Scholar
Aluja, M., Piñero, J., López, M., Ruíz, C., Zúñiga, A., Piedra, E., Díaz-Fleischer, F. & Sivinski, J. (2000 a) New host plant and distribution records in Mexico for Anastrepha spp., Toxotrypana curvicauda Gerstacker, Rhagoletis zoqui Bush, Rhagoletis sp., and Hexachaeta sp. (Diptera: Tephritidae). Proceedings of the Entomological Society of Washington 102, 802–815.Google Scholar
Aluja, M., Piñero, J., Jácome, I., Díaz-Fleischer, F. & Sivinski, J. (2000 b) Behavior of flies in the genus Anastrepha (Trypetinae: Toxotrypanini). pp. 375–406 in Aluja, M. & Norrbom, A. (Eds) Fruit Flies (Diptera: Tephritidae): Phylogeny and Evolution of Behavior. Boca Raton, Florida, CRC.Google Scholar
Aluja, M., Jácome, I. & Macías-Ordoñez, R. (2001) Effect of adult nutrition on male sexual performance in four tropical fruit fly species of the genus Anastrepha (Diptera: Tephritidae). Journal of Insect Behavior 14, 759–775.Google Scholar
Aluja, M., Birke, A., Ceymann, M., Guillén, L., Arrigoni, E., Baumgartner, D., Pascacio, C. & Samietz, J. (2014 a) Agroecosystem resilience to invasive insect species expanding their geographical range in response to global climate change. Agriculture, Ecosystem and Environment 186, 54–63.Google Scholar
Aluja, M., Arredondo, J., Díaz-Fleischer, F., Birke, A., Rull, J., Niogret, J. & Epsky, N. (2014 b) Susceptibility of 15 mango (Mangifera indica) cultivars to the attack by Anastrepha ludens and A. obliqua and the role of underdeveloped fruit as pest reservoirs: management implications. Journal of Economic Entomology 101, 375–388.Google Scholar
Association of Official Analytical Chemists (AOAC) (1975) Official Methods of Analysis. 12th edn. Washington, DC, Association of Official Analytical Chemists.Google Scholar
Balagawi, S., Vijaysegaran, S., Drew, R.A.I. & Raghu, S. (2005) Influence of fruit traits on oviposition preference and offspring performance of Bactrocera tryoni (Froggatt) (Diptera: Tephritidae) on three tomato (Lycopersicon lycopersicum) cultivars. Australian Journal of Entomology 44, 97–103.Google Scholar
Balagawi, S., Drew, R.A. & Clarke, A.R. (2013) Simultaneous tests of the preference-performance and phylogenetic conservatism hypotheses: is either theory useful? Arthropod-Plant Interactions 7, 299–313.Google Scholar
Behar, A., Jurkevitch, E. & Yuval, B. (2008) Bringing back the fruit into fruit fly–bacteria interactions. Molecular Ecology 17, 1375–1386.Google Scholar
Bernays, E. (2001) Neuronal limitations in phytophagous insects: implications for diet breadth and evolution of host affiliations. Annual Review of Entomology 46, 703–727.Google Scholar
Bernays, E., Singer, M.S. & Rodrigues, D. (2004) Foraging in nature: foraging efficiency and attentiveness in caterpillars with different diet breadths. Ecological Entomology 29, 389–397.Google Scholar
Bernays, E.A. & Funk, D. (1999) Specialists make faster decisions than generalists: experiments with aphids. Proceedings of the Royal Society of London 266, 1–6.Google Scholar
Birke, A. & Aluja, M. (2011) Anastrepha ludens and A. serpentina (Diptera: Tephritidae) do not infest Psidium guajava (Myrtaceae), but A. obliqua occasionally shares this resource with A. striata in nature. Journal of Economic Entomology 104, 1204–1211.Google Scholar
Birke, A., Guillén, L., Midgarden, D. & Aluja, M. (2013) Fruit flies, Anastrepha ludens (Loew), A. obliqua (Macquart) and A. grandis (Macquart) (Diptera: Tephritidae): three pestiferous tropical fruit flies that could potentially expand their range to temperate areas. pp. 192–213 in Peña, J. (Ed.) Potential Invasive Pests of Agricultural Crops. Wallingford, UK, CABI International.Google Scholar
Birke, A., Acosta, E. & Aluja, M. (2015) Limits to the host range of the highly polyphagous tephritid fruit fly Anastrepha ludens in its natural habitat. Bulletin of Entomological Research 105, 743–753.Google Scholar
Clark, K.E., Hartley, S.E. & Johnson, S.N. (2011) Does mother know best? The preference–performance hypothesis and parent–offspring conflict in aboveground–belowground herbivore life cycles. Ecological Entomology 36, 117–124.Google Scholar
Clarke, A.R. (2016) Why so many polyphagous fruit flies (Diptera: Tephritidae): a further contribution to the ‘generalism’ debate. Biological Journal of the Linnaean Society 120, 245–257.Google Scholar
Conover, W.J. & Iman, R.I. (1981) Rank transformations as a bridge between parametric and nonparametric statistics. American Statistics 35, 124–133.Google Scholar
Courtney, S. (1988) If it's not coevolution, it must be predation? Ecology 69, 910–911.Google Scholar
Cunningham, J.P., Carlsson, M.A., Tommaso, F.V., Dekker, T. & Clarke, A.R. (2016) Ripening volatiles are key attractant stimuli enabling resource specialism in generalist fruit flies. Journal of Chemical Ecology 42, 931–940.Google Scholar
Craig, T.P. & Itami, J.K. (2008) Evolution of preference and performance relationships. pp. 20–28 in Tilmon, K. (Ed.) Specialization, Speciation, and Radiation. The Evolutionary Biology of Herbivorous Insects. Berkeley, US, University of California Press.Google Scholar
Dethier, V.G. (1954) Evolution of feeding preferences in phytophagous insects. Evolution 8, 33–54.Google Scholar
Duyck, P.F., David, P., Junod, G., Brunel, C., Dupont, R. & Quilici, S. (2006) Importance of competition mechanisms in successive invasions by polyphagous tephritids in La Réunion. Ecology 87, 1770–1780.Google Scholar
Egan, S.P. & Funk, D.J. (2006) Individual advantages to ecological specialization: insights on cognitive constraints from three conspecific taxa. Proceedings of the Royal Society of London B: Biological Sciences 273, 843–848.Google Scholar
Ehrlich, P.R. & Raven, H. (1964) Butterflies and plants: a study in coevolution. Evolution 18, 586–608.Google Scholar
Erbout, N., De Meyer, M., Vangestel, C. & Lens, L. (2009) Host plant toxicity affects developmental rates in a polyphagous fruit fly: experimental evidence. Biological Journal of the Linnean Society 97, 728–737.Google Scholar
Fitt, G.P. (1986 a) The roles of adult and larval specialisations in limiting the occurrence of five species of Dacus (Diptera: Tephritidae) in cultivated fruits. Oecologia 69, 101–109.Google Scholar
Fitt, G.P. (1986 b) The influence of a shortage of hosts on the specificity of oviposition behaviour in species of Dacus (Diptera: Tephritidae). Physiological Entomology 11, 133–143.Google Scholar
Fox, G.A., Negrete-Yankelevich, S. & Sosa, V.J. (Eds) (2015) Ecological Statistics: Contemporary Theory and Application. Oxford, UK, Oxford University Press.Google Scholar
Greany, P.D., Styer, S.C., Davis, P.L., Shaw, P.E. & Chambers, D.L. (1983) Biochemical resistance of citrus to fruit flies. Demonstration and elucidation of resistance to the Caribbean fruit fly, Anastrepha suspensa. Entomologia Experimentalis et Applicata 34, 40–50.Google Scholar
Gripenberg, S., Mayhew, P.J., Parnell, M. & Roslin, T. (2010) A meta-analysis of preference–performance relationships in phytophagous insects. Ecology Letters 13, 383–393.Google Scholar
Guillen, L., Adaime, R., Birke, A., Velázquez, O., Angeles, G., Ortega, F. & Aluja, M. (2017) Effect of resin ducts and sap content on infestation and development of immature stages of Anastrepha obliqua and Anastrepha ludens (Diptera: Tephritidae) in four mango (Sapindales: Anacardiaceae) cultivars. Journal of Economic Entomology 110, 719–730.Google Scholar
Hafsi, A., Facon, B., Ravigné, V., Chiroleu, F., Quilici, S., Chermiti, B. & Duyck, P.F. (2016) Host plant range of a fruit fly community (Diptera: Tephritidae): does fruit composition influence larval performance? BMC Ecology 16, 40. doi: 10.1186/s12898-016-0094-8.Google Scholar
Jácome, I., Aluja, M. & Liedo, P. (1999) Impact of adult diet on demographic and population parameters of the tropical fruit fly Anastrepha serpentina (Diptera: Tephritidae). Bulletin of Entomological Research 89, 165–175.Google Scholar
Jaenike, J. (1978) On optimal oviposition behavior in phytophagous insects. Theoretical Population Biology 14, 350–356.Google Scholar
Jaenike, J. (1990) Host specialization in phytophagous insects. Annual Review of Ecology and Systematics 21, 243–247.Google Scholar
Leyva, J.L., Browning, H.W. & Gilstrap, F.E. (1991) Development of Anastrepha ludens (Diptera: Tephritidae) in several host fruit. Environmental Entomology 20, 1160–1165.Google Scholar
Loxdale, H.D., Lushai, G. & Harvey, J.A. (2011) The evolutionary improbability of ‘generalism’ in nature, with special reference to insects. Biological Journal of the Linnean Society 103, 1–18.Google Scholar
Montgomery, D.C. (2006) Diseño de Análisis de Experimentos. Mexico City, Mexico, Limusa Wiley.Google Scholar
Muthuthantri, S. & Clarke, A.R. (2012) Five commercial citrus are poor hosts of the polyphagous fruit fly, Bactrocera tryoni (Froggatt) (Diptera: Tephritidae) in laboratory studies. Australian Journal of Entomology 51, 289–298.Google Scholar
Norrbom, A.L. (2003) Host Plant Database for Anastrepha and Toxotrypana (Diptera: Tephritidae: Toxotrypanini). Washington, DC, Diptera Data Dissemination Disk (CD-ROM), North American Dipterist's Society.Google Scholar
Opp, S.B. & Prokopy, R.J. (1986) Approaches and methods for direct behavioral observation and analysis of plant-insect interactions. pp. 1–22 in Miller, J.R. & Miller, T.A. (Eds) Insect-Plant Interaction. New York, US, Springer.Google Scholar
Padilla, R. (2003) Cosecha y postcosecha. pp. 134–144 in González, E., Padilla, J.S., Reyes, L., Perales, M.A. & Esquivel, F. (Eds) Guayaba: su Cultivo en México. México, INIFAP.Google Scholar
Papachristos, D.P. & Papadopoulos, N.T. (2009) Are citrus species favourable hosts for the Mediterranean fruit fly? A demographic perspective. Entomologia Experimentalis et Applicata 132, 1–12.Google Scholar
Pascacio-Villafán, C., Lapointe, S., Williams, T., Sivinski, J., Niedz, R. & Aluja, M. (2014) Mixture-amount design and response surface modeling to assess the effects of flavonoids and phenolic acids on developmental performance of Anastrepha ludens. Journal of Chemical Ecology 40, 297–306.Google Scholar
Pascacio-Villafán, C., Williams, T., Birke, A. & Aluja, M. (2016) Nutritional and non-nutritional food components modulate phenotypic variation but not physiological trade-offs in an insect. Scientific Reports 6, 29413. doi: 10.1038/srep29413.Google Scholar
Plummer, C.C., McPhail, M. & Monk, J.W. (1941) The yellow chapote: a native host of the Mexican fruit fly. United States Department of Agriculture Technical Bulletin 755, 1–12.Google Scholar
Pree, D.J. (1977) Resistance to development of larvae of the apple maggot in crab apples. Journal of Economic Entomology 70, 611–614.Google Scholar
Rashmi, M.A., Verghese, A., Shivashankar, S., Chakravarthy, A.K., Sumathi, M. & Kandakoor, S. (2017) Does change in tannin content in mango (Mangifera indica) fruits influence the extent of fruit fly (Bactrocera dorsalis Hendel) herbivory? Journal of Entomology and Zoology Studies 5, 381–385.Google Scholar
Rattanapun, W., Amornsak, W. & Clarke, A.R. (2009) Bactrocera dorsalis preference for and performance on two mango varieties at three stages of ripeness. Entomologia Experimentalis et Applicata 131, 243–253.Google Scholar
Rattanapun, W., Amornsak, W. & Clarke, A.R. (2010) Is a mango just a mango? Testing within-fruit oviposition site choice and larval performance of a highly polyphagous fruit fly. Arthropod-Plant Interactions 4, 35–44.Google Scholar
Salvatore, A., Borkosky, S., Willink, E. & Bardon, A. (2004) Toxic effects of lemon peel constituents on Ceratitis capitata. Journal of Chemical Ecology 30, 323–333.Google Scholar
Singer, M.S., Rodrigues, D., Stireman, J.O. III & Carriere, Y. (2004) Roles of food quality and enemy-free space in host use by a generalist insect herbivore. Ecology 85, 2747–2753.Google Scholar
Statsoft. (1998). Statistica, Version 5.1. Tulsa, OK, Statsoft.Google Scholar
Tallamy, D.W., Mullin, C.A. & Frazier, J.L. (1999) An alternate route to insect pharmacophagy: the loose receptor hypothesis. Journal of Chemical Ecolology 25, 1987–1997.Google Scholar
Tania, M.L., Brandalha, F. & Zucoloto, F.S. (2004) Selection of oviposition sites by wild Anastrepha obliqua (Macquart) (Diptera: Tephritidae) based on the nutritional composition. Neotropical Entomology 33, 557–562.Google Scholar
Thomas, D.B. (2004) Hot peppers as a host for the Mexican fruit fly Anastrepha ludens (Diptera: Tephritidae). Florida Entomologist 87, 603–608.Google Scholar
Thomas, D.B. (2012) Mexican fruit fly (Diptera: Tephritidae) and the phenology of its native host plant yellow chapote (Rutaceae) in Mexico. Journal of Entomological Science 47, 1–16.Google Scholar
Thompson, J.N. (1988) Coevolution and alternative hypotheses on insect/plant interactions. Ecology 69, 893–895.Google Scholar
Wetzel, W.C. & Strong, D.R. (2015) Host selection by an insect herbivore with spatially variable density dependence. Oecologia 179, 777–784.Google Scholar
Wetzel, W.C., Kharouba, H.M., Robinson, M., Holyoak, M. & Karban, R. (2016) Variability in plant nutrients reduces insect herbivore performance. Nature 539, 425–427.Google Scholar