Testing host-associated differentiation in a quasi-endophage and a parthenogen on native trees

Journal of Evolutionary Biology

Volumn 23, Issue 5, 2010, Pages 945-956

  Dickey, A M ^a   Medina, R F ^a  

^a TEXAS A AND M UNIVERSITY   (United States)

Author keywords

Amplified fragment length polymorphisms; Aphids; Genetic differentiation; Host plant

Indexed keywords

APHID; CATERPILLAR; DECIDUOUS TREE; DIVERGENCE; GENETIC DIFFERENTIATION; HERBIVORE; HOST PLANT; LIFE HISTORY TRAIT; PARTHENOGENESIS; SUBPOPULATION; SYMPATRY;

AMPLIFIED FRAGMENT LENGTH POLYMORPHISM; ANALYSIS OF VARIANCE; ANIMAL; APHID; ARTICLE; BAYES THEOREM; BIOLOGICAL MODEL; CLUSTER ANALYSIS; GENETIC VARIABILITY; GENETICS; HOST PATHOGEN INTERACTION; MOTH; PARASITOLOGY; PARTHENOGENESIS; PECAN; PHYSIOLOGY; SPECIES DIFFERENCE; SPECIES DIFFERENTIATION; UNITED STATES; CARYA;

AMPLIFIED FRAGMENT LENGTH POLYMORPHISM ANALYSIS; ANALYSIS OF VARIANCE; ANIMALS; APHIDS; BAYES THEOREM; CARYA; CLUSTER ANALYSIS; GENETIC SPECIATION; GENETIC VARIATION; HOST-PATHOGEN INTERACTIONS; MODELS, GENETIC; MOTHS; PARTHENOGENESIS; SPECIES SPECIFICITY; TEXAS;

APHIDIDAE; CARYA AQUATICA; CARYA ILLINOINENSIS; HEXAPODA;

EID: 77955163150     PISSN: 1010061X     EISSN: 14209101     Source Type: Journal    
DOI: 10.1111/j.1420-9101.2010.01962.x     Document Type: Article

References (97)

1. Abrahamson AG, Weis AE. Evolutionary Ecology Across Three Trophic Levels: Goldenrods, Gallmakers, and Natural Enemies 1997, Princeton University Press, Princeton, NJ
2. Abrahamson WG, Blair CP, Eubanks MD, Morehead SA. Sequential radiation of unrelated organisms: the gall fly Eurosta solidaginis and the tumbling flower beetle Mordellistena convicta. J. Evol. Biol. 2003, 16:781-789.
3. Akimoto S. The evolution of gall parasitism accompanied by a host shift in the gall aphid, Eriosoma yangi (Homoptera, Aphidoidea). Biol. J. Linn. Soc. 1988, 35:297-312.
4. Akimoto S. Local adaptation and host race formation of a gall-forming aphid in relation to environmental heterogeneity. Oecologia 1990, 83:162-170.
5. Anstead JA, Burd JD, Shufran KA. Mitochondrial DNA sequence divergence among Schizaphis graminum (Hemiptera Aphididae) clones from cultivated and non-cultivated hosts: haplotype and host associations. Bull. Entomol. Res. 2002, 92:17-24.
6. Arakaki N, Miyoshi T, Noda H. Wolbachia-mediated parthenogenesis in the predatory thrips Fanklintothrips vespiformis (Thysanoptera Insecta). Proc. R. Soc. B Biol. Sci. 2001, 268:1011-1016.
7. Berlocher SH, Feder JL. Sympatric speciation in phytophagous insects: moving beyond controversy? Annu. Rev. Entomol. 2002, 47:773-815.
8. Blackman RL, Eastop VF. Aphids on the Worlds Trees - An Identification and Information Guide 1994, CAB International, Wallingford
9. Blackman RL, Eastop VF, Hills M. Morphological and cytological separation of Amphorophora Buckton (Homoptera: Aphididae) feeding on European rasberry and blackberry (Rubus spp.). Bull. Entomol. Res. 1977, 67:285-296.
10. Brunner PC, Chatzivassiliou EK, Katis NI, Frey JE. Host-associated genetic differentiation in Thrips tabaci (Insecta; Thysanoptera), as determined from mtDNA sequence data. Heredity 2004, 93:364-370.
11. Bush GL. Sympatric host race formation and speciation in frugivorous flies of genus Rhagoletis (Diptera, Tephritidae). Evolution 1969, 23:237-251.
12. Butlin RK. Divergence in emergence time of host races due to differential gene flow. Heredity 1990, 65:47-50.
13. Carletto J, Lombaert E, Chavigny P, Brevault T, Lapchin L, Vanlerberghe-Masutti F. Ecological specialization of the aphid Aphis gossypii Glover on cultivated host plants. Mol. Ecol. 2009, 18:2198-2212.
14. Cornell HV, Hawkins BA, Hochberg ME. Towards an empirically-based theory of herbivore demography. Ecol. Entomol. 1998, 23:340-349.
15. Dixon AF. Aphid Ecology 1998, 2nd edn, Chapman and Hall, London
16. Dorchin N, Scott ER, Clarkin CE, Luongo MP, Jordan S, Abrahamson WG. Behavioural, ecological and genetic evidence confirm the occurrence of host-associated differentiation in goldenrod gall-midges. J. Evol. Biol. 2009, 22:729-739.
17. Dreger-Jauffret F, Shorthouse JD. Diversity of gall-inducing insects and their galls. Biology of Insects-Induced Galls 1992, 8-33. Shorthouse JD, Rohfritsch O. eds, Oxford University Press, Oxford
18. Dres M, Mallet J. Host races in plant-feeding insects and their importance in sympatric speciation. Philos. Trans. R. Soc. Lond. Ser. B-Biol. Sci. 2002, 357:471-492.
19. Eastop VF. Deductions from the present day host plants of aphids and related insects. Insect/Plant Relationships 1973, 157-178. Vanemden HF. eds, Symposia of the Royal Entomological Society, London, No. 6. Blackwell Scientific Publications, Oxford
20. Edmunds GF, Alstad DN. Responses of black pineleaf scales to host plant variability. Insect Life History Patterns 1981, 29-38. Denno RF, Dingle H. eds, Springer-Verlag, New York
21. Emelianov I, Simpson F, Narang P, Mallet J. Host choice promotes reproductive isolation between host races of the larch budmoth Zeiraphera diniana. J. Evol. Biol. 2003, 16:208-218.
22. Eubanks MD, Blair CP, Abrahamson WG. One host shift leads to another? Evidence of host-race formation in a predaceous gall-boring beetle. Evolution 2003, 57:168-172.
23. Evanno G, Regnaut S, Goudet J. Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol. Ecol. 2005, 14:2611-2620.
24. Excoffier L, Smouse PE, Quattro JM. Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction sites. Genetics 1992, 131:479-491.
25. Falush D, Stephens M, Pritchard JK. Inference of population structure using multi locus genotype data: linked loci and correlated allele frequencies. Genetics 2003, 164:1567-1587.
26. Falush D, Stephens M, Pritchard JK. Inference of population structure using multilocus genotype data: dominant markers and null alleles. Mol. Ecol. Notes 2007, 7:574-578.
27. Feder JL. The effects of parasitoids on sympatric host races of Rhagoletis pomonella (Diptera, Tephritidae). Ecology 1995, 76:801-813.
28. Feder JL, Filchak KE. 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. Entomol. Exp. Appl. 1999, 91:211-225.
29. Feder JL, Williams SM, Berlocher SH, McPheron BA, Bush GL. The population genetics of the apple maggot fly, Rhagoletis pomonella and the snowberry maggot, R. zephyria: implications for models of sympatric speciation. Entomol. Exp. Appl. 1999, 90:9-24.
30. Forbes AA, Powell THQ, Stelinski LL, Smith JJ, Feder JL. Sequential sympatric speciation across trophic levels. Science 2009, 323:776-779.
31. Fralish JS, Franklin SB. Taxonomy and Ecology of Woody Plants in North American Forests (Excluding Mexico and Subtropical Florida) 2002, Wiley, New York
32. Funk DJ, Filchak KE, Feder JL. Herbivorous insects: model systems for the comparative study of speciation ecology. Genetica 2002, 116:251-267.
33. Godfray HCJ. Parasitoids: Behavioral and Evolutionary Ecology 1994, Princeton University Press, Princeton
34. Gompert Z, Fordyce JA, Forister ML, Shapiro AM, Nice CC. Homoploid hybrid speciation in an extreme habitat. Science 2006, 314:1923-1925.
35. Grauke LJ, Pratt JW, Morris H. Phenology and site adaptation of Louisiana hickories. Research Report 1987, 181-185. Station PRE, ed, Louisiana Agricultural Experiment Station, Baton Rouge
36. Grauke LJ, Iqbal MJ, Reddy AS, Thompson TE. Developing microsatellite DNA markers in pecan. J. Am. Soc. Hortic. Sci. 2003, 128:374-380.
37. Guldemond JA, Mackenzie A. Sympatric speciation in aphids. I. Host race formation by escape from gene flow. Individuals, Populations and Patterns in Ecology 1994, 367-378. Leather SR, Watt ADMills NJWalters KFA. eds, Intercept, Andover
38. Guldemond JA, Tigges WT, De Vrijer PWF. Host races of Aphis gossypii (Homoptera: Aphididae) on Cucumber and Chrysanthemum. Environ. Entomol. 1994, 23:6.
39. Hartl DL. A fundamental theorem of natural selection for sex linkage or arrhenotoky. Am. Nat. 1972, 106:9.
40. Hendry AP, Day T, Taylor EB. Population mixing and the adaptive divergence of quantitative traits in discrete populations: a theoretical framework for empirical tests. Evolution 2001, 55:459-466.
41. King CE. Random genetic drift during cyclical ameiotic parthenogenesis. Hydrobiologia 1993, 255:205-212.
42. King CE, Murtaugh P. Effects of asexual reproduction on the neighborhood area of cyclical parthenogens. Hydrobiologia 1997, 358:55-62.
43. Komatsu T, Akimoto S. Genetic differentiation as a result of adaptation to the phenologies of individual host trees in the galling aphid Kaltenbachiella japonica. Ecol. Entomol. 1995, 20:33-42.
44. Loxdale HD. The nature and reality of the aphid clone: genetic variation, adaptation and evolution. Agric. For. Entomol. 2008, 10:81-90.
45. Lozier JD, Roderick GK, Mills NJ. Genetic evidence from mitochondrial, nuclear, and endosymbiont markers for the evolution of host plant associated species in the aphid genus Hyalopterus (Hemiptera Aphididae). Evolution 2007, 61:1353-1367.
46. Lynch M. The limits to life history evolution in Daphnia. Evolution 1984, 38:18.
47. Lynch M, Gabriel W. Phenotypic evolution and parthenogenesis. Am. Nat. 1983, 122:745-764.
48. Lynch M, Milligan BG. Analysis of population genetic structure with RAPD markers. Mol. Ecol. 1994, 3:91-99.
49. Magalhaes S, Forbes MR, Skoracka A, Osakabe M, Chevillon C, McCoy KD. Host race formation in the Acari. Exp. Appl. Acarol. 2007, 42:225-238.
50. Manchester SR. The Fossil History of the Juglandaceae 1987, Missouri Botanical Garden, St. Louis, MO
51. Manning WE. Classification within the Juglandaceae. Ann. Mo. Bot. Gard. 1978, 65:1058-1087.
52. Margaritopoulos JT, Malarky G, Tsitsipis JA, Blackman RL. Microsatellite DNA and behavioural studies provide evidence of host-mediated speciation in Myzus persicae (Hemiptera Aphididae). Biol. J. Linn. Soc. 2007, 91:687-702.
53. Martel C, Rejasse A, Rousset F, Bethenod MT, Bourguet D. Host-plant-associated genetic differentiation in Northern French populations of the European corn borer. Heredity 2003, 90:141-149.
54. Medina RF, Barbosa P, Christman M, Battisti A. Number of individuals and molecular markers to use in genetic differentiation studies. Mol. Ecol. Notes 2006, 6:1010-1013.
55. Meudt HM, Clarke AC. Almost forgotten or latest practice? AFLP applications, analyses and advances. Trends Plant Sci. 2007, 12:106-117.
56. Mitchell PL, Olszak R, Stoetzel MB, Harris MK. Fauna associated with galls of Phylloxera spp. on pecan. Southwest. Entomol. 1984, 9:8.
57. Mitter C, Farrell BD, Wiegmann B. The phylogenetic study of adaptive zones - has phytophagy promoted insect diversification? Am. Nat. 1988, 132:107-128.
58. Mizell RF, Schiffhauer DE. Larval infestation levels of pecan bud moth, Gretchena bolliana (Lepidoptera, Tortricidae), in relation to cultivar and position on the tree. Environ. Entomol. 1986, 15:436-438.
59. Mopper S. Phenology - how time creates spatial structure in endophagous insect populations. Ann. Zool. Fenn. 2005, 42:327-333.
60. Muller C, Barker A, Boeve JL, De Jong PW, De Vos H, Brakefield PM. Phylogeography of two parthenogenetic sawfly species (Hymenoptera Tenthredinidae): relationship of population genetic differentiation to host plant distribution. Biol. J. Linn. Soc. 2004, 83:219-227.
61. Nault BA, Shelton AM, Gangloff-Kaufmann JL, Clark ME, Werren JL, Cabrera-La Rosa JC, Kennedy GG. Reproductive modes in onion thrips (Thysanoptera Thripidae) populations from New York onion fields. Environ. Entomol. 2006, 35:1264-1271.
62. Neiman M, Linksvayer TA. The conversion of variance and the evolutionary potential of restricted recombination. Heredity 2006, 96:11.
63. Nosil P. Adaptive population divergence in cryptic color-pattern following a reduction in gene flow. Evolution 2009, 63:1902-1912.
64. Nyman T. The willow bud galler Euura mucronata Hartig (Hymenoptera Tenthredinidae): one polyphage or many monophages? Heredity 2002, 88:288-295.
65. Peakall R, Smouse PE. GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol. Ecol. Notes 2006, 6:288-295.
66. Peccoud J, Ollivier A, Plantegenest M, Simon JC. A continuum of genetic divergence from sympatric host races to species in the pea aphid complex. Proc. Natl Acad. Sci. USA 2009, 106:7495-7500.
67. Price PW. Evolutionary Biology of Parasites 1980, Princeton University Press, Princeton
68. Pritchard JK, Wen X, Falush D. Documentation for STRUCTURE software: Version 2.2 2007, http://pritch.bsd.uchicago.edu, Available from
69. Rundle HD, Nosil P. Ecological speciation. Ecol. Lett. 2005, 8:336-352.
70. Saunders JA, Mischke S, Hemeida AA. The Use of AFLP Techniques for DNA Fingerprinting in Plants 2001, 1-9. Beckman Coulter Application Notes
71. Scheffer SJ, Hawthorne DJ. Molecular evidence of host-associated genetic divergence in the holly leafminer Phytomyza glabricola (Diptera: Agromyzidae): apparent discordance among marker systems. Mol. Ecol. 2007, 16:2627-2637.
72. Schlutter D. Ecology and the origin of species. Trends Ecol. Evol. 2001, 16:372-380.
73. Schoonhoven LM, Jermy T, van Loon JJA. Insect-Plant Biology: From Physiology to Evolution 1998, 1 edn, Chapman & Hall, London
74. Serra M, Gomez A, Carmona MJ. Ecological genetics of Brachionus sympatric sibling species. Hydrobiologia 1998, 388:373-384.
75. Simon JC, Carre S, Boutin M, Prunier-Leterme N, Sabater-Munoz B, Latorre A, Bournoville R. Host-based divergence in populations of the pea aphid: insights from nuclear markers and the prevalence of facultative symbionts. Proc. R. Soc. B-Biol. Sci. 2003, 270:1703-1712.
76. Slatkin M. Gene flow and selection in a cline. Genetics 1973, 75:733-756.
77. Smith MW, Arnold DC, Eikenbary RD, Rice NR, Shiferaw A, Cheary BS, Carroll BL. Influence of ground cover on phytophagous and saprophagous arthropods in pecan trees. Southwest. Entomol. 1996, 21:303-316.
78. Stam P. The evolution of reproductive isolation in closely adjacent plant populations through differential flowering time. Heredity 1983, 50:105-118.
79. Stilling P, Rossi AM. Deme formation in a dispersive gall-forming midge. Genetic Structure and Local Adaptation in Natural Insect Populations 1998, 22-34. Mopper S, Strauss SY. eds, pp, Chapman & Hall, New York, NY
80. Stireman JO, Nason JD, Heard SB. Host-associated genetic differentiation in phytophagous insects: general phenomenon or isolated exceptions? evidence from a goldenrod insect-community. Evolution 2005, 59:2573-2587.
81. Stireman JO, Nason JD, Heard SB, Seehawer JM. Cascading host-associated genetic differentiation in parasitoids of phytophagous insects. Proc. R. Soc. B Biol. Sci. 2006, 273:523-530.
82. Stireman JO, Janson EM, Carr TG, Devlin H, Abbot P. Evolutionary radiation of Asteromyia carbonifera (Diptera: Cecidomyiidae) gall morphotypes on the goldenrod Solidago altissima (Asteraceae). Biol. J. Linn. Soc. 2008, 95:840-858.
83. Stone DE, Adrouny GA, Adrouny S. Morphological and chemical evidence on the hybrid nature of bitter pecan, Carya X lecontei. Brittonia 1965, 17:10.
84. Strauss SY, Lau JA, Carroll SP. Evolutionary responses of natives to introduced species: what do introductions tell us about natural communities? Ecol. Lett. 2006, 9:354-371.
85. Sunnucks P, DeBarro PJ, Lushai G, Maclean N, Hales D. Genetic structure of an aphid studied using microsatellites: cyclic parthenogenesis, differentiated lineages and host specialization. Mol. Ecol. 1997, 6:1059-1073.
86. Sword GA, Joern A, Senior LB. Host plant-associated genetic differentiation in the snakeweed grasshopper, Hesperotettix viridis (Orthoptera: Acrididae). Mol. Ecol. 2005, 14:2197-2205.
87. Tedders WL. Important Biological and Morphological Characteristics of the Foliar-Feeding Aphids of Pecan 1978, U.S. Department of Agriculture, Science and Education Administration, Washington
88. Thompson TE, Grauke LJ. Pecans and other hickories (Carya). Acta Hortic 1991, 290:839-906.
89. Vanlerberghe-Masutti F, Chavigny P. Host-based genetic differentiation in the aphid Aphis gossypii Glover, evidenced from RAPD fingerprints. Mol. Ecol. 1998, 7:905-914.
90. Vekemans X. AFLP-SURV Version 1.0 2002, Distributed by the author, Laboratoire de Génétique et Ecologie Végétale, Université Libre de Bruxelles, Belgium
91. Via S, Hawthorne DJ. The genetic architecture of ecological specialization: correlated gene effects on host use and habitat choice in pea aphids. Am. Nat. 2002, 159:S76-S88.
92. Vialatte A, Dedryver CA, Simon JC, Galman M, Plantegenest M. Limited genetic exchanges between populations of an insect pest living on uncultivated and related cultivated host plants. Proc. R. Soc. Lond. Ser. B Biol. Sci. 2005, 272:1075-1082.
93. Vos P, Hogers R, Bleeker M, Reijans M, Vandelee T, Hornes M, Frijters A, Pot J, Peleman J, Kuiper M, Zabeau M. AFLP - a new technique for DNA-fingerprinting. Nucleic Acids Res. 1995, 23:4407-4414.
94. Walker F. Descriptions of Aphides. Ann. Mag. Nat. Hist. 1850, 2:14-28.
95. Ward SA. Theoretical perspective on sympatric speciation in aphids (Homoptera: Aphidinea: Aphididae). Entomol. Gen. 1991, 16:177-192.
96. Waring GL, Abrahamson WG, Howard DJ. Genetic differentiation among host-associated populations of the gallmaker Eurosta solidaginis (Diptera: Tephritidae). Evolution 1990, 44:1648-1655.
97. Zhivotovsky LA. Estimating population structure in diploids with multilocus dominant DNA markers. Mol. Ecol. 1999, 8:907-913.