Russian wheat aphids (Diuraphis noxia) in China: Native range expansion or recent introduction?

Molecular Ecology

Volumn 21, Issue 9, 2012, Pages 2130-2144

  Zhang, B ^a,b,c   Edwards, O R ^c,d   Kang, L ^b   Fuller, S J ^a,c  

^a QUEENSLAND UNIVERSITY OF TECHNOLOGY   (Australia)

^b INSTITUTE OF ZOOLOGY   (China)

^c Australia Cooperative Research Centre for National Plant Biosecurity   (Australia)

^d CSIRO   (Australia)

Author keywords

Diuraphis noxia; genetic structure; geographic isolation; native range; population expansion; wheat domestication

Indexed keywords

MICROSATELLITE DNA; MITOCHONDRIAL DNA;

ANIMAL; APHID; ARTICLE; CHINA; GENETIC VARIABILITY; GENETICS; MITOCHONDRION; PHYSIOLOGY; WHEAT;

ANIMALS; APHIDS; CHINA; DNA, MITOCHONDRIAL; GENETIC VARIATION; MICROSATELLITE REPEATS; MITOCHONDRIA; TRITICUM;

APHIDIDAE; DIURAPHIS NOXIA; POACEAE; TRITICUM AESTIVUM;

EID: 84862806146     PISSN: 09621083     EISSN: 1365294X     Source Type: Journal    
DOI: 10.1111/j.1365-294X.2012.05517.x     Document Type: Article

References (89)

1. Abbot P, (2011) A closer look at the spatial architecture of aphid clones. Molecular Ecology, 20, 4587-4589.
2. An CB, Tang LY, Barton L, et al. (2005) Climate change and cultural response around 4000 cal yr BP in the western part of Chinese Loess Plateau. Quaternary Research, 63, 347-352.
3. Arnaud-Haond S, Belkhir K, (2007) Genclone: a computer program to analyse genotypic data, test for clonality and describe spatial clonal organization. Molecular Ecology Notes, 7, 15-17.
4. Basky Z, (2002) Biotypic variation in Russian wheat aphid (Diuraphis noxia Kurdjumov Homoptera: Aphididae) between Hungary and South Africa. Cereal Research Communications, 30, 133-139.
5. Beerli P, (2008) MIGRATE version 3.0: a maximum likelihood and Bayesian estimator of gene flow using the coalescent. Available at:, last accessed on 23 March 2011.
6. Belkhir K, Borsa P, Chikhi L, et al. (19962004) GENETIX 4.05, Logiciel sous Windows pour la Génétique des Populations. Laboratoire Génome, Populations, Interactions, CNRS UMR 5000, Université de Montpellier II, Montpellier, France.
7. Bellwood P, (2001) Early agriculturalist population diasporas? Farming, languages, and genes. Annual Review of Anthropology, 20, 181-207.
8. Bilgin R, (2007) Kgtests: a simple Excel Macro program to detect signatures of population expansion using microsatellites. Molecular Ecology Notes, 7, 416-417.
9. Bonizzoni M, Guglielmino CR, Smallridge CJ, et al. (2004) On the origin of medfly invasion and expansion in Australia. Molecular Ecology, 13, 3845-3855.
10. Bright C, (1999) Invasive species: pathogens of globalisation. Foreign Policy, 116, 50-64.
11. Burd JD, Porter DR, Puterka GJ, et al. (2006) Biotypic variation among North American Russian wheat aphid population. Journal of Economic Entomology, 99, 1862-1866.
12. Chapuis MP, Loiseau A, Michalakis Y, et al. (2009) Outbreaks, gene flow and effective population size in the migratory locust, Locusta migratoria: a regional-scale comparative survey. Molecular Ecology, 18, 792-800.
13. Charaabi K, Carletto J, Chavigny P, et al. (2008) Genotypic diversity of the cotton-melon aphid Aphis gossypii (Glover) in Tunisia is structured by host plants. Bulletin of Entomological Research, 98, 333-341.
14. Clement M, Posada D, Crandall K, (2000) TCS: a computer program to estimate gene genealogies. Molecular Ecology, 9, 1657-1660.
15. Clua A, Castro AM, Ramos S, et al. (2004) The biological characteristics and distribution of the greenbug, Schizaphis graminum, and Russian wheat aphid, Diuraphis noxia (Hemiptera: Aphididae) in Argentina and Chile. European Journal of Entomology, 101, 193-198.
16. Cornuet JM, Luikart G, (1996) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics, 144, 2001-2014.
17. Cornuet JM, Santos F, Beaumont MA, et al. (2008) Inferring population history with DIY ABC: a user-friendly approach to approximate Bayesian computation. Bioinformatics, 24, 2713-2719.
18. Delmotte F, Leterme N, Gauthier JP, et al. (2002) Genetic architecture of sexual and asexual populations of the aphid Rhopalosiphum padi based on allozyme and microsatellite markers. Molecular Ecology, 11, 711-723.
19. Diamond J, (2002) Evolution, consequences and future of plant and animal domestication. Nature, 418, 700-707.
20. DiLeo M, Row JR, Lougheed SC, (2010) Discordant patterns of population structure for two co-distributed snake species across a fragmented Ontario landscape. Diversity and Distributions, 16, 571-581.
21. Dixon AFG, (1998) Aphid Ecology, 2nd edn. Chapman and Hall, London.
22. Dolatti L, Ghareyazie B, Moharramipour S, et al. (2005) Evidence for regional diversity and host adaptation in Iranian population of the Russian wheat aphid. Entomologia experimentalis et applicata, 114, 171-180.
23. Du BR, (2000) Investigation of the distribution and suitable area of Russian wheat aphid, Diuraphis noxia (Kurdjumov) in Xinjiang. Xinjiang Agricultural Science, 1, 82-85.
24. Evanno G, Regnaut S, Goudet J, (2005) Detecting the number of clusters of individuals using the software structure: a simulation study. Molecular Ecology, 14, 2611-2620.
25. Excoffier L, Laval G, Schneider S, (2005) Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evolutionary Bioinformatics Online, 1, 47-50.
26. Ferrari J, Godfray HC, Faulconbridge AS, et al. (2006) Population differentiation and genetic variation in host choice among pea aphids from eight host plant genera. Evolution, 60, 1574-1584.
27. Fu YX, (1997) Statistical methods of neutrality of mutations against population growth, hitchhiking and background selection. Genetics, 147, 915-925.
28. Fu YX, Li WH, (1993) Statistical tests of neutrality of mutations. Genetics, 133, 693-709.
29. Goodisman MAD, Matthews RW, Crozier RH, (2001) Hierarchical genetic structure of the introduced wasp Vespula germanica in Australia. Molecular Ecology, 10, 1423-1432.
30. Goudet J, (2001) FSTAT, a program to estimate and test gene diversities and fixation indices, version 2.9.3. Available at:.
31. Haley SD, Peairs FB, Walker CB, et al. (2004) Occurrence of a new Russian wheat aphid biotype in Colorado. Crop Science, 44, 1589-1592.
32. Hall T, (2004) BioEdit v. 7.0.0. Available at:.
33. Harrison JS, Mondor EB, (2011) Evidence for an invasive aphid 'superclone': extremely low genetic diversity in oleander aphid (Aphis nerii) populations in the southern United States. PLoS ONE, 6, e17524.
34. Jimoh MA, Botha CEJ, Edwards O, Bradley G, (2011) Population growth rate and relative virulence of the two South African biotypes of Russian wheat aphid, Diuraphis noxia, and bird cherry-oat aphid, Rhopalosiphum padi, on resistant and non-resistant barley. Entomologia Experimentalis et Applicata, 138, 12-20.
35. Jyoti JL, Qureshi JA, Michaud JP, et al. (2006) Virulence of two Russian wheat aphid to eight wheat cultivars at two temperature. Crop Science, 46, 774-780.
36. Kiriac I, Gruber F, Poprawski TJ, et al. (1990) Occurrence of sexual morphs of Russian wheat aphid, Diuraphis noxia (Homoptera: Aphididae), in several locations in the Soviet Union and the Northwestern United States. Proceedings of the Entomological Society of Washington, 92, 544-547.
37. Kovalev OV, Poprawski TJ, Stekolshchinov AV, et al. (1991) Diuraphis Aizenberg (Hom., Aphididae): key to apterous viviparous females and a review of Russian language literature on the natural history of Diuraphis noxia (Kudjumov, 1913). Journal of Applied Entomology, 112, 425-436.
38. Li XQ, Dodson J, Zhou XY, et al. (2007) Early cultivated wheat and broadening of agriculture in Neolithic China. The Holocene, 17, 555-560.
39. Liang HB, Zhang RZ, Zhang GX, (1999) Prediction of suitable areas for Russian wheat aphid in China. Acta Entomologica Sinica, 42S, 55-61.
40. Librado P, Rozas J, (2009) DnaSP v. 5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics, 25, 1451-1452.
41. Liu X, Marshall JL, Stary P, et al. (2010) Global phylogenetics of Diuraphis noxia (Hemiptera: Aphididae), an invasive aphid species: evidence for multiple invasions into North America. Journal of Economic Entomology, 103, 958-965.
42. Llewellyn KS, Loxdale HD, Harrington R, et al. (2003) Migration and genetic structure of the grain aphid (Sitobion avenae) in Britain related to climate and clonal fluctuation as revealed using microsatellites. Molecular Ecology, 12, 21-34.
43. Loxdale HD, Hardie J, Halber S, et al. (1993) The relative importance of short- and long-range movement of flying aphids. Biological Reviews, 68, 291-311.
44. Marshall TC, Slate J, Kruuk LEB, Pemberton JM, (1998) Statistical confidence for likelihood-based paternity inference in natural populations. Molecular Ecology, 7, 639-655.
45. Martinez-Torres D, Moya A, Hebert PDN, Simon JC, (1997) Geographic distribution and seasonal variation of mitochondrial DNA haplotypes in the aphid Rhopalosiphum padi (Hemiptera: Aphididae). Bulletin of Entomological Research, 87, 161-167.
46. Michel AP, Zhang W, Jung KJ, et al. (2009) Population genetic structure of Aphis glycines. Environmental Entomology, 38, 1301-1311.
47. Motro U, Thomson G, (1982) On heterozygosity and the effective size of populations subject to size changes. Evolution, 36, 1059-1066.
48. Papadopoulou A, Anastasiou I, Vogler AP, (2010) Revisiting the insect mitochondrial molecular clock: the mid-Aegean trench calibration. Molecular Biology and Evolution, 27, 1659-1672.
49. Peccoud J, Ollivier A, Plantegenest M, Simon JC, (2009) A continuum of genetic divergence from sympatric host races to species in the pea aphid complex. Proceedings of the National Academy of Science USA, 16, 7495-7500.
50. Piry S, Luikart G, Cornuet JM, (1999) Bottleneck: a computer program for detecting recent reduction in the effective population size using allele frequency data. Journal of Heredity, 90, 502-503.
51. Pritchard JK, Stephens M, Donnelly P, (2000) Inference of population structure using multilocus genotype data. Genetics, 1555, 945-959.
52. Puterka GJ, Burd JD, Burton RL, (1992) Biotypic variation in a worldwide collection of Russisan wheat aphid (Hemiptera: Aphididae). Journal of Economic Entomology, 85, 1497-1506.
53. Pysek P, Richardson DM, Pergl J, et al. (2008) Geographical and taxonomic biases in invasion ecology. Trends in Ecology and Evolution, 23, 237-244.
54. Ramos-Onsins SE, Rozas J, (2002) Statistical properties of new neutrality tests against population growth. Molecular Biology and Evolution, 19, 2092-2100.
55. Raymond M, Rousset F, (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. Journal of Heredity, 86, 248-249.
56. Reich DE, Goldstein DB, (1998) Genetic evidence for a Paleolithic human population expansion in Africa. Proceedings of the National Academy of Sciences USA, 95, 8119-8123.
57. Reich DE, Feldman MW, Goldstein DB, (1999) Statistical properties of two tests that use multilocus data sets to detect population expansions. Molecular Biology and Evolution, 16, 453-466.
58. Rice WR, (1989) Analyzing tables of statistical tests. Evolution, 43, 223-225.
59. Richerson PJ, Boyd R, Bettinger RL, (2001) Was agriculture impossible during the Pleistocene but mandatory during the Holocene? A climate change hypothesis. American Antiquity, 66, 287-411.
60. Roderick GK, (1996) Geographic structure of insect populations: gene flow, phylogeography, and their uses. Annual Review of Entomology, 41, 325-352.
61. Rosenberg NA, (2004) Distruct: a program for the graphical display of population structure. Molecular Ecology Resources, 4, 137-138.
62. Ross KG, Shoemaker DD, (2008) Estimation of the number of founders of an invasive pest insect population: the fire ant Solenopsis invicta in the USA. Proceedings of Royal Society. B, 275, 2231-2240.
63. Ross KG, Krieger MJB, Shoemaker DD, (2003) Alternative genetic foundations for a key social polymorphism in fire ants. Genetics, 165, 1853-1867.
64. Ross KG, Krieger MJB, Keller L, et al. (2007) Genetic variation and structure in native populations of the fire ant Solenopsis invicta: evolutionary and demographic implications. Biological Journal of the Linnean Society, 92, 541-560.
65. Rousset F, (2008) Genepop'007: a complete reimplementation of the Genepop software for Windows and Linux. Molecular Ecology Resources, 8, 103-106.
66. Scott JM, (2007) Native and exotic plant species exhibit similar population dynamics during Succession. Ecology, 88, 1098-1104.
67. Shufran KA, Payton TL, (2009) Limited genetic variation within and between Russian wheat aphid (Hemiptera: Aphididae) biotypes in the United States. Journal of Economic Entomology, 102, 440-445.
68. Shufran KA, Burd JD, Anstead JA, Lushai G, (2000) Mitochondrial DNA sequence divergence among greenbug (Homoptera: Aphididae) biotypes: evidence for host-adapted races. Insect Molecular Biology, 9, 179-184.
69. Shufran KA, Kirkman LR, Puterka GJ, (2007) Absence of mitochondrial DNA sequence variation in Russian wheat aphid (Hemiptera: Aphididae) populations consistent with a single introduction into the United States. Journal of the Kansas Entomological Society, 80, 319-326.
70. Simon C, Frati F, Beckenbach A, et al. (1994) Evolution, weighting, and phylogenetic utility of mitochondrial gene sequences and a compilation of conserved polymerase chain reaction primers. Annals of the Entomological Society of America, 87, 651-701.
71. Simon JC, Baumann S, Sunnucks P, et al. (1999) Reproductive mode and population genetic structure of the cereal aphid Sitobion avenae studied using phenotypic and microsatellite markers. Molecular Ecology, 8, 531-545.
72. Simon C, Buckley TR, Frati F, et al. (2006) Incorporating molecular evolution into phylogenetic analysis, and a new compilation of conserved polymerase chain reaction primers for animal mitochondrial DNA. Annual Review of Ecology, Evolution, and Systematics, 37, 545-579.
73. Smith CM, Belay T, Stuffer C, et al. (2004) Identification of Russian wheat aphid (Homoptera: Aphididae) populations virulent to the Dn4 resistance gene. Journal of Economic Entomology, 97, 1112-1117.
74. Stary P, (1999) Distribution and ecology of the Russian wheat aphid, Diuraphis noxia (Kurdj.), expanded to Central Europe (Hom.: Aphididae). Journal of Pest Science, 72, 25-30.
75. Sunnucks P, Hales DF, (1996) Numerous transposed sequences of mitochondrial cytochrome oxidase I-II in aphids of the genus Sitobion (Hemiptera: Aphididae). Molecular Biology and Evolution, 13, 510-524.
76. Sunnucks P, De Barro PJ, Lushai G, et al. (1997) Genetic structure of an aphid studied using microsatellites: cyclic parthenogenesis, differentiated lineages, and host specialization. Molecular Ecology, 6, 1059-1073.
77. Tajima F, (1989) Statistical-method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics, 123, 585-595.
78. Tamura K, Dudley J, Nei M, Kumar S, (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Molecular Biology and Evolution, 24, 1596-1599.
79. Thornton CP, Schurr TG, (2004) Genes, language, and culture: an example from the Tarim Basin. Oxford Journal of Archaeology, 23, 83-106.
80. Van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P, (2004) MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Molecular Ecology Notes, 4, 535-538.
81. Venette RC, Ragsdale DW, (2004) Assessing the invasion by soybean aphid (Homoptera: Aphididae): where will it end? Annals of the Entomological Society of America, 97, 219-226.
82. Vorburger C, (2006) Temporal dynamics of genotypic diversity reveal strong clonal selection in the aphid Myzus persicae. Journal of Evolutionary Biology, 19, 97-107.
83. Weir BS, Cockerham CC, (1984) Estimating F-statistics for the analysis of population structure. Evolution, 38, 1358-1370.
84. Wilson GA, Rannala B, (2003) Bayesian inference of recent migration rates using multilocus genotypes. Genetics, 163, 1177-1191.
85. Wilson ACC, Sunnucks P, Hales DF, (1997) A microsatellite linked to the X-chromosome of Sitobion aphids reveals random inheritence of the X-chromosome in males. Genetical Research, Cambridge, 69, 233-236.
86. Wilson ACC, Massonnet B, Simon JC, et al. (2004) Cross-species amplification of microsatellite loci in aphids: assessment and application. Molecular Ecology Notes, 4, 104-109.
87. Zhang RZ, Liang HB, Zhang GX, (1999a) Research on Russian wheat aphid, Diuraphis noxia Kurdjumov, in China. Acta Entomologica Sinica, 42S, 11-17.
88. Zhang RZ, Liang HB, Zhang GX, (1999b) Russian wheat aphid, Diuraphis noxia, and its research progress worldwide. Acta Entomologica Sinica, 42S, 130-140.
89. Zhang Y, Wang L, Wu K, et al. (2008) Flight performance of the soybean aphid, Aphis glycines (Hemiptera: Aphididae) under different temperature and humidity regimens. Environmental Entomology, 37, 301-306.