Effect of host plant chemistry on genetic differentiation and reduction of gene flow among Anastrepha fraterculus (Diptera: Tephritidae) populations exploiting sympatric, synchronic hosts

Environmental Entomology

Volumn 42, Issue 4, 2013, Pages 790-798

  Oroño, Luis ^a,b   Paulin, Laura ^d   Alberti, Andrea C ^d   Hilal, Mirna ^e   Ovruski, Sergio ^a,b   Vilardi, Juan C ^d   Rull, Juan ^c   Aluja, Martin ^c  

^a Universidad Nacional de Chilecito   (Argentina)

^b PLANTA PILOTO DE PROCESOS INDUSTRIALES MICROBIOLÓGICOS PROIMI CONICET   (Argentina)

^c INSTITUTO DE ECOLOGÍA   (Mexico)

^d UNIVERSIDAD DE BUENOS AIRES   (Argentina)

^e UNIVERSIDAD NACIONAL DE TUCUMÁN   (Argentina)

Author keywords

Cryptic species complex; Gene flow; Host mediated differentiation; South American fruit fly

Indexed keywords

ADAPTIVE RADIATION; BIOCHEMICAL COMPOSITION; CRYPSIS; ENTOMOLOGY; FLY; FRUIT; GENE FLOW; GENETIC DIFFERENTIATION; HOST PLANT; KAIROMONE; PHYTOCHEMISTRY; PLANT-HERBIVORE INTERACTION; SECONDARY METABOLITE; SEX PHEROMONE; SPECIALIZATION; SPECIES COMPLEX; SYMPATRY;

PHEROMONE;

ANIMAL; ARGENTINA; ARTICLE; CHEMISTRY; FEMALE; FOOD CHAIN; GENE FLOW; GENETICS; INTERSPERSED REPEAT; PHYSIOLOGY; POLYMERASE CHAIN REACTION; PRUNUS; PSIDIUM; SPECIES DIFFERENTIATION; SYMPATRY; TEPHRITIDAE; WALNUT;

ANIMALS; ARGENTINA; FEMALE; FOOD CHAIN; GENE FLOW; GENETIC SPECIATION; INTERSPERSED REPETITIVE SEQUENCES; JUGLANS; PHEROMONES; POLYMERASE CHAIN REACTION; PRUNUS; PSIDIUM; SYMPATRY; TEPHRITIDAE;

EID: 84881465449     PISSN: 0046225X     EISSN: None     Source Type: Journal    
DOI: 10.1603/EN13020     Document Type: Article

References (68)

1. Alberti, A. C., M. S. Rodriguero, P. Gomez Cendra, B. O. Saidman, and J. C. Vilardi. 2002. Evidence indicating that Argentine populations of Anastrepha fraterculus(Diptera: Tephritidae) belong to a single biological species. Ann. Entomol. Soc. Am. 95: 505-512
2. Alberti, A. C., V. A. Confalonieri, R. O. Zandomeni, and J. C. Vilardi. 2008. Phylogeographic studies on natural populations of the South American fruit ßy, Anastrepha fraterculus(Diptera: Tephritidae). Genetica 132: 1-8
3. Aluja, M., J. Piñero, I. Jácome, F. Díaz-Fleischer, and J. Sivinski. 2000. Behavior of ßies in the genus Anastrepha(Trypetinae: Toxotrypanini), pp. 375-406. In M. Aluja, A. L. Norrbom (eds.). Fruit Flies (Tephritidae): Phylogeny and Evolution of Behavior. CRC, Boca Raton, FL
4. Aluja, M., D. Perez-Staples, R. Macias-Ordoñez, J. Piñero, B. McPheron, and V. Hernández-Ortiz. 2003. Nonhost status of Citrus sinensis cultivar Valencia and C. paradise cultivar Ruby Red to Mexican Anastrepha fraterculus(Diptera: Tephritidae). J. Econ. Entomol. 96: 1693-1703
5. Baker, P. S., A.S.T. Chan, and M. A. Jimeno-Zavala. 1986. Dispersal and orientation of sterile Ceratitis capitata and Anastrepha ludens (Tephritidae) in Chiapas, Mexico. J. Appl. Ecol. 23: 27-38
6. Basso, A., A. Sonvico, L. Quesada-Allue, and F. Manso. 2003. Karyotipic and molecular identi cation of laboratory stocks of the South American fruit ßy Anastrepha fraterculus(Wied) (Diptera: Tephritidae). J. Econ. Entomol. 96: 1237-1244
7. Becerra, J. X. 1997. Insects on plants: Macroevolutionary chemical trends in host use. Science 276: 253-256
8. Berlocher, S. H. 2000. Radiation and divergence in the Rhagoletis pomonella species group: Inferences from allozymes. Evolution 54: 543-557
9. Berlocher, S. H., and J. L. Feder. 2002. Sympatric speciation in phytophagous insects: Moving beyond controversy? Annu. Rev. Entomol. 47: 773-815
10. Bernays, E., and M. Graham. 1988. On the evolution of host speci city in phytophagous arthropods. Ecology 69: 886-892
11. Blair, C. P., R. V. Schlanger, S. E. Diamond, and W. G. Abrahamson. 2010. Nutrition as a facilitator of host-race formation: The shift of a stem-boring beetle to a gall host. Ecol. Entomol. 35: 396-406
12. Bradford, M. M. 1976. A rapid and sensitive method for the quanti cation of micrograms quantities of protein-die binding. Analyt. Biochem. 72: 248-254
13. Bush, G. L. 1969. Sympatric host race formation and speciation in frugivorous ßies of the genus Rhagoletis (Diptera: Tephritidae). Evolution 23: 237-251
14. Cáceres, C., D. F. Segura, M. T. Vera, V. Wornoayporn, J. L. Cladera, P. Teal, P. Sapountzis, K. Bourtzis, A. Zacharopoulou, and A. S. Robinson. 2009. Incipient speciation revealed in Anastrepha fraterculus (Diptera: Tephritidae) by studies on mating compatibility, sex pheromones, hybridisation and cytology. Biol. J. Linn. Soc. 97: 152-165
15. Cardini, C., L. F. Leloir, and J. Chiriboga. 1955. The biosynthesis of sucrose. J. Biol. Chem. 214: 149-155
16. Clarke, A. R., K. F. Armstrong, A. E. Carmichael, J. R. Milne, S. Raghu, G. K. Roderick, and D. K. Yeates. 2004. Invasive phytophagous pests arising through recent tropical evolutionary radiation: The Bactrocera dorsalis complex of fruit ßies. Annu. Rev. Entomol. 50: 293-319
17. Depres, L., J. P. David, and C. Gallet. 2007. The evolutionary ecology of insect resistance to plant chemicals. Trends Ecol. Evol. 22: 298-307
18. Drès, M., and J. Mallet. 2002. Host races in plant-feeding insects and their important in sympatric speciation. Phil. Trans. R. Soc. B 357: 471-492
19. Excoffier, L. 2003. Analysis of population subdivision, pp. 713-750. In D. Balding, M. Bishop, and C. Cannings (eds.), Handbook of Statistical Genetics, 2nd ed. Wiley, Ltd., New York, NY
20. Feder, J. L. 1995. The effects of parasitoids on sympatric host races of Rhagoletis pomonella (Diptera:Tephritidae). Ecology 76: 801-813
21. Feder, J. L., K. Reynolds,W.Go, and E. C. Wang. 1995. Intra and inter-speci c competition and host race formation in the apple maggot ßy, Rhagoletis pomonella (Diptera: Tephritida). Oecology 101: 416-425
22. Ferveur, J. F. 2005. Cuticular hydrocarbons: Their evolution and roles in Drosophila pheromonal communication. Behav. Genet. 35: 279-295
23. Filchak, K. E., J. B. Roethele, amd J. L. Feder. 2000. Natural selection and sympatric divergence in the apple maggot Rhagoletis pomonella. Nature 407: 739-42
24. Fox, L A., and P. A. Morrow. 1981. Specialization: Species property or local phenomenoñScience 211: 887-893
25. Frankham, R., J. D. Ballou, and D. A. Briscoe. 2002. Introduction to conservation genetics. Cambridge University Press, Cambridge, UK
26. Gasperi, G., M. Bonizzoni, L. M. Gomulski, V. Murelli, C. Torti, A. R. Malacrida, and C. R. Guglielmino. 2002. Genetic differentiation, gene ßow and the origin of infestations of the medßy, Ceratitis capitata. Genetica 116: 125-135
27. Glendinning, J. I. 2002. How do herbivorous insects cope with noxious secondary plant compounds in their diet? Entomol. Exp. Applic. 104: 15-25
28. Gross, J., N. E. Fatouros, and M. Hilker. 2004. The signi cance of bottom-up effects for host plant specialization in Chrysomela leaf beetles. Oikos 105: 368-376
29. Hagerman, A. E., and L. G. Butler. 1978. Protein precipitation method for the quantitative determination of tannins. J. Agric. Food Chem. 26: 809-812
30. Heath, R. R., P. J. Landolt, D. C. Robacker, B. D. Dueben, and N. D. Epsky. 2000. Sexual pheromones of tephritid ßies: Clues to unravel phylogeny and behavior, pp. 793-809. In M. Aluja and A. L. Norrbom (eds.)], Fruit Fly (Tephritidae) Phylogeny and Evolution of Behavior. CRC, Boca Raton, FL
31. Hernández-Ortiz, V., J. A. Gómez-Anaya, A. Sánchez, B. A. McPheron, and M. Aluja. 2004. Morphometric analysis of Mexican and South American populations of the Anastrepha fraterculus complex (Diptera: Tephritidae) and recognition of a distinct Mexican morphotype. Bull. Entomol. Res. 94: 487-499
32. Landolt, P. J., and T.W.Phillips. 1997. Host plant inßuences on sex pheromone behavior of phytophagous insects. Annu. Rev. Entomol. 42: 371-91
33. Liang, D., and J. Silverman. 2000. "You are what you eat": Diet modi es cuticular hydrocarbons and nestmate recognition in the Argentine ant, Linepithema humile. Naturwissenschaften 87: 412-416
34. Lynch, M., and B. G. Milligan. 1994. Analysis of population genetic structure whit RAPD markers. Molec. Ecol. 3: 91-99
35. Loxdale, H. D., G. Lushai, and J. A. Harvey. 2011. The evolutionary improbability of ÔgeneralismÕ in nature, with special reference to insects. Biol. J. Linn. Soc. 103: 1-18
36. Malavasi, A., and J. S. Morgante. 1983. Populations genetics of Anastrepha fraterculus (Diptera, Tephritidae) in different host: Genetic differentiations and heterozygosity. Genetica 60: 207-211
37. Mallet, J. 2008. Hybridization, ecological races and the nature of species: Empirical evidence for the ease of speciation. Phil. Trans. R. Soc. B. 363: 2971-2986
38. Mirecki. R., and A. H. Teramura. 1984. Effects of ultraviolet-B irradiance on soybean V. The dependence of plants sensitivity on the photosynthetic photon ßux density during and after leaf expansion. Plant Physiol. 74: 475-480
39. Mopper, S., M. Beck, D. Simberloff, and P. Stiling. 1995. Local adaptation and agents of selection in a mobile insect. Evolution 49: 810-815
40. Nei, M. 1978. Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89: 583-590
41. Norrbom, A. L. 2004. Host plant database for Anastrepha and Toxotrypana (Diptera: Tephritidae: Toxotrypanini). Diptera Data Dissemination Disk 2
42. Ovruski, S., P Schliserman, and M. Aluja. 2003. Native and introduced host plants of Anastrepha fraterculus and Ceratitis capitata (Diptera: Tephritidae) in northwestern Argentina. J. Econ. Entomol. 96: 1108-1118
43. Prokopy, R. B., and D. R. Papaj. 2000. Behavior of ßies of the genera Rhagoletis, Zonosemata, and Carpomya (Trypetinae: Carpomyina), pp. 219-252. In M. Aluja and A. L. Norrbom (eds.), Fruit Flies (Tephritidae): Phylogeny and Evolution of Behavior. CRC, Boca Raton, FL
44. R Development Core Team. 2011. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria
45. Rundle, H. D., S. F. Chenoweth, P. Doughty, and M. W. Blows. 2005. Divergent selection and the evolution of signal traits and mating preferences. PLoS Biol. 3: 1988-1995
46. Thomas, D. B. 2003. Reproductive phenology of the Mexican fruit ßy, Anastrepha ludens (Loew) (Diptera: Tephritidae) in the Sierra Madre Oriental, Northern Mexico. Neotrop. Entomol. 32: 385-397
47. Schliserman, P. 2001. Abundancia estacional de himenó pteros parasitoides de Anastrepha fraterculus y Ceratitis capitata (Dõ'ptera: Tephritidae) en áreas de bosque secundario de la Sierra de San Javier, Tucumán. Tesis de Maestrõ'a, Universidad Nacional de La Rioja, La Rioja, Argentina
48. Schliserman, P. 2005. Dinámica poblacional y estructura de hábitat de Ceratitis capitata y Anastrepha fraterculus (Diptera: Tephritidae) en la ladera Oriental de la Sierra de San Javier, Tucumán. Tesis de Doctorado. Facultad de Ciencias Naturales e IML, Universidad Nacional de Tucumán, Tucumán, Argentina
49. Schliserman, P., S. M. Ovruski, C. Colin, A. Norrbom, and M. Aluja. 2004. First report of Juglans australis (Juglandaceae) as a natural host plant for Anastrepha schultzi(Diptera: Tephritidae) with notes on probable parasitism by Doryctobracon areolatus, D. brasiliensis, Opius bellus(Braconidae) and Aganaspis pelleranoi (Figitidae)". Fla. Entomol. 87: 597-599
50. Segura, D. F., M. T. Vera, C. F. Cagnotti, N. Vaccaro, N. de Coll, S. M. Ovruski, and J. L. Cladera. 2006. Relative abundance of Ceratitis capitata and Anastrepha fraterculus(Diptera: Tephritidae) in diverse host species and localities of Argentina. Ann. Entomol. Soc. Am. 99: 70-83
51. Segura, D. F., M. T. Vera, J. Rull, V. Wornoayporn, A. Islam, and A. S. Robinson. 2011. Assortative mating among Anastrepha fraterculus (Diptera: Tephritidae) hybrids from two distinct populations as a possible route to radiation of the fraterculus cryptic species group. Biol. J. Linn. Soc. 102: 346-354
52. Selivon, D., A.L.P. Perondini, and J. S. Morgante. 2005. A genetic-morphological characterization of two cryptic species of the Anastrepha fraterculus complex. (Diptera: Tephritidae). Ann. Entomol. Soc. Am. 98: 367-381
53. Smadja, C., and R. K. Butlin. 2009. On the scent of speciation: The chemosensory system and its role in premating isolation. Heredity 101: 77-97
54. Smith-Caldas, M.R.B., B. A. McPheron, J. G. Silva, and R. A. Zucchi. 2001. Phylogenetic relationships among species of the fraterculus group (Anastrepha: Diptera: Tephritidae) inferred from DNA sequences of mitochondrial cytochrome oxidase 1. Neotrop. Entomol. 30: 565-573
55. StatSoft, Inc. 2004. STATISTICA (data analysis software system), version 7. www.statsoft.com
56. Steck, G. J. 1991. Biochemical systematics and population genetic structure of Anastrepha fraterculus and related species (Diptera: Tephritidae). Ann. Entomol. Soc. Am. 84: 10-28
57. Steck, G. J., and W. S. Sheppard. 1993. Mitochondrial DNA variation in Anastrepha fraterculus, pp. 9-14. In M. Aluja and P. Liedo (eds.), Fruit Flies Biology and Management. Springer, New York, NY
58. Stennett, M. D., and W. J. Etges. 1997. Premating isolation is determined by larval rearing substrates in cactophilic Drosophila mojavensis. III. Epicuticular hydrocarbon variation is determined by use of different host plants in Drosophila mojavensis and Drosophila arizonae. J. Chem. Ecol. 23: 2803-2824
59. Swain, T., and W. E. Hillis. 1959. The phenols constituents of Prunnus domestica I. The quantitative analysis of phenolics constituents. J. Sci. Food Agric. 10: 63-68
60. Symonds, M. R., and M. A. Elgar. 2008. The evolution of pheromone diversity. Trends Ecol. Evol 23: 220-228
61. Vekemans, X., T. Beauwens,M.Lemaire, and I. Roldan-Ruiz. 2002. Data from ampli ed fragment length polymorphism(AFLP) markers show indication of size homoplasy and of a relationship between degree of homoplasy and fragment size. Molec. Ecol. 11: 139-151
62. Venables, W. N., and B. D. Ripley. 2002. Modern applied statistics with S, 4th ed. Springer, New York, NY. (ISBN: 0-387-95457-0
63. Vera, M. T., C. Cáceres, V. Wornoayporn, A. Islam, A. S. Robinson, M. H. de la Vega, J. Hendrichs, and J. P. Cayol. 2006. Mating incompatibility among populations of the South American fruit ßy Anastrepha fraterculus (Diptera: Tephritidae). Ann. Entomol. Soc. Am. 99: 387-397
64. Xie, X., A. Michel, D. Schwarz, J. Rull, S. Velez, A. Forbes, M. Aluja, and J. L. Feder. 2008. Radiation and divergence in the Rhagoletis pomonella species Group: Inferences from DNA sequence data. J. Evol. Biol. 21: 900-913
65. Zhivotovsky, L. A. 1999. Estimating population structure in diploids with multilocus dominant DNA makers. Molec. Ecol. 8: 907-913
66. Zietkiewicz, E., A. Rafalski, and D. Labuda. 1994. Genome ngerprinting by simple sequence repeats (SSR)-anchored polymerase chain reaction ampli cation. Genomics 20: 176-183
67. Zucchi, R. A. 2000. Taxonomõ'a, pp. 13-24. In A. Malavasi and R. A. Zucchi (eds.), Moscas-das-Frutas de Importância Econômica no Brasil. Conhecimento Básico e Aplicado. Holos Editora, Riberão Preto, Brasil
68. Zvereva, E. L., O. Y. Kruglova, and M. V. Kozlov. 2010. Drivers of host plant shifts in the leaf beetle Chrysomela lapponica: Natural enemies or competitioñEcol. Entomol. 35: 611-622