Climate effects on life cycle variation and population genetic architecture of the black bean aphid, Aphis fabae

Molecular Ecology

Volumn 20, Issue 19, 2011, Pages 4165-4181

  Sandrock, Christoph ^a,e   Razmjou, Jabraeil ^b   Vorburger, Christoph ^c,d  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b UNIVERSITY OF MOHAGHEGH ARDABILI   (Iran)

^c ETH ZURICH   (Switzerland)

^d SWISS FEDERAL INSTITUTE OF AQUATIC SCIENCE AND TECHNOLOGY   (Switzerland)

^e AGROSCOPE LIEBEFELD POSIEUX RESEARCH STATION ALP   (Switzerland)

Author keywords

Aphis fabae; contagious parthenogenesis; crop pest; cyclical parthenogenesis; host associated differentiation

Indexed keywords

MICROSATELLITE DNA;

ANIMAL; APHID; ARTICLE; BAYES THEOREM; BIOLOGICAL MODEL; CLIMATE; EUROPE; FEMALE; GENE FLOW; GENETIC VARIABILITY; GENETICS; GENOTYPE; GROWTH, DEVELOPMENT AND AGING; LIFE CYCLE STAGE; MALE; PHYSIOLOGY; SEXUAL BEHAVIOR; VICIA FABA;

ANIMALS; APHIDS; BAYES THEOREM; CLIMATE; EUROPE; FEMALE; GENE FLOW; GENETIC VARIATION; GENOTYPE; LIFE CYCLE STAGES; MALE; MICROSATELLITE REPEATS; MODELS, BIOLOGICAL; SEXUAL BEHAVIOR, ANIMAL; VICIA FABA;

ACER PENSYLVANICUM; AMARANTHACEAE; APHIDIDAE; APHIS FABAE; VICIA FABA;

EID: 80053227237     PISSN: 09621083     EISSN: 1365294X     Source Type: Journal    
DOI: 10.1111/j.1365-294X.2011.05242.x     Document Type: Article

References (107)

1. 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. (Pubitemid 46046572)
2. Arnaud-Haond S, Duarte CM, Alberto F, Serrao EA, (2007) Standardizing methods to address clonality in population studies. Molecular Ecology, 16, 5115-5139. (Pubitemid 350265252)
3. Balloux F, Lehmann L, de MeeÃs T, (2003) The population genetics of clonal and partially clonal diploids. Genetics, 164, 1635-1644. (Pubitemid 37102223)
4. Barton NH, Charlesworth B, (1998) Why sex and recombination? Science, 281, 1986-1990. (Pubitemid 28475479)
5. Belkhir K, Borsa P, Chikhi L, Raufaste N, Bonhomme F, (19962004) GENETIX 4.05, Logiciel Sous Windows TM Pour la Génétique des Populations. Laboratoire Génome, Populations, Interactions, CNRS UMR 5000, Université de Montpellier II, Montpellier, France.
6. Bell G, (1982) The Masterpiece of Nature: the Evolution and Genetics of Sexuality. University of California Press, Berkeley, CA.
7. Birky CW, (1996) Heterozygosity, heteromorphy, and phylogenetic trees in asexual eukaryotes. Genetics, 144, 427-437.
8. Blackman RL, (1972) The inheritance of life-cycle differences in Myzus persicae (Sulz.) (Hem., Aphididae). Bulletin of Entomological Research, 62, 281-294.
9. Blackman RL, (1974) Life-cycle variation of Myzus persicae (Sulz.) (Hem., Aphididae) in different parts of the world. Bulletin of Entomological Research, 63, 595-607.
10. Blackman RL, Eastop VF, (2000) Aphids on the World's Crops: An Identification and Information Guide, 2nd edn. p. 228. John Wiley and Sons, Chichester.
11. Blackman RL, Eastop VF, (2007) Taxonomic issues. In: Aphids as Crop Pest (eds, Van Emden H, Harrington R,). CAB International, Wallingford, UK.
12. Bonnet P, van de Peer Y, (2002) ZT: a software tool for simple and partial Mantel tests. Journal of Statistical Software, 7, 1-12. (Pubitemid 39217779)
13. Brevault T, Carletto J, Linderme D, Vanlerberghe-Masutti F, (2008) Genetic diversity of the cotton aphid Aphis gossypii in the unstable environment of a cotton growing area. Agricultural and Forest Entomology, 10, 215-223. (Pubitemid 351977629)
14. Britton NF, Mogie M, (2001) Poor male function favours the coexistence of sexual and asexual relatives. Ecology Letters, 4, 116-121. (Pubitemid 32228507)
15. Carletto J, Martin T, Vanlerberghe-Masutti F, Brevault T, (2010) Insecticide resistance traits differ among and within host races in Aphis gossypii. Pest Management Science, 66, 301-307.
16. Chakraborty R, Jin L, (1993) A unified approach to the study of hypervariable polymorphisms: statistical considerations of determining relatedness and population distances. In: DNA Fingerprinting: State of the Scienc (eds, Pena SDJ, Chakraborty R, Epplen JT, Jeffreys AJ,), pp. 153-175. Birkhäuser, Basel, Switzerland.
17. Charaabi K, Carletto J, Chavigny P, et al. (2008) Genotypic diversity of the cotton-melon aphid Aphis gossypii (Glover) in Tunesia is structured by host plants. Bulletin of Entomological Research, 98, 333-341. (Pubitemid 352019734)
18. Coeur d'Acier A, Sembene M, Audiot P, Rasplus JY, (2004) Polymorphic microsatellites loci in the black Aphid, Aphis fabae Scopoli, 1763 (Hemiptera, Aphididae). Molecular Ecology Notes, 4, 306-308. (Pubitemid 38689018)
19. Dedryver CA, Le Gallic JF, Gauthier JP, Simon JC, (1998) Life cycle of the cereal aphid Sitobion avenae F.: polymorphism and comparison of life history traits associated with sexuality. Ecological Entomology, 23, 123-132. (Pubitemid 28257931)
20. Dedryver CA, Hullé M, Le Gallic JF, Caillaud MC, Simon JC, (2001) Coexistence in space and time of sexual and asexual populations of the cereal aphid Sitobion avenae. Oecologia, 128, 379-388. (Pubitemid 32773944)
21. Dedryver CA, Le Gallic JF, Haack L, et al. (2008) Seasonal and annual genotypic variation and the effect of climate on population genetic structure of the cereal aphid Sitobion avenae in northern France. Bulletin of Entomological Research, 98, 159-168. (Pubitemid 351346263)
22. Delmotte F, Leterme N, Bonhomme J, Rispe C, Simon JC, (2001) Multiple routes to asexuality in an aphid species. Proceedings of the Royal Society of London Series B-Biological Sciences, 268, 2291-2299. (Pubitemid 33096093)
23. Delmotte F, Leterme N, Gauthier JP, Rispe C, Simon JC, (2002) Genetic architecture of sexual and asexual populations of the aphid Rhopalosiphum padi based on allozyme and microsatellite markers. Molecular Ecology, 11, 711-723. (Pubitemid 34443725)
24. Delmotte F, Sabater B, Leterme N, et al. (2003) Phylogenetic evidence for hybrid origins of asexual lineages in an aphid species. Evolution, 57, 1291-1303. (Pubitemid 36821241)
25. Dixon AFG, (1998) Aphid Ecology, 2nd edn. Chapman & Hall, London.
26. Doncaster CP, Pound GE, Cox SJ, (2000) The ecological cost of sex. Nature, 404, 281-285. (Pubitemid 30163544)
27. 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. (Pubitemid 40886055)
28. Excoffier L, Laval G, Schneider S, (2005) Arlequin (version 3.0): An integrated software package for population genetics data analysis. Evolutionary Bioinformatics, 1, 47-50.
29. Falush D, Stephens M, Pritchard JK, (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics, 164, 1567-1587. (Pubitemid 37102217)
30. Feder JL, Berlocher SH, Roethele JB, et al. (2003) Allopatric genetic origins for sympatric host-plant shifts and race formation in Rhagoletis. Proceedings of the National Academy of Sciences, USA, 100, 10314-10319. (Pubitemid 37071875)
31. Fenton B, Woodford JAT, Malloch G, (1998) Analysis of clonal diversity of the peach-potato aphid, Myzus persicae (Sulzer), in Scotland, UK and evidence for the existence of a predominant clone. Molecular Ecology, 7, 1475-1487. (Pubitemid 28504065)
32. Fenton B, Margaritopoulos JT, Malloch GL, Foster SP, (2010) Micro-evolutionary change in relation to insecticide resistance in the peach-potato aphid, Myzus persicae. Ecological Entomology, 35, 131-146.
33. Frantz A, Plantegenest M, Mieuzet L, Simon JC, (2006a) Ecological specialization correlates with genotypic differentiation in sympatric host-populations of the pea aphid. Journal of Evolutionary Biology, 19, 392-401.
34. Frantz A, Plantegenest M, Simon JC, (2006b) Temporal habitat variability and the maintenance of sex in host populations of the pea aphid. Proceedings of the Royal Society B-Biological Sciences, 273, 2887-2891. (Pubitemid 44764374)
35. Gauffre B, Coeur d'Acier A, (2006) New polymorphic microsatellite loci, cross-species amplification and PCR multiplexing in the black aphid, Aphis fabae Scopoli. Molecular Ecology Notes, 6, 440-442. (Pubitemid 43780756)
36. Gilabert A, Simon JC, Mieuzet L, et al. (2009) Climate and agricultural context shape reproductive mode variation in an aphid crop pest. Molecular Ecology, 18, 3050-3061.
37. Goudet J, (2001) FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3). Available from. Updated from Goudet (1995).
38. Guillemaud T, Mieuzet L, Simon JC, (2003) Spatial and temporal genetic variability in French populations of the peach-potato aphid, Myzus persicae. Heredity, 91, 143-152. (Pubitemid 36996663)
39. Haack L, Simon JC, Gauthier JP, Plantegenest M, Dedryver CA, (2000) Evidence for predominant clones in a cyclically parthenogenetic organism provided by combined demographic and genetic analyses. Molecular Ecology, 9, 2055-2066. (Pubitemid 32053340)
40. Hales DF, Tomiuk J, Wöhrmann K, Sunnucks P, (1997) Evolutionary and genetic aspects of aphid biology: a review. European Journal of Entomology, 94, 1-55.
41. Halkett F, Plantegenest M, Prunier-Leterme N, et al. (2005a) Admixed sexual and facultatively asexual aphid lineages at mating sites. Molecular Ecology, 14, 325-336. (Pubitemid 40141498)
42. Halkett F, Simon JC, Balloux F, (2005b) Tackling the population genetics of clonal and partially clonal organisms. Trends in Ecology & Evolution, 20, 194-201. (Pubitemid 40359266)
43. Halkett F, Kindlmann P, Plantegenest M, Sunnucks P, Simon JC, (2006) Temporal differentiation and spatial coexistence of sexual and facultative asexual lineages of an aphid species at mating sites. Journal of Evolutionary Biology, 19, 809-815.
44. Halkett F, Plantegenest M, Bonhomme J, Simon JC, (2008) Gene flow between sexual and facultatively asexual lineages of an aphid species and the maintenance of reproductive mode variation. Molecular Ecology, 17, 2998-3007. (Pubitemid 351793534)
45. Hamilton WD, (1980) Sex versus non-sex versus parasite. Oikos, 35, 282-290.
46. Hardie J, (1980) Reproductive, morphological and behavioral affinities between the alate gynopara and virginopara of the aphid, Aphis fabae. Physiological Entomology, 5, 385-396.
47. Hardie J, Vaz Nunes M, (2001) Aphid photoperiodic clocks. Journal of Insect Physiology, 47, 821-832. (Pubitemid 32587201)
48. Herzog J, Müller CB, Vorburger C, (2007) Strong parasitoid-mediated selection in experimental populations of aphids. Biology Letters, 3, 667-669.
49. Hoffmann AA, Reynolds KT, Nash MA, Weeks AR, (2008) A high incidence of parthenogenesis in agricultural pests. Proceedings of the Royal Society B-Biological Sciences, 275, 2473-2481.
50. Hullé M, Maurice D, Rispe C, Simon JC, (1999) Clonal variability in sequences of morph production during the transition from parthenogenetic to sexual reproduction in the aphid Rhopalosiphum padi (Sternorrhyncha: Aphididae). European Journal of Entomology, 96, 125-134.
51. Iglisch I, (1968) Über die Entstehung der Rassen der 'Schwarzen Bohnenläuse" (Aphis fabae Scop. und verwandte Arten), über ihre phytopathologische Bedeutung und über die Aussichten für erfolgversprechende Bekämpfungsmassnahmen (Homoptera: Aphididae). Mitteilungen aus der Biologischen Bundesanstalt für Land- und Forstwirtschaft Berlin-Dahlem, 131, 1-34.
52. Innes DJ, Hebert PDN, (1988) The origin and genetic basis of obligate parthenogenesis in Daphnia pulex. Evolution, 42, 1024-1035.
53. Jörg E, Lampel G, (1996) Enzyme electrophoretic studies on the Aphis fabae group (Hom., Aphididae). Journal of Applied Entomology, 120, 7-18. (Pubitemid 26263595)
54. Kanbe T, Akimoto SI, (2009) Allelic and genotypic diversity in long-term asexual populations of the pea aphid, Acyrthosiphon pisum in comparison with sexual populations. Molecular Ecology, 18, 801-816.
55. Kondrashov AS, (1988) Deleterious mutations and the evolution of sexual reproduction. Nature, 336, 435-440.
56. Langella O, (1999) Populations 1.2.30. Available at.
57. Le Trionnaire G, Hardie J, Jaubert-Possamai S, Simon JC, Tagu D, (2008) Shifting from clonal to sexual reproduction in aphids: physiological and developmental aspects. Biology of the Cell, 100, 441-451.
58. 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. (Pubitemid 36108104)
59. Llewellyn KS, Loxdale HD, Harrington R, Clark SJ, Sunnucks P, (2004) Evidence for gene flow and local clonal selection in field populations of the grain aphid (Sitobion avenae) in Britain revealed using microsatellites. Heredity, 93, 143-153. (Pubitemid 39027138)
60. Loxdale HD, Lushai G, (2003) Rapid changes in clonal lines: the death of a 'sacred cow'. Biological Journal of the Linnean Society, 79, 3-16. (Pubitemid 36599262)
61. Loxdale HD, Hardie J, Halbert S, et al. (1993) The relative importance of short-range and long-range movement of flying aphids. Biological Reviews of the Cambridge Philosophical Society, 68, 291-311. (Pubitemid 23160587)
62. Loxdale HD, Massonnet B, Schöfl G, Weisser W, (2011) Evidence for a quiet revolution: seasonal variation in colonies of the specialist tansy aphid, Macrosiphonella tanacetaria (Kaltenbach) (Hemiptera: Aphididae) studied using microsatellite markers. Bulletin of Entomological Research, 101, 221-239.
63. Lynch M, (1984) Destabilizing hybridization, general-purpose genotypes, and geographic parthenogenesis. Quarterly Review of Biology, 59, 257-290. (Pubitemid 15277586)
64. Mackenzie A, (1996) A trade-off for host plant utilization in the black bean aphid, Aphis fabae. Evolution, 50, 155-162. (Pubitemid 3035487)
65. Massonnet B, Simon JC, Weisser WW, (2002) Metapopulation structure of the specialized herbivore Macrosiphoniella tanacetaria (Homoptera, Aphididae). Molecular Ecology, 11, 2511-2521. (Pubitemid 35436673)
66. Maynard Smith J, (1978) The Evolution of Sex. Cambridge University Press, Cambridge.
67. Maynard Smith J, (1988) The evolution of recombination. In: The Evolution of Sex: an Examination of Current Idea (eds, Michod RE, Levin BR,), pp. 106-125. Sinauer, Sunderland, MA.
68. de MeeÃs T, Lehmann L, Balloux F, (2006) Molecular epidemiology of clonal diploids: a quick overview and a short DIY (do it yourself) notice. Infection Genetics and Evolution, 6, 163-170. (Pubitemid 43285823)
69. de MeeÃs T, McCoy KD, Prugnolle F, et al. (2007) Population genetics and molecular epidemiology or how to 'débusquer la bête'. Infection Genetics and Evolution, 7, 308-332. (Pubitemid 46172943)
70. Meusel H, Jäger E, Rauschert S, Weinert E, (1978) Vergleichende Chronologie der zentraleuropäischen Flora, Karten-Band II. Fischer Verlag, Jena.
71. Moran NA, (1992) The evolution of aphid life cycles. Annual Review of Entomology, 37, 321-348. (Pubitemid 24406663)
72. Müller FP, (1982) Das Problem Aphis fabae. Zeitschrift für angewandte Entomologie, 94, 432-446.
73. Paland S, Colbourne JK, Lynch M, (2005) Evolutionary history of contagious asexuality in Daphnia pulex. Evolution, 59, 800-813. (Pubitemid 40589290)
74. Papura D, Simon JC, Halkett F, et al. (2003) Predominance of sexual reproduction in Romanian populations of the aphid Sitobion avenae inferred from phenotypic and genetic structure. Heredity, 90, 397-404. (Pubitemid 36610580)
75. Peck JR, (1994) A ruby in the rubbish-beneficial mutations, deleterious mutations and the evolution of sex. Genetics, 137, 597-606. (Pubitemid 24157019)
76. Peck JR, Yearsley JM, Waxman D, (1998) Explaining the geographic distributions of sexual and asexual populations. Nature, 391, 889-892. (Pubitemid 28157665)
77. Pritchard JK, Stephens M, Donnelly P, (2000) Inference of population structure using multilocus genotype data. Genetics, 155, 945-959. (Pubitemid 30397141)
78. Raymond B, Searle JB, Douglas AE, (2001) On the processes shaping reproductive isolation in aphids of the Aphis fabae (Scop.) complex (Aphididae: Homoptera). Biological Journal of the Linnean Society, 74, 205-215. (Pubitemid 33613851)
79. Rice WR, (1989) Analyzing tables of statistical tests. Evolution, 43, 223-225.
80. Rispe C, Pierre JS, (1998) Coexistence between cyclical parthenogens, obligate parthenogens, and intermediates in a fluctuating environment. Journal of Theoretical Biology, 195, 97-110. (Pubitemid 28521911)
81. Rispe C, Pierre JS, Simon JC, Gouyon PH, (1998) Models of sexual and asexual coexistence in aphids based on constraints. Journal of Evolutionary Biology, 11, 685-701. (Pubitemid 28551965)
82. Rispe C, Bonhomme J, Simon JC, (1999) Extreme life-cycle and sex ratio variation among sexually produced clones of the aphid Rhopalosiphum padi (Homoptera: Aphididae). Oikos, 86, 254-264. (Pubitemid 29407499)
83. Rousset F, (1997) Genetic differentiation and estimation of gene flow from F-statistics under isolation by distance. Genetics, 145, 1219-1228. (Pubitemid 27149123)
84. Sandrock C, Vorburger C, (2011) Single-locus recessive inheritance of asexual reproduction in a parasitoid wasp. Current Biology, 21, 433-437.
85. 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. (Pubitemid 29208107)
86. Simon JC, Rispe C, Sunnucks P, (2002) Ecology and evolution of sex in aphids. Trends in Ecology & Evolution, 17, 34-39. (Pubitemid 34076725)
87. Simon JC, Delmotte F, Rispe C, Crease T, (2003) Phylogenetic relationships between parthenogens and their sexual relatives: the possible routes to parthenogenesis in animals. Biological Journal of the Linnean Society, 79, 151-163. (Pubitemid 36590308)
88. Slatkin M, (1974) Hedging ones evolutionary bets. Nature, 250, 704-705.
89. Smith MAH, Mackay PA, (1990) Latitudinal variation in the photoperiodic responses of populations of pea aphid (Homoptera, Aphididae). Environmental Entomology, 19, 618-624.
90. Sokal RR, Rohlf FJ, (1995) Biometry, 3rd edn. W.H. Freeman and Co., San Francisco, CA.
91. Sunnucks P, De Barro PJ, Lushai G, Maclean N, Hales DF, (1997) Genetic structure of an aphid studied using microsatellites: cyclic parthenogenesis, differentiated lineages and host specialization. Molecular Ecology, 6, 1059-1073.
92. Tank A, Wijngaard JB, Konnen GP, et al. (2002) Daily dataset of 20th-century surface air temperature and precipitation series for the European Climate Assessment. International Journal of Climatology, 22, 1441-1453. (Pubitemid 35288961)
93. Tas ICQ, Van Dijk PJ, (1999) Crosses between sexual and apomictic dandelions (Taraxacum). I. The inheritance of apomixis. Heredity, 83, 707-714. (Pubitemid 30044774)
94. Thieme T, (1987) Members of the complex of Aphis fabae Scop. and their host plants. In: Population Structure, Genetics and Taxonomy of Aphids and Thysanopter (eds, Holmann J, Pelikan J, Dixon AFG, Weisman L,), pp. 314-323. SPB Academic Publishing, The Hague.
95. Thieme T, (1988) On the Biology of Aphis fabae mordwilkowi Börner and Janisch, 1922 (Hom, Aphididae). Journal of Applied Entomology-Zeitschrift für angewandte Entomologie, 105, 510-515.
96. Thieme T, Dixon AFG, (1996) Mate recognition in the Aphis fabae complex: daily rhythm of release and specificity of sex pheromones. Entomologia Experimentalis Et Applicata, 79, 85-89.
97. Vandel A, (1928) La parthénogenäse géographique. Contribution à l'étude biologique et cytologique de la parthénogenäse naturelle. Bulletin Biologique de la France et de la Belgique, 62, 164-281.
98. Vaz Nunes M, Hardie J, (2000) On critical night lengths and temperature compensation in the photoperiodic response of two geographical clones of the black bean aphid, Aphis fabae. Physiological Entomology, 25, 303-308. (Pubitemid 32053293)
99. Via S, (1999) Reproductive isolation between sympatric races of pea aphids. I. Gene flow restriction and habitat choice. Evolution, 53, 1446-1457. (Pubitemid 29524139)
100. Vialatte A, Dedryver CA, Simon JC, Galman M, Plantegenest M, (2005) Limited genetic exchanges between populations of an insect pest living on uncultivated and related cultivated host plants. Proceedings of the Royal Society B-Biological Sciences, 272, 1075-1082. (Pubitemid 40943958)
101. Vorburger C, (2006) Temporal dynamics of genotypic diversity reveal strong clonal selection in the aphid Myzus persicae. Journal of Evolutionary Biology, 19, 97-107.
102. Vorburger C, Lancaster M, Sunnucks P, (2003) Environmentally related patterns of reproductive modes in the aphid Myzus persicae and the predominance of two 'superclones' in Victoria, Australia. Molecular Ecology, 12, 3493-3504. (Pubitemid 37496709)
103. Walsh PS, Metzgar DA, Higuchi R, (1991) Chelex 100 as a medium for the simple extraction of DNA for PCR-based typing from forensic material. BioTechniques, 10, 506-513.
104. Walther GR, Post E, Convey P, et al. (2002) Ecological responses to recent climate change. Nature, 416, 389-395. (Pubitemid 34272866)
105. Weir BS, Cockerham CC, (1984) Estimating F-statistics for the analysis of population structure. Evolution, 38, 1358-1370. (Pubitemid 16277759)
106. Williams GC, (1975) Sex and Evolution, Princeton University Press, Princeton, NJ.
107. Wöhrmann K, Tomiuk J, (1988) Life-cycle strategies and genotypic variability in populations of aphids. Journal of Genetics, 67, 43-52.