Levels of clonal mixing in the black bean aphid Aphis fabae, a facultative ant mutualist

Molecular Ecology

Volumn 20, Issue 22, 2011, Pages 4772-4785

  Vantaux, Amélie ^a   Billen, J ^a   Wenseleers, T ^a  

^a UNIVERSITY OF LEUVEN   (Belgium)

Author keywords

Competition; Dispersal; Hemiptera; Kin structure; Relatedness

Indexed keywords

MICROSATELLITE DNA;

ANIMAL; ANT; APHID; ARTICLE; DNA SEQUENCE; GENETIC VARIABILITY; GENETICS; GENOTYPING TECHNIQUE; PHYSIOLOGY; SPECIES DIFFERENCE;

ANIMALS; ANTS; APHIDS; GENETIC VARIATION; GENOTYPING TECHNIQUES; MICROSATELLITE REPEATS; SEQUENCE ANALYSIS, DNA; SPECIES SPECIFICITY;

EID: 83555162295     PISSN: 09621083     EISSN: 1365294X     Source Type: Journal    
DOI: 10.1111/j.1365-294X.2011.05204.x     Document Type: Article

References (99)

1. Abbot P (2009) On the evolution of dispersal and altruism in aphids. Evolution, 63, 2687-2696.
2. Abbot P, Withgott JH, Moran NA (2001) Genetic conflict and conditional altruism in social aphid colonies. Proceedings of the National Academy of Sciences of the United States of America, 98, 12068-12071.
3. Allee WC (1931) Animal Aggregations, A Study in General Sociology. The University Chicago Press, Chicago, IL.
4. Angulo E, Roemer GW, Berec L, Gascoigne J, Courchamp F (2007) Double allee effects and extinction in the island fox. Conservation Biology, 21, 1082-1091.
5. 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.
6. Berec L, Angulo E, Courchamp F (2007) Multiple Allee effects and population management. Trends in Ecology & Evolution, 22, 185-191.
7. Blackmer JL, Rodriguez-Saona C, Byers JA, Shope KL, Smith JP (2004) Behavioral response of Lygus hesperus to conspecifics and headspace volatiles of alfalfa in a Y-tube olfactometer. Journal of Chemical Ecology, 30, 1547-1564.
8. Braendle C, Davis GK, Brisson JA, Stern DL (2006) Wing dimorphism in aphids. Heredity, 97, 192-199.
9. 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.
10. Courchamp F, Macdonald DW (2001) Crucial importance of pack size in the African wild dog Lycaon pictus. Animal Conservation, 4, 169-174.
11. David CT, Hardie J (1988) The visual responses of free-flying summer and autumn forms of the black bean aphid, Aphis fabae, in an automated flight chamber. Physiological Entomology, 13, 277-284.
12. De Barro PJ, Sherratt TN, Carvalho GR et al. (1994) An analysis of secondary spread by putative clones of Sitobion avenae within a Hampshire wheat field using the multilocus (GATA)4 probe. Insect Molecular Biology, 3, 253-260.
13. De Meester L, Vanoverbeke J (1999) An uncoupling of male and sexual egg production leads to reduced inbreeding in the cyclical parthenogen Daphnia. Proceedings of the Royal Society of London Series B-Biological Sciences, 266, 2471-2477.
14. Detrain C, Verheggen FJ, Diez L, Wathelet B, Haubruge E (2010) Aphid-ant mutualism: how honeydew sugars influence the behaviour of ant scouts. Physiological Entomology, 35, 168-174.
15. Dixon AFG (1977) Aphid ecology: life-cycles, polymorphism, and population regulation. Annual Review of Ecology and Systematics, 8, 329-353.
16. Dixon AFG (1998) Aphid Ecology: An Optimization Approach, 2nd edn. Chapman and Hall, London.
17. Dixon AFG, Agarwala BK (1999) Ladybird-induced life-history changes in aphids. Proceedings of the Royal Society of London Series B-Biological Sciences, 266, 1549-1553.
18. Dixon AFG, Wratten SD (1971) Laboratory studies on aggregation, size and fecundity in black bean aphid, Aphis fabae Scop. Bulletin of Entomological Research, 6, 97-111.
19. 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.
20. Ferrari J, Via S, Godfray HCJ (2008) Population differentiation and genetic variation in performance on eight hosts in the pea aphid complex. Evolution, 62, 2508-2524.
21. Fischer MK, Hoffmann KH, Völkl W (2001) Competition for mutualists in an ant-homopteran interaction mediated by hierarchies of ant attendance. Oikos, 92, 531-541.
22. Fletcher RJ (2006) Emergent properties of conspecific attraction in fragmented landscapes. American Naturalist, 168, 207-219.
23. Frank SA (1986) Dispersal polymorphisms in subdivided populations. Journal of Theoretical Biology, 122, 303-309.
24. Frati F, Salerno G, Conti E, Bin F (2008) Role of the plantconspecific complex in host location and intra-specific communication of Lygus rugulipennis. Physiological Entomology, 33, 129-137.
25. Gauffre B, D’Acier AC (2006) New polymorphic microsatellite loci, cross-species amplification and PCR multiplexing in the black aphid, Aphis fabae Scopoli. Molecular Ecology Notes, 6, 440-442.
26. 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.
27. Hamilton WD (1964a) Genetical evolution of social behaviour 1. Journal of Theoretical Biology, 7, 1-16.
28. Hamilton WD (1964b) Genetical evolution of social behaviour 2. Journal of Theoretical Biology, 7, 17-52.
29. Hamilton WD (1987) Kinship, recognition, disease and intelligence: constraints of social evolution. In: Animal Societies: Theories & Facts (eds Ito Y, Brown JL, Kikkawa J), pp. 81-102. Japan Scientific Societies Press, Tokyo.
30. Hamilton WD, May RM (1977) Dispersal in stable habitats. Nature, 269, 578-581.
31. Hardy OJ, Vekemans X (2002) SPAGEDi: a versatile computer program to analyse spatial genetic structure at the individual or population levels. Molecular Ecology Notes, 2, 618-620.
32. Harrington R, Taylor LR (1990) Migration for survival: finescale population redistribution in an Aphid, Myzus persicae. Journal of Animal Ecology, 59, 1177-1193.
33. Harrison RG (1980) Dispersal polymorphisms in insects. Annual Review of Ecology and Systematics, 11, 95-118.
34. 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.
35. Hatano E, Kunert G, Weisser WW (2010) Aphid wing induction and ecological costs of alarm pheromone emission under field conditions. PLoS ONE, 5, e11188.
36. Hodgson C (1991) Dispersal of apterous aphids (Homopetera, aphididae) from their host plant and its significance. Bulletin of Entomological Research, 81, 417-427.
37. Hodgson DJ (2001) Monoclonal aphid colonies and the measurement of clonal fitness. Ecological Entomology, 26, 444-448.
38. Howard MT, Dixon AFG (1992) The effect of plant phenology on the induction of alatae and the development of populations of Metopolophium dirhodum (Walker), the rose grain aphid, on winter wheat. Annals of Applied Biology, 120, 203-213.
39. Johnson PCD, Whitfield JA, Foster WA, Amos W (2002) Clonal mixing in the soldier-producing aphid Pemphigus spyrothecae (Hemiptera: Aphididae). Molecular Ecology, 11, 1525-1531.
40. Krause J, Ruxton G (2002) Living in Groups. Oxford University Press, New York.
41. Kunert G, Otto S, Rose USR, Gershenzon J, Weisser WW (2005) Alarm pheromone mediates production of winged dispersal morphs in aphids. Ecology Letters, 8, 596-603.
42. Kunert G, Trautsch J, Weisser WW (2007) Density dependence of the alarm pheromone effect in pea aphids, Acyrthosiphon pisum (Sternorrhyncha: Aphididae). European Journal of Entomology, 104, 47-50.
43. Kunert G, Schmoock-Ortlepp K, Reissmann U, Creutzburg S, Weisser WW (2008) The influence of natural enemies on wing induction in Aphis fabae and Megoura viciae (Hemiptera: Aphididae). Bulletin of Entomological Research, 98, 57-62.
44. Lande R (1996) Statistics and partitioning of species diversity, and similarity among multiple communities. Oikos, 76, 5-13.
45. Lees AD (1966) The control of polymorphism in aphids. In: Advances in Insect Physiology (eds Beament JWL, Treherne JE, Wigglesworth VB), pp. 207-277. Academic Press, London.
46. Loxdale HD (2008) The nature and reality of the aphid clone: genetic variation, adaptation and evolution. Agricultural and Forest Entomology, 10, 81-90.
47. Loxdale HD, Brookes CP (1990) Temporal genetic stability within and restricted migration (gene flow) between local populations of the blackberry-grain aphid Sitobion fragariae in South-East England. Journal of Animal Ecology, 59, 497-514.
48. Loxdale HD, Massonnet B, Schofl G, Weisser WW (2011) Evidence for a quiet revolution: seasonal variation in colonies of the specialist tansy aphid, Macrosiphoniella tanacetaria (Kaltenbach) (Hemiptera: Aphididae) studied using microsatellite markers. Bulletin of Entomological Research, 101, 221-239.
49. Mackenzie A (1996) A trade-off for host plant utilization in the black bean aphid, Aphis fabae. Evolution, 50, 155-162.
50. Massonnet B, Weisser WW (2004) Patterns of genetic differention between populations of the specialized herbivore Macrosiphoniella tanacetaria (Homoptera, Aphididae). Heredity, 93, 577-584.
51. Michaud JP, Jyoti JL, Qureshi JA (2006) Positive correlation of fitness with group size in two biotypes of Russian wheat aphid (Homoptera: Aphididae). Journal of Economic Entomology, 99, 1214-1224.
52. Minks AK, Harrewijn P (1987) Aphids. Their Biology, Natural Enemies and Control. Elsevier, Amsterdam, The Netherlands.
53. Moran NA (1992) The evolution of aphid life cycles. Annual Review of Entomology, 37, 321-348.
54. Mousseau TA, Dingle H (1991) Maternal effects in insect life histories. Annual Review of Entomology, 36, 511-534.
55. Müller CB, Williams IS, Hardie J (2001) The role of nutrition, crowding and interspecific interactions in the development of winged aphids. Ecological Entomology, 26, 330-340.
56. Nielsen R, Tarpy DR, Reeve HK (2003) Estimating effective paternity number in social insects and the effective number of alleles in a population. Molecular Ecology, 12, 3157-3164.
57. Nottingham SF, Hardie J, Dawson GW et al. (1991) Behavioral and electrophysiological responses of aphids to host and nonhost plant volatiles. Journal of Chemical Ecology, 17, 1231-1242.
58. Offenberg J (2001) Balancing between mutualism and exploitation: the symbiotic interaction between Lasius ants and aphids. Behavioral Ecology and Sociobiology, 49, 304-310.
59. Ozaki K (1995) Intergall migration in aphids; a model and a test of ESS dispersal rate. Evolutionary Ecology, 9, 542-549.
60. Perrin N, Goudet J (2001) Inbreeding, kinship, and the evolution of natal dispersal. In: Dispersal (eds Clobert J, Danchin E, Dhondt AA, Nichols JD), pp. 123-142. Oxford University Press, Oxford.
61. Pickett JA, Wadhams LJ, Woodcock CM, Hardie J (1992) The chemical ecology of aphids. Annual Review of Entomology, 37, 67-90.
62. Pike N, Foster WA (2008) The ecology of altruism in a clonal insect. In: Ecology of Social Evolution (eds Korb J, Heinze J), pp. 37-56. Springer-Verlag, Berlin.
63. Plantegenest M, Kindlmann P (1999) Evolutionarily stable strategies of migration in heterogeneous environments. Evolutionary Ecology, 13, 229-244.
64. Powell G, Hardie J (2001) The chemical ecology of aphid host alternation: how do return migrants find the primary host plant? Applied Entomology and Zoology, 36, 259-267.
65. Powell G, Maniar SP, Pickett JA, Hardie J (1999) Aphid responses to non-host epicuticular lipids. Entomologia Experimentalis Et Applicata, 91, 115-123.
66. Queller DC, Goodnight KF (1989) Estimating relatedness using genetic markers. Evolution, 43, 258-275.
67. Qureshi JA, Michaud JP (2005) Comparative biology of three cereal aphids on TAM 107 wheat. Environmental Entomology, 34, 27-36.
68. Ronce O, Gandon S, Rousset F (2000) Kin selection and natal dispersal in an age-structured population. Theoretical Population Biology, 58, 143-159.
69. Shibao H (1998) Social structure and the defensive role of soldiers in a eusocial bamboo aphid, Pseudoregma bambucicola (Homoptera: Aphididae): a test of the defenceoptimization hypothesis. Researches on Population Ecology, 40, 325-333.
70. Shibao H (1999) Reproductive schedule and factors affecting soldier production in the eusocial bamboo aphid Pseudoregma bambucicola (Homoptera, Aphididae). Insectes Sociaux, 46, 378-386.
71. Shufran KA, Black WC, Margolies DC (1991) DNA fingerprinting to study spatial and temporal distributions of an aphid, Schizaphis graminum (Homoptera: Aphididae). Bulletin of Entomological Research, 81, 303-313.
72. Simon J-C, Stoeckel S, Tagu D (2010) Evolutionary and functional insights into reproductive strategies of aphids. Comptes Rendus Biologies, 333, 488-496.
73. Sloggett JJ, Weisser WW (2002) Parasitoids induce production of the dispersal morph of the pea aphid, Acyrthosiphon pisum. Oikos, 98, 323-333.
74. Stadler B, Dixon AFG (1998) Costs of ant attendance for aphids. Journal of Animal Ecology, 67, 454-459.
75. Stadler B, Dixon AFG (1999) Ant attendance in aphids: why different degrees of myrmecophily? Ecological Entomology, 24, 363-369.
76. Stadler B, Dixon AFG (2005) Ecology and evolution of aphidant interactions. Annual Review of Ecology Evolution and Systematics, 36, 345-372.
77. Stadler B, Dixon AFG, Kindlmann P (2002) Relative fitness of aphids: effects of plant quality and ants. Ecology Letters, 5, 216-222.
78. Stadler B, Kindlmann P, Smilauer P, Fiedler K (2003) A comparative analysis of morphological and ecological characters of European aphids and lycaenids in relation to ant attendance. Oecologia, 135, 422-430.
79. Stern DL, Foster WA (1996) The evolution of soldiers in aphids. Biological Reviews of the Cambridge Philosophical Society, 71, 27-79.
80. Stroyan HLG (1984) Aphids-Pterocommatinae and Aphidinae (Aphidini), Homoptera, Aphididae. Royal Entomological Society of London, London.
81. Sutherland ORW (1969) The role of crowding in the production of winged forms by two strains of the pea aphid, Acyrthosiphon pisum. Journal of Insect Physiology, 15, 1385-1410.
82. Taylor PD (1988) An inclusive fitness model for dispersal of offspring. Journal of Theoretical Biology, 130, 363-378.
83. Turchin P, Kareiva P (1989) Aggregation in Aphis varians: an effective strategy for reducing predation risk. Ecology, 70, 1008-1016.
84. Vanlerberghe-Masutti F, Chavigny P, Fuller SJ (1999) Characterization of microsatellite loci in the aphid species Aphis gossypii Glover. Molecular Ecology, 8, 693-695.
85. Vercken E, Kramer AM, Tobin PC, Drake JM (2011) Critical patch size generated by Allee effect in gypsy moth, Lymantria dispar (L.). Ecology Letters, 14, 179-186.
86. Verheggen FJ, Haubruge E, De Moraes CM, Mescher MC (2009) Social environment influences aphid production of alarm pheromone. Behavioral Ecology, 20, 283-288.
87. 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.
88. Via S (2009) Natural selection in action during speciation. Proceedings of the National Academy of Sciences of the United States of America, 106, 9939-9946.
89. Völkl W, Woodring J, Fischer M, Lorenz MW, Hoffmann KH (1999) Ant-aphid mutualisms: the impact of honeydew production and honeydew sugar composition on ant preferences. Oecologia, 118, 483-491.
90. Walsh PS, Metzger DA, Higuchi R (1991) Chelex-100 as a medium for simple extraction of DNA for PCR-based typing from forensic material. BioTechniques, 10, 506-513.
91. Way MJ, Banks CJ (1967) Intra-specific mechanisms in relation to the natural regulation of numbers of Aphis fabae Scop. Annals of Applied Biology, 59, 189-205.
92. Webster B, Bruce T, Dufour S et al. (2008) Identification of volatile compounds used in host location by the black bean aphid, Aphis fabae. Journal of Chemical Ecology, 34, 1153-1161.
93. Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution, 38, 1358-1370.
94. Weisser WW, Braendle C, Minoretti N (1999) Predator-induced morphological shift in the pea aphid. Proceedings of the Royal Society of London Series B-Biological Sciences, 266, 1175-1181.
95. Wilson ACC, Sunnucks P, Hales DF (1999) Microevolution, low clonal diversity and genetic affinities of parthenogenetic Sitobion aphids in New Zealand. Molecular Ecology, 8, 1655-1666.
96. Woodring J, Wiedemann R, Fischer MK, Hoffmann KH, Völkl W (2004) Honeydew amino acids in relation to sugars and their role in the establishment of ant-attendance hierarchy in eight species of aphids feeding on tansy (Tanacetum vulgare). Physiological Entomology, 29, 311-319.
97. Wu GM, Boivin G, Brodeur J, Giraldeau LA, Outreman Y (2010) Altruistic defence behaviours in aphids. BMC Evolutionary Biology, 10, 19.
98. Yao I (2010) Contrasting patterns of genetic structure and dispersal ability in ant-attended and non-attended Tuberculatus aphids. Biology Letters, 6, 282-286.
99. Yao I, Akimoto S (2009) Seasonal changes in the genetic structure of an aphid-ant mutualism as revealed using microsatellite analysis of the aphid Tuberculatus quercicola and the ant Formica yessensis. Journal of Insect Science, 9, 18.