The pea aphid, Acyrthosiphon pisum: An emerging genomic model system for ecological, developmental and evolutionary studies

BioEssays

Volumn 28, Issue 7, 2006, Pages 747-755

  Brisson, Jennifer A ^a   Stern, David L ^a  

^a PRINCETON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACYRTHOSIPHON PISUM; APHID; DEVELOPMENTAL STAGE; ECOLOGY; EVOLUTION; GENETIC ANALYSIS; GENOMICS; NONHUMAN; PHENOTYPE; POPULATION RESEARCH; REVIEW; VIRUS TRANSMISSION;

ADAPTATION, BIOLOGICAL; ANIMALS; APHIDS; BIOLOGICAL EVOLUTION; ECOLOGY; EVOLUTION; FEMALE; GENOME, INSECT; LIFE CYCLE STAGES; MALE; MODELS, GENETIC; PEAS; PLANT VIRUSES; POLYMORPHISM, GENETIC; SYMBIOSIS;

ACYRTHOSIPHON PISUM; APHIDIDAE; BACTERIA (MICROORGANISMS);

EID: 33747505101     PISSN: 02659247     EISSN: None     Source Type: Journal    
DOI: 10.1002/bies.20436     Document Type: Review

References (91)

1. Heie OE. 1987. Paleontology and phylogeny. In: Minks AK, Harrewijn P, editors. Aphids: Their Biology, Natural Enemies, and Control. Amsterdam: Elsevier.
2. Heie OE. 1996. The evolutionary history of aphids and a hypothesis on the coevolution of aphids and plants. Bollettino Di Zoologia Agraria E Di Bachicoltura 28:149-155.
3. Von Dohlen CD, Moran NA. 2000. Molecular data support a rapid radiation of aphids in the Cretaceous and multiple origins of host alternation. Biol J Linn Soc 4:689-717.
4. Blackman RL, Eastop VF. 2000. Aphids on the world's crops: an identification and information guide. Chichester: John Wiley & Sons Ltd.
5. Oerke EC. 1994. Estimated losses in major food and cash crops. In: Oerke EC, Dehne HW, Schonbeck F, Weber A, editors. Crop production and crop protection. Amsterdam: Elsevier.
6. Dixon AFG. 1998. Aphid Ecology. London, UK: Chapman & Hall.
7. Minks AK, Harrewijn P. 1980. Aphids, their biology, natural enemies, and control. Amsterdam: Elsevier.
8. Heie OE. 1980. The Aphidoidea (Hemiptera) of Fennoscandia and Denmark. 1. General Part. The families Mindaridae, Hormaphididae, Thelaxidae, Anoeciidae, and Pemphigidae. Fauna Ent. Scandinavica 9:
9. Moran NA. 1992. The evolution of aphid life cycles. Ann Rev Ent 37:321-348.
10. Blackman RL, Eastop VF. 1994. Aphids on the world's trees: an identification and information guide. Wallingford: CAB International.
11. Blackman RL. 1981. Aphid genetics and host plant resistance. Bull. SROP 4:13-19.
12. Caillaud MC, Via S. 2000. Specialized feeding behavior influences both ecological specialization and assortative mating in sympatric host races of pea aphids. Am Nat 156:606-621.
13. Blackman RL. 1987. Reproduction, cytogenetics and development. In: Minks AK, Harrewijn P, editors. Aphids: Their biology, natural enemies & control. Amsterdam: Elsevier.
14. Orlando E. 1974. Sex determination in Megoura viciae Buckton (Homoptera, Aphididae). Monitore Zoologico Italiano (N.S.) 8:61-70.
15. Wilson ACC, Sunnucks P, Hales DF. 1997. Random loss of X chromosome at male determination in an aphid, Sitobion near fragariae, detected using an X-linked polymorphic microsatellite marker. Genet Res 69:233-236.
16. Caillaud MC, Boutin M, Braendle C, Simon J-C. 2002. A sex-linked locus controls wing polymorphism in males of the pea aphid, Acyrthosiphon pisum (Harris). Heredity 89:346-352.
17. Shingleton AW, Sisk GC, Stern DL. 2003. Diapause in the pea aphid (Acyrthosiphon pisum) is a slowing but not a cessation of development. BMC Dev Biol 3:7.
18. Sutherland ORW. 1969. The role of crowding in the production of winged forms by two strains of the pea aphid, Acyrthosiphon pisum. J Insect Phys 15:1385-1410.
19. Mackauer M, Nair KK, Unnithan GC. 1979. Effect of precocene II on alate production in the pea aphid, Acyrthosiphon pisum. Can J Zool 57:856-859.
20. Braendle C, Caillaud MC, Stern DL. 2005. Genetic mapping of aphicarus - a sex-linked locus controlling a wing polymorphism in the pea aphid (Acyrthosiphon pisum). Heredity 94:435-442.
21. Hawthorne DJ, Via S. 2001. Genetic linkage of ecological specialiazation and reproductive isolation in pea aphids. Nature 412:904-907.
22. Via S, Hawthorne DJ. 2002. The genetic architecture of ecological specialization: correlated gene effects on host use and habitat choice in pea aphids. Am Nat 159:376-388.
23. Wheeler DE. 1986. Developmental and physiological determinants of caste in social Hymenoptera: evolutionary implications. Am Nat 128:13-34.
24. Shapiro AM. 1976. Seasonal polyphenism. Evolutionary Biology 9:259-333.
25. Emlen DJ. 1994. Environmental control of horn length dimorphism in the beetle Onthophagus acuminatus (Coleoptera: Scarabaeidae). Proc R Soc Lond Ser B 256:131-136.
26. Stern DL, Foster WA. 1996. The evolution of soldiers in aphids. Biol Rev Cambridge Phil Soc 71:27-79.
27. Essig EO, Abernathy F. 1952. The aphid genus Periphyllus (Family Aphidae); a systematic, biological, and ecological study. Berkeley: University of California Press.
28. Zera AJ, Denno RF. 1997. Physiology and ecology of dispersal polymorphism in insects. Ann Rev Ent 42:207-230.
29. Kring JB. 1977. Structure of the eyes of the pea aphid, Acyrthosiphon pisum. Annals Ent Soc Am 70:855-860.
30. Muller CB, Williams IS, Hardie J. 2001. The role of nutrition, crowding, and interspecific interactions in the development of winged aphids. Ecol Ent 26:330-340.
31. Sloggett JJ, Weisser WW. 2002. Parasitoids induce production of the dispersal morphs of the pea aphid, Acyrthosiphon pisum. Oikos 98:323-333.
32. Podjasek JO, Bosnjak LM, Booker DJ, Mondor EB. 2005. Alarm pheromone induces a transgenerational wing polyphenism in the pea aphid, Acyrthosiphon pisum. Can J Zool 83:1138-1141.
33. Kunert G, Otto S, Rose USR, Gershenzon J, Weisser WW. 2005. Alarm pheromone mediates production of winged dispersal morphs in aphids. Ecol Letters 8:596-603.
34. Tsuji H, Kawaka K. 1987. Development and degeneration of wing buds and indirect flight muscles in the pea aphid (Acyrtosiphon pisum (Harris)). Jap J Applied Ent Zool 31:247-252.
35. Hille Ris Lambers L. 1966. Polymorphism in the Aphididae. Ann Rev Ent 11:47-78.
36. Lees AD. 1966. The control of polymorphism in aphids. Adv Ins Phys 3:207-277.
37. Braendle C, Friebe I, Caillaud MC, Stern DL. 2005. Genetic variation for an aphid wing polyphenism is genetically linked to naturally occurring wing polymorphism. Proc Roy Soc London B 272:657-665.
38. Abouheif E, Wray GA. 2002. Evolution of the gene network underlying wing polyphenism in ants. Science 297:249-252.
39. Hardie J. 1980. Juvenile hormone mimics the photoperiodic apterization of the alate gynopara of the aphid Aphis fabae. Nature 286:602-604.
40. Johannsen OA, Butt FH. 1941. Embryology of insects and myriapods. New York: McGraw-Hill Book Co Inc.
41. Miura T, Braendle C, Shingleton A, Sisk G, Kambhampati S, et al. 2003. A comparison of parthenogenetic and sexual embryogenesis of the pea aphid Acyrthosiphon pisum (Hemiptera: Aphidoidea). J Exp Zool B Mol Dev Evol 295B:59-81.
42. Dixon AFG. 1990. Evolutionary aspects of parthenogenetic reproduction in aphids. Acta Phytopath. Entomol. Hung 25:41-56.
43. Blackman RL. 1978. Early development of the parthenogenetic egg in three species of aphids (Homoptera: Aphididae). Int J Insect Morphol Embryol 7:33-44.
44. Blackman RL. 1979. Stability and variation in aphid clonal lineages. Biol J Linnean Soc 11:259-277.
45. Simon JC, Rispe C, Sunnucks P. 2002. Ecology and evolution of sex in aphids. Trends Ecol Evol 17:34-39.
46. Simon JC, Delmotte F, Rispe C, Crease T. 2003. Phylogenetic relationships between parthenogens and their sexual relatives: the possible routes to parthenogenesis in animals. Biol J Linn Soc 79:151-163.
47. Maynard Smith J. 1978. The evolution of sex. Cambridge University Press.
48. Williams GC. 1975. Sex and Evolution. Princeton: Princeton University Press.
49. Baumann P, Moran NA, Baumann L. 2000. Bacteriocyte-associated endosymbionts of insects. In: Dworkin M, editor. The Prokaryotes. New York: Springer.
50. Wernegreen JJ. 2002. Genome evolution in bacterial endosymbionts of insects. Nature Rev Genet 3:850-861.
51. Moran NA, Wernegreen JJ. 2000. Lifestyle evolution in symbiotic bacteria: insights from genomics. Trends Ecol Evol 8:321-326.
52. Klasson L, Andersson SGE. 2004. Evolution of minimal-gene-sets in host-dependent bacteria. Trends Microb 12:37-43.
53. Shigenobu S, Watanabe H, Httori M, Sakaki Y, Ishikawa H. 2000. Genome sequence of the endocellular bacterial symbiont of aphids Buchnera sp. APS. Nature 407:81-86.
54. Tamas I, Klasson L, Canback B, Naslund AK, Eriksson AS, et al. 2002. 50 million years of genomic stasis in endosymbiotic bacteria. Science 296:2376-2379.
55. van Ham RCHJ, Kamerbeek J, Palacio C, Rausell C. 2003. Reductive genome evolution in Buchnera aphidicola. Proc Nat Acad Sci USA 100:
56. Buchner P. 1965. Endosymbiosis of animals with plant microorganisms. New York: Interscience Publishers, Inc.
57. Braendle C, Miura T, Bickel R, Shingleton AW, Kambhampati S, et al. 2003. Developmental origin and evolution of bacteriocytes in the aphid-Buchnera symbiosis. Plos Biology 1:70-76.
58. Montllor CB, Maxmen A, Purcell AH. 2002. Facultative bacterial endosymbionts benefit pea aphids, Acyrthosiphon pisum, under heat strees. Ecol Ent 27:189-195.
59. Oliver KM, Russell JA, Moran NA, Hunter MS. 2003. Facultative bacterial symbionts in aphids confer resistance to parasitic wasps. Proc Nat Acad Sci USA 100:1803-1807.
60. Kerry OM, Moran NA, Hunter MS. 2005. Variation in resistance to parasitism in aphids is due to symbionts not host genotype. Proc Nat Acad Sci USA 102:12795-12800.
61. Tsuchida T, Koga R, Fukatsu T. 2004. Host plant specialization governed by facultative symbiont. Science 303:1989-1989.
62. Leonardo TE, Mondor EB. 2005. Symbiont modifies host life history traits that affect gene flow. Proc R Soc Lond Ser B in press.
63. Ono M, Swanson JJ, Field LM, Devonshire AL, Siegfried BD. 1999. Amplification and methylation of an esterase gene associated with insecticide-resistance in greenbugs, Schizaphis graminum (Rondani) (Homoptera:Aphididae). Insect Bioch Mol Biol 29:1065-1073.
64. Loxdale HD, Brookes CP, Wynne IR, Clark SJ. 1998. Genetic variability within and between English populations of the damson-hop aphid, Phorodon humuli (Hemiptera: Aphididae), with special reference to esterases associated with insecticide resistance. Bull. Ent Res 88:513-526.
65. Barber MD, Moores GD, Tatchell GM, Vice WE, Denholm I. 1999. Insecticide resistance in the current-lettuce aphid, Nasonovia ribisnigri (Hemiptera: Aphididae) in the U.K. Bull Ent Res 89:17-23.
66. Wang KY, Liu TX, Yu CH, Jiang XY, Yi MQ. 2002. Resistance of Aphis gosypii (Homoptera: Aphididae) to fenvalerate and imidacloprid and activities of detoxification enzymes on cotton and cucumber. J Econ Ent 95:407-413.
67. Field LM, Devonshire AL, Forde BG. 1988. Molecular evidence that insecticide resistance in peach-potato aphids (Myzus persicae Sulz.) results from amplification of an esterase gene. Biochem J 251:309-312.
68. Field LM, Foster SP. 2002. Amplified esterase genes and their relationship with other insecticide resistance mechanisms in English field populations of the aphids, Myzus persica (sulzer). Pest Management Science 58:889-894.
69. Gao JR, Kambhampati S, Zhu KY. 2002. Molecular cloning and characterisation of a greenbus (Schizaphis graminum) cDNA encoding acetylcholinesterase possibly evolved from a duplicate gene lineage. Ins Biochem Mol Biol 32:765-775.
70. Thompson M, Steichen JC, Ffrenchconstant RH. 1995. Conservation of Cyclodiene Insecticide Resistance-Associated Mutation in Insects (Vol 2, Pg 149, 1993). Insect Mol Biol 4:124-124.
71. Martinez-Torres D, Foster SP, Field LM, Devonshire AL, Williamson MS. 1999. A sodium channel point mutation is associated with resistance to DDT and pyrethroid insecticides in the peach-potato aphid, Myzus persicae (Sulzer) (Hemiptera: Aphididae). Insect Mol Biol 8:339-346.
72. Andrews MC, Callaghan A, Field LM, Williamson MS, Moores GD. 2004. Identification of mutations conferring insecticide-insensitive AChE in the cotton-melon aphid, Aphis gossypii Glover. Insect Mol Biol 13:555-561.
73. Via S. 1994. Population structure and local adaptation in a clonal herbivore. In: Real LA, editor. Ecological Genetics. Princeton, NJ: Princeton University Press.
74. Via S. 1991. The genetic structure of host plant adaptation in a spatial patchwork: demographic variability among reciprocally transplanted pea aphid clones. Evolution 45:827-852.
75. Via S. 1999. Reproductive isolation between sympatric races of pea aphids. I. Gene flow restriction and habitat choice. Evolution 53:1446-1457.
76. Pickett JA, Wadhams LJ, Woodcock CM, Hardie J. 1992. The Chemical Ecology of Aphids. Annual Review of Entomology 37:67-90.
77. Hekmat-Scafe DS, Scafe CR, McKinney AJ, Tanouye MA. 2002. Genome-wide analysis of the odorant-binding protein gene family in Drosophila melanogaster. Genome Res 12:1357-1369.
78. Zhou JJ, Huang WS, Zhang GA, Pickett JA, Field LM. 2004. "Plus-C" odorant-binding protein genes in two Drosophila species and the malaria mosquito Anopheles gambiae. Gene 327:117-129.
79. Gao Q, Chess A. 1999. Identification of candidate Drosophila olfactory receptors from genomic DNA sequence. Genomics 60:31-39.
80. Kim J, Carlson JR. 2002. Gene discovery by e-genetics: Drosophila odor and taste receptors. J Cell Science 115:1107-1112.
81. Jacobs SP, Liggins AP, Zhou JJ, Pickett JA, Jin X, et al. 2005. OS-D-like genes and their expression in aphids (Hemiptera: Aphididae). Insect Mol Biol 14:423-432.
82. Robert Y. 1987. Dispersion and migration. In: Minks AK, Harrewijn P, editors. Aphids, their biology, natural enemies, and control. Amsterdam, Netherlands: Elsevier.
83. Pirone TP, Blanc S. 1996. Helper-dependent vector transmission of plant viruses. Ann Rev Phytopath 34:227-247.
84. Liu S, He X, Park G, Josefsson C, Perry KL. 2002. A conserved capsid protein surface domain of cucumber mosaic virus is essential for efficient aphid vector transmission. J Virol 76:9756-9762.
85. Bauwe H and Kolukisaoglu U. 2003. Genetic manipulation of glycine decarboxylation. J Exp Bot 54:1523-1535.
86. Garret A, Kerlan C, Thomas D. 1996. Ultrastructural study of acquisition and retention of potato leafroll luteovirus in the alimentary canal of its aphid vector, Myzus persicae Sulz Arch Vir 141:1279-1292.
87. Peiffer ML, FGildow FE, Gray SM. 1997. Two distinct mechanisms regulate luteovirus transmission efficiency and specificity at the aphid salivary gland. J Gen Virol 78:495-503.
88. van den Heuvel JFJM, Verbeek M, van der Wilk F. 1994. Endosymbiotic bacteria associated with circulative transmission of potato leafroll virus by Myzus persicae. J Gen Virol 75:2559-2565.
89. van den Heuvel JFJM, Bruyere A, Hogenhout SA, Ziegler-Graff V, Brault V, et al. 1997. The N-terminal region of the luteovirus readthrough domain determines virus binding to Buchnera GroEL and is essential for virus persistence in the aphid. J Virol 71:7258-7265.
90. Li C, Cox-Foster D, Gray SM, Gildow F. 2001. Vector specificity of barley yellow dwarf virus (BYDV) transmission: identification of potential cellular receptors binding BYDV-MAV in the aphid, Sitobion avenae. Virology 286:125-133.
91. Gray SM, Gildow F. 2003. Luteovirus-aphid interactions. Ann Rev Phytopath 41:539-566.