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Random Mating among Anastrepha ludens (Diptera: Tephritidae) Adults of Geographically Distant and Ecologically Distinct Populations in Mexico

Published online by Cambridge University Press:  09 December 2008

M. Aluja ,
J. Rull ,
D. Pérez-Staples ,
F. Díaz-Fleischer  and
J. Sivinski
M. Aluja*
Affiliation:
Instituto de Ecología, A.C., Apartado Postal 63, C.P. 91000Xalapa, Veracruz, Mexico
J. Rull
Affiliation:
Instituto de Ecología, A.C., Apartado Postal 63, C.P. 91000Xalapa, Veracruz, Mexico
D. Pérez-Staples
Affiliation:
INBIOTECA, Universidad Veracruzana, Apartado Postal 250, C.P. 91090Xalapa, Veracruz, Mexico
F. Díaz-Fleischer
Affiliation:
INBIOTECA, Universidad Veracruzana, Apartado Postal 250, C.P. 91090Xalapa, Veracruz, Mexico
J. Sivinski
Affiliation:
Center for Medical, Agricultural & Veterinary Entomology, 1600/1700SW 23rdGainesville, Florida32608, USA
*
*Author for correspondence Fax: +52 (228) 8421800 Ext. 4115 E-mail: [email protected]
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Abstract

The Mexican fruit fly Anastrepha ludens (Loew) (Diptera: Tephritidae) is a polyphagous pestiferous insect with a geographical range encompassing highly variable environmental conditions. Considering that cryptic species have been recently found among South American representatives of the same taxonomic group as A. ludens, we tested whether or not some populations of A. ludens have evolved assortative mating as an isolating mechanism that maintains intrapopulation genetic differences and behavioral adaptations to local conditions. Males and females stemming from widely separated locations with similar environmental conditions and males and females stemming from populations within individual-flight range, but collected in different hosts (a native and an exotic one), mated randomly amongst themselves when placed in a field cage. Despite the fact that sibling males and females from two distinct populations also mated randomly amongst themselves, siblings engaged in significantly longer copulations than non-siblings, indicating that perhaps adults discriminated mates with similar genetic compositions. Our results have important practical implications as A. ludens is the most devastating pest of citrus in Mexico and Central America, and large-scale releases of sterile flies are used to control it.

Keywords

Anastrepha ludensassortative matingreproductive isolationsib-matingsterile insect techniquecitrus
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 99 , Issue 2 , April 2009 , pp. 207 - 214
Copyright
Copyright © 2008 Cambridge University Press

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References

Aluja, M. (1993) Manejo Integrado de la Mosca de la Fruta. 241 pp. Mexico D.F., Mexico, Editorial Trillas.Google Scholar
Aluja, M. (1994) Bionomics and management of Anastrepha. Annual Review of Entomology 39, 155–178.CrossRefGoogle Scholar
Aluja, M. & Mangan, R.L. (2008) Fruit Fly (Diptera: Tephritidae) host status determination: Critical conceptual, methodological, and regulatory considerations. Annual Review of Entomology 53, 473–502.CrossRefGoogle ScholarPubMed
Aluja, M., Cabrera, M., Rios, E., de la Rosa, G., Guillen, J. & Hendrichs, J. (1987) Natural host plant survey of economically important fruit flies (Diptera: Tephritidae) of Chiapas, Mexico. Florida Entomologist 70, 329–338.CrossRefGoogle Scholar
Aluja, M., Celedonio-Hurtado, H., Liedo, P., Cabrera, M., Castillo, F., Guillén, J. & Rios, E. (1996) Seasonal population fluctuations and ecological implications for management of Anastrepha fruit flies (Diptera: Tephritidae) in commercial mango orchards in Southern Mexico. Journal of Economic Entomology 89, 654–667.Google Scholar
Aluja, M., Piñero, J., Jácome, I., Díaz-Fleischer, F. & Sivinski, J. (2000) Behavior of flies in the genus Anastrepha (Trypteinae: Toxotrypanini). pp. 375–408in Aluja, M. & Norrbom, A.L. (Eds) Fruit Flies (Tephritidae): Phylogeny and Evolution of Behavior. Boca Raton, FL, CRC Press.Google Scholar
Aluja, M., Jacome, I. & Macias-Ordoñez, R. (2001) Effect of adult nutrition on male sexual performance in four neotropical fruit fly species of the genus Anastrepha (Diptera: Tephritidae). Journal of Insect Behavior 14, 759–775.CrossRefGoogle Scholar
Aluja, M., Rull, J., Sivinski, J., Díaz-Fleisher, F., Norrbom, A.L., Wharton, R.A., López, M. & Macías-Ordoñez, R. (2003) Fruit flies of the genus Anastrepha (Diptera: Tephritidae) and associated native parasitoids (Hymenoptera) in the tropical rainforest biosphere reserve of Montes Azules, Chiapas, Mexico. Environmental Entomology 32, 1377–1385.CrossRefGoogle Scholar
Aluja, M., Pérez-Staples, D., Sivinski, J., Sánchez, A. & Piñero, J.Effects of male condition on fitness in two tropical tephritid flies with contrasting life histories. Animal Behaviour, in press (doi: 10.1016/j.anbehav.2008.08.020).Google Scholar
An, X., Tebo, M., Song, S., Frommer, M. & Raphael, K.A. (2004) The cryptochrome (cry) gene and a mating isolation mechanism in tephritid fruit flies. Genetics 168, 2025–2036.Google Scholar
Aspbury, A.S & Gabor, C.R. (2004) Discriminating males alter sperm production between species. Proceedings of the National Academy of Sciences 101, 15970–15973.CrossRefGoogle ScholarPubMed
Berlocher, S.H. & Feder, J.L. (2002) Sympatric speciation in phytophagous insects: Moving beyond controversy? Annual Review of Entomology 47, 773–815.CrossRefGoogle ScholarPubMed
Birke, A., Aluja, M., Greany, P., Bigurra, E., Pérez-Staples, D. & McDonald, R. (2006) Long aculeus and behavior of Anastrepha ludens renders gibberellic acid ineffective as an agent to reduce ‘Ruby Red’ grapefruit susceptibility to the attack of this pestiferous fruit fly in commercial citrus orchards. Journal of Economic Entomology 99, 1184–1193.CrossRefGoogle Scholar
Cayol, J.P. (2000) Changes in sexual behaviour and life history traits of tephritid species caused by mass-rearing processes. pp. 843–860in Aluja, M. & Norrbom, A.L. (Eds) Fruit Flies (Tephritidae): Phylogeny and Evolution of Behavior. Boca Raton, FL, CRC Press.Google Scholar
Cayol, J.P., Coronado, P. & Taher, M. (2002) Sexual compatibility in Medfly (Diptera: Tephritidae) from different origins. Florida Entomologist 85, 51–57.Google Scholar
Celedonio-Hurtado, H., Aluja, M. & Liedo, P. (1995) Adult population fluctuations of Anastrepha species (Diptera: Tephritidae) in tropical orchard habitats of Chiapas, Mexico. Environmental Entomology 24, 861–869.CrossRefGoogle Scholar
Dambroski, H.R., Linn, C., Berlocher, S.H., Forbes, A., Roelofs, W. & Feder, J.L. (2005) The genetic basis of fruit odor discrimination in Rhagoletis flies and its significance for sympatric host shifts. Evolution 59, 1953–1964.Google ScholarPubMed
Díaz-Fleischer, F. & Aluja, M. (2003) Clutch size in frugivorous insects as a function of host firmness: the case of the tephritid fly Anastrepha ludens. Ecological Entomology 28, 268–277.CrossRefGoogle Scholar
Dres, M. & Mallet, J. (2002) Host races in plant-feeding insects and their importance in sympatric speciation. Philosopical Transactions of the Royal Society London 357, 471–492.CrossRefGoogle ScholarPubMed
Eberhard, W.G. (1996) Female Control: Sexual Selection by Cryptic Female Choice. 472 pp. Princeton, NJ, Princeton University Press.Google Scholar
Eberhard, W.G. & Cordero, C. (1995) Sexual selection by cryptic female choice on male seminal products: a new bridge between sexual selection and reproductive physiology. Trends in Ecology and Evolution 10, 493–496.CrossRefGoogle ScholarPubMed
Feder, J.L. & Filchak, K. (1999) It's about time: the evidence for host plant-mediated selection in the apple maggot fly, Rhagoletis pomonella, and its implications for fitness trade-offs in phytophagous insects. Entomologia Experimentalis et Applicata 91, 211–225.CrossRefGoogle Scholar
Feder, J.L., Opp, S., Wlazlo, B., Reynolds, K., Go, W. & Spisak, S. (1994) Host fidelity is an effective pre-mating barrier between sympatric races of the apple maggot fly. Proceedings of the National Academy of Sciences 91, 7990–7994.CrossRefGoogle Scholar
Field, S.A., Taylor, P.W. & Yuval, B. (1999) Sources of variability in copula duration of Mediterranean fruit flies. Entomologia Experimentalis et Applicata 92, 271–276.CrossRefGoogle Scholar
Heath, R.R., Landolt, P.J., Robacker, D.C., Dueben, B. & Epsky, N.D. (2000) Sexual pheromones of tephritid flies: Clues to unravel phylogeny and behaviour. pp. 793–810in Aluja, M. & Norrbom, A.L. (Eds) Fruit Flies (Tephritidae): Phylogeny and Evolution of Behavior. Boca Raton, FL, CRC Press.Google Scholar
Hernández-Ortiz, V., Gómez-Amaya, J.A., Sánchez, A., McPheron, B.A. & Aluja, M. (2004) Morphometric analysis of Mexican and South American populations of the Anastrepha fraterculus complex (Diptera: Tephritidae) and recognition of a distinct Mexican morphotype. Bulletin of Entomological Research 94, 487–499.Google Scholar
Höglund, J. & Alatalo, R.V. (1995) Leks. 248 pp. Princeton, NJ, Princeton University Press.CrossRefGoogle Scholar
Howard, D.J. (1999) Conspecific sperm and pollen precedence and speciation. Annual Review of Ecology and Systematics 30, 109–132.CrossRefGoogle Scholar
Linn, C., Feder, J.L., Nojima, S., Dambroski, H.R., Berlocher, S.H. & Roeloefs, W. (2003) Fruit odor discrimination and sympatric host race formation in Rhagoletis. Proceedings of the National Academy of Sciences 100, 11,490–11,493.Google Scholar
Meza-Hernández, J.S. & Díaz-Fleischer, F. (2006) Comparison of sexual compatibility between laboratory and wild Mexican fruit flies under laboratory and field conditions. Journal of Economic Entomology 99, 1979–1986.Google Scholar
Morrow, J., Scott, L., Congdon, B., Yeates, D., Frommer, M. & Sved, J. (2000) Close genetic similarity between two sympatric species of tephritid fruit fly reproductively isolated by mating time. Evolution 54, 899–910.Google Scholar
Norrbom, A.L., Zucchi, R.A. & Hernández-Ortiz, V. (2000) Phylogeny of the genera Anastrepha and Toxotrypana (Trypetinae: Toxotrypanini) based on morphology. pp. 375–406in Aluja, M. & Norrbom, A.L. (Eds) Fruit Flies (Tephritidae): Phylogeny and Evolution of Behavior. Boca Raton, NJ, CRC Press.Google Scholar
Orozco-Dávila, D., Hernández, R., Meza, S. & Domínguez, J. (2007) Sexual competitiveness and compatibility between mass-reared sterile flies and wild populations of Anastrepha ludens (Diptera: Tephritidae) from different regions in Mexico. Florida Entomologist 90, 19–26.Google Scholar
Pérez-Staples, D. & Aluja, M. (2004) Anastrepha striata (Diptera: Tephritidae) females mated to virgin males live longer. Annals of the Entomological Society of America 97, 1336–1341.Google Scholar
Pérez-Staples, D., Prabhu, V. & Taylor, P.W. (2007) Post-teneral protein performance enhances sexual performance of Queensland fruit flies. Physiological Entomology 32, 127–153.CrossRefGoogle Scholar
Pérez-Staples, D., Aluja, M., Macías-Ordóñez, R. & Sivinski, J. (2008a) Reproductive trade-offs from mating with a successful male: the case of the tephritid fly Anastrepha obliqua. Behavioral Ecology and Sociobiology 62, 1333–1340.CrossRefGoogle Scholar
Pérez-Staples, D., Harmer, M.T., Collins, S.R. & Taylor, P.W. (2008b) Potential for pre-release diet supplements to increase the sexual performance and longevity of male Queensland fruit flies. Agricultural and Forest Entomology 10, 255–262.Google Scholar
Pike, N. & Meats, A. (2002) Potential for mating between Bactrocera tryoni (Froggatt) and B. neohumeralis (Hardy) (Diptera: Tephritidae). Australian Journal of Entomology 41, 70–74.CrossRefGoogle Scholar
Rull, J., Brunel, O. & Mendez, M.E. (2005) Mass rearing history negativeley affects mating success of male Anastrepha ludens (Diptera: Tephritidae) reared for the sterile insect technique. Journal of Economic Entomology 98, 1510–1516.CrossRefGoogle ScholarPubMed
Simmons, L.W. (2001) Sperm Competition and Its Evolutionary Consequences in the Insects. 448 pp. Princeton, NJ, Princeton University Press.Google Scholar
Sivinski, J., Burk, T. & Webb, J.C. (1984) Acoustic courtship signals in the Caribbean fruit fly Anastrepha suspensa (Loew). Animal Behaviour 32, 1011–1016.CrossRefGoogle Scholar
Sivinski, J., Aluja, M., Dodson, G.N., Freidberg, A., Headrick, D.H., Kaneshiro, K.Y. & Landolt, P.J. (2000) Topics in the evolution of sexual behavior in tephritidae. pp. 751–792in Aluja, M. & Norrbom, A.L. (Eds) Fruit Flies (Tephritidae): Phylogeny and Evolution of Behavior. Boca Raton, NJ, CRC Press.Google Scholar
Shelly, T.E. & Kennely, S. (2002) Influence of male diet on male mating success and longevity and female remating in the Mediterranean fruit fly (Diptera: Tephritidae) under laboratory conditions. Florida Entomologist 85, 572–579.CrossRefGoogle Scholar
Shelly, T.E., Rendón, P., Hernandez, E., Salgado, S., Mcinnis, D., Villalobos, E. & Liedo, P. (2003) Effects of diet, ginger root oil, and elevation on the mating competitiveness of male Mediterranean fruit flies (Diptera: Tephritidae) from a mass-reared, genetic sexing strain in Guatemala. Journal of Economic Entomology 96, 1132–1141.Google Scholar
Steck, G.J. (1991) Biochemical systematics and population genetic structure of Anastrepha fraterculus and related species (Diptera: tephritidae). Annals of the Entomological Society of America 84, 10–28.CrossRefGoogle Scholar
Thomas, D.B. (2003) Reproductive phenology of the Mexican fruit fly, Anastrepha ludens (Loew) (Diptera: Tephritidae) in the Sierra Madre Oriental, Northern Mexico. Neotropical Entomology 32, 385–397.CrossRefGoogle Scholar
Thomas, D.B. & Loera-Gallardo, J. (1998) Dispersal and longevity of mass-released, sterilized Mexican fruit flies (Diptera: Tephritidae). Environmental Entomology 27, 1045–1052.Google Scholar
Vera, M.T., Cáceres, C., Wornoayporn, V., Islam, A., Robinson, A.S., De la Vega, M.H., Hendrichs, J. & Cayol, J.P. (2006) Mating incompatibility among populations of the South American Fruit Fly Anastrepha fraterculus (Diptera: Tephritidae). Annals of the Entomological Society of America 99, 387–397.CrossRefGoogle Scholar