Chemical Ecology and Sociality in Aphids: Opportunities and Directions

Review Article

Abstract

Aphids have long been recognized as good phytochemists. They are small sap-feeding plant herbivores with complex life cycles that can involve cyclical parthenogenesis and seasonal host plant alternation, and most are plant specialists. Aphids have distinctive traits for identifying and exploiting their host plants, including the expression of polyphenisms, a form of discrete phenotypic plasticity characteristic of insects, but taken to extreme in aphids. In a relatively small number of species, a social polyphenism occurs, involving sub-adult “soldiers” that are behaviorally or morphologically specialized to defend their nestmates from predators. Soldiers are sterile in many species, constituting a form of eusociality and reproductive division of labor that bears striking resemblances with other social insects. Despite a wealth of knowledge about the chemical ecology of non-social aphids and their phytophagous lifestyles, the molecular and chemoecological mechanisms involved in social polyphenisms in aphids are poorly understood. We provide a brief primer on aspects of aphid life cycles and chemical ecology for the non-specialists, and an overview of the social biology of aphids, with special attention to chemoecological perspectives. We discuss some of our own efforts to characterize how host plant chemistry may shape social traits in aphids. As good phytochemists, social aphids provide a bridge between the study of insect social evolution sociality, and the chemical ecology of plant-insect interactions. Aphids provide many promising opportunities for the study of sociality in insects, and to understand both the convergent and novel traits that characterize complex sociality on plants.

Keywords

Aphids Sociality Chemical ecology Polyphenisms Fatty acids 

Notes

Acknowledgments

We are grateful for support from NSF IOS- 1147033 and students and colleagues who have contributed to this work.

References

  1. Abbot P (2015) The physiology and genomics of social transitions in aphids. In: Zayed A, Kent CF (eds) Genomics, physiology and behaviour of social insects, vol 48. Adv Insect Physiol. Elsevier, New York, pp 163–188CrossRefGoogle Scholar
  2. Abbot P, Chapman TC (2017) Sociality in aphids and thrips. In: Rubenstein D, Abbot P (eds) Comparative social evolution. Cambridge University Press, Cambridge, pp 154–187CrossRefGoogle Scholar
  3. Abbot P, Chhatre V (2007) Kin structure provides no explanation for intruders in social aphids. Mol Ecol 16:3659–3670PubMedCrossRefGoogle Scholar
  4. Abbot P, Withgott JH, Moran NA (2001) Genetic conflict and conditional altruism in social aphid colonies. Proc Natl Acad Sci U S A 98:12068–12071PubMedPubMedCentralCrossRefGoogle Scholar
  5. Akçay E, Linksvayer TA, Van Cleve J (2015) Bridging social evolution theory and emerging empirical approaches to social behavior. Curr Opin Behav Sci 6:1–6CrossRefGoogle Scholar
  6. Akimoto S (1992) Shift in life-history strategy from reproduction to defense with colony age in the galling aphid Hemipodaphis persimilis producing defensive first-instar larvae. Res Popul Ecol 34:359–372CrossRefGoogle Scholar
  7. Akimoto S, Ozaki K, Matsumoto Y (1996) Production of first-instar defenders by the hormaphidid gall-forming aphid Hamamelistes cristafoliae living anholocyclically on Betula maximowicziana. Jap J Entomol 64:879–888Google Scholar
  8. Alfaress S, Hijaz F, Killiny N (2015) Chemical composition of cornicle secretion of the brown citrus aphid Toxoptera citricida. Physiol Entomol 41:38–47CrossRefGoogle Scholar
  9. Aoki S (1976) Occurrence of dimorphism in the first instar larva of Colophina clematis (Homoptera, Aphidoidea). Kontyû 44:130–137Google Scholar
  10. Aoki S, Kurosu U (2010) A review of the biology of Cerataphidini (Hemiptera, Aphididae, Hormaphidinae), focusing mainly on their life cycles, gall formation, and soldiers. Psyche 2010:1–34CrossRefGoogle Scholar
  11. Aoki S, Makino S (1982) Gall usurpation and lethal fighting among fundatrices of the aphid Epipemphigus niisimae (Homoptera, Pemphigidae). Kontyû 50:365–376Google Scholar
  12. Aoki S, Kurosu U, Stern DL (1991) Aphid soldiers discriminate between soldiers and non-soldiers, rather than between kin and non-kin, in Ceratoglyphina bambusae. Anim Behav 42:865–866CrossRefGoogle Scholar
  13. Arakaki N (1989) Alarm pheromone eliciting attack and escape responses in the sugar-cane woolly aphid, Ceratovacuna lanigera (Homoptera, Pemphigidae). J Ethol 7:83–90CrossRefGoogle Scholar
  14. Atkins CA, Smith PMC, Rodriguez-Medina C (2011) Macromolecules in phloem exudates—a review. Protoplasma 248:165–172PubMedCrossRefGoogle Scholar
  15. Behmer ST (2008) Nutrition in insects. In: Capinera JL (ed) Encyclopedia of entomology. Springer, DordrechtGoogle Scholar
  16. Benning UF, Tamot B, Guelette BS, Hoffmann-Benning S (2012) New aspects of phloem-mediated long-distance lipid signaling in plants. Front Plant Sci 3:53PubMedPubMedCentralCrossRefGoogle Scholar
  17. Billen J, Sobotník J (2015) Insect exocrine glands. Arthropod Struct Dev 44:399–400PubMedCrossRefGoogle Scholar
  18. Birnbaum SSL, Abbot P (2018) Insect adaptations towards plant toxins in milkweed-herbivore systems. Entomol Exp Appl, in pressGoogle Scholar
  19. Birnbaum SSL, Rinker D, Gerardo N, Abbot P (2017) Transcriptional profile and differential fitness across a cardenolide gradient in a specialist milkweed insect. Mol Ecol 26:6742–6741PubMedCrossRefGoogle Scholar
  20. Blackman RL, Eastop VF (1994) Aphids on the world's trees: an identification and information guide. University Press, LondonGoogle Scholar
  21. Bourke AFD (2011) Principles of social evolution. Oxford University Press, OxfordCrossRefGoogle Scholar
  22. Braendle C, Davis GK, Brisson JA, Stern DL (2006) Wing dimorphism in aphids. Heredity 97:192–199PubMedCrossRefGoogle Scholar
  23. Brisson JA (2010) Aphid wing dimorphisms: linking environmental and genetic control of trait variation. Philos Trans R Soc Lond Ser B Biol Sci 365:605–616CrossRefGoogle Scholar
  24. Brisson JA, Davis GK (2016) The right tools for the job: regulating polyphenic morph development in insects. Curr Opin Insect Sci 13:1–6PubMedPubMedCentralCrossRefGoogle Scholar
  25. Brisson JA, Stern DL (2006) The pea aphid, Acyrthosiphon pisum: an emerging genomic model system for ecological, developmental and evolutionary studies. BioEssays 28:747–755PubMedCrossRefGoogle Scholar
  26. Bruce TJA, Wadhams LJ, Woodcock CM (2005) Insect host location: a volatile situation. Trends Plant Sci 10:269–274PubMedCrossRefGoogle Scholar
  27. Byers JA (2005) A cost of alarm pheromone production in cotton aphids, Aphis gossypii. Naturwissenschaften 92:69–72PubMedCrossRefGoogle Scholar
  28. Callow RK, Greenway AR, Griffiths DC (1973) Chemistry of secretion from cornicles of various species of aphids. J Insect Physiol 19:737–748CrossRefGoogle Scholar
  29. Camazine S, Deneubourg JL, Franks N, Sneyd J, Theraulaz G, Bonabeau E (2002) Self-organization in biological systems. Princeton University Press, PrincetonGoogle Scholar
  30. Cao HH, Liu HR, Zhang ZF, Liu TX (2016) The green peach aphid Myzus persicae perform better on pre-infested Chinese cabbage Brassica pekinensis by enhancing host plant nutritional quality. Sci Rep 6:21954PubMedPubMedCentralCrossRefGoogle Scholar
  31. Cooper LC, Desjonqueres C, Leather SR (2014) Cannibalism in the pea aphid, Acyrthosiphon pisum. Insect Sci 21:750–758PubMedCrossRefGoogle Scholar
  32. Crespi BJ (1994) Three conditions for the evolution of eusociality: are they sufficient? Insect Soc 41:395–400CrossRefGoogle Scholar
  33. Davis GK (2012) Cyclical parthenogenesis and viviparity in aphids as evolutionary novelties. J Exp Zool B Mol Dev Evol 318:448–459PubMedCrossRefGoogle Scholar
  34. De Vos M, Jander G (2009) Myzus persicae (green peach aphid) salivary components induce defence responses in Arabidopsis thaliana. Plant Cell Environ 32:1548–1560PubMedCrossRefGoogle Scholar
  35. Dixon AFG (1998) Aphid ecology. Springer, New YorkGoogle Scholar
  36. Döring TF (2014) How aphids find their host plants, and how they don't. Ann Appl Biol 165:3–26CrossRefGoogle Scholar
  37. Elzinga DA, Jander G (2013) The role of protein effectors in plant–aphid interactions. Curr Opin Plant Biol 16:451–456PubMedCrossRefGoogle Scholar
  38. Elzinga DA, De Vos M, Jander G (2014) Suppression of plant defenses by a Myzus persicae (green peach aphid) salivary effector protein. Mol Plant-Microbe Interact 27:747–756PubMedPubMedCentralCrossRefGoogle Scholar
  39. Febvay GR, Febvay G, Pageaux JF, Pageaux JFO, Bonnot G, Bonnot G (1992) Lipid composition of the pea aphid, Acyrthosiphon pisum (Harris) (Homoptera: Aphididae), reared on host plant and on artificial media. Arch Insect Biochem Physiol 21:103–118CrossRefGoogle Scholar
  40. Fewell J, Abbot P (2017) Insect sociality. In: Córdoba-Aguilar A, González-Tokman D, González-Santoyo I (eds) Insect behavior: from mechanisms to ecological and evolutionary consequences. Oxford University Press, OxfordGoogle Scholar
  41. Fry BG, Roelants K, Champagne DE, Scheib H, Tyndall JDA, King GF et al (2009) The toxicogenomic multiverse: convergent recruitment of proteins into animal venoms. Annu Rev Genomics Hum Genet 10:483–511PubMedCrossRefGoogle Scholar
  42. Gäde G (2009) Peptides of the adipokinetic hormone/red pigment-concentrating hormone family: a new take on biodiversity. Ann N Y Acad Sci 1163:125–136PubMedCrossRefGoogle Scholar
  43. Gao N, Hardie J (1997) Melatonin and the pea aphid, Acyrthosiphon pisum. J Insect Physiol 43:615–620PubMedCrossRefGoogle Scholar
  44. Gospocic J, Shields EJ, Glastad KM, Lin Y, Penick CA, Yan H et al (2017) The neuropeptide corazonin controls social behavior and caste identity in ants. Cell 170:748–752PubMedCrossRefGoogle Scholar
  45. Greenway AR, Griffiths DC (1973) A comparison of triglycerides from aphids and their cornicle secretions. J Insect Physiol 19:1649–1655CrossRefGoogle Scholar
  46. Guelette BS, Benning U, Hoffmann-Benning S (2012) Identification of lipids and lipid-binding proteins in phloem exudates from Arabidopsis thaliana. J Exp Bot 63:3603–3616PubMedPubMedCentralCrossRefGoogle Scholar
  47. Guillemaud T, Mieuzet L, Simon JC (2003) Spatial and temporal genetic variability in French populations of the peach-potato aphid, Myzus persicae. Heredity 91:143–152PubMedCrossRefGoogle Scholar
  48. Hattori M, Kishida O, Itino T (2013) Soldiers with large weapons in predator-abundant midsummer: phenotypic plasticity in a eusocial aphid. Evol Ecol 27:847–862CrossRefGoogle Scholar
  49. Hölldobler B, Wilson EO (2008) The superorganism: the beauty, elegance, and strangeness of insect societies. W.W. Norton & Co, New YorkGoogle Scholar
  50. Ijichi N, Shibao H, Miura T, Matsumoto T (2004) Soldier differentiation during embryogenesis of a social aphid, Pseudoregma bambucicola. Entomol Sci 7:143–155CrossRefGoogle Scholar
  51. Ijichi N, Shibao H, Miura T, Matsumoto T, Fukatsu T (2005) Analysis of natural colonies of a social aphid Colophina arma: population dynamics, reproductive schedule, and survey for ecological correlates with soldier production. Appl Entomol Zool 40:239–245CrossRefGoogle Scholar
  52. Ishikawa A, Miura T (2013) Transduction of high-density signals across generations in aphid wing polyphenism. Physiol Entomol 38:150–156CrossRefGoogle Scholar
  53. Ishikawa A, Ogawa K, Gotoh H, Walsh TK, Tagu D, Brisson JA et al (2011) Juvenile hormone titer and related gene expression during the change of reproductive modes in the pea aphid. Insect Mol Biol 21:49–60PubMedCrossRefGoogle Scholar
  54. Jedličková V, Jedlička P, Lee HJ (2015) Characterization and expression analysis of adipokinetic hormone and its receptor in eusocial aphid Pseudoregma bambucicola. Gen Comp Endocrinol 223:38–46PubMedCrossRefGoogle Scholar
  55. Johnson BR, Linksvayer TA (2010) Deconstructing the superorganism: social physiology, groundplans, and sociogenomics. Q Rev Biol 85:57–79PubMedCrossRefGoogle Scholar
  56. Kachroo A, Kachroo P (2009) Fatty acid–derived signals in plant defense. Annu Rev Phytopathol 47:153–176PubMedCrossRefGoogle Scholar
  57. Kim JH, Jander G (2007) Myzus persicae (green peach aphid) feeding on Arabidopsis induces the formation of a deterrent indole glucosinolate. Plant J 49:1008–1019PubMedCrossRefGoogle Scholar
  58. Kini RM (2003) Excitement ahead: structure, function and mechanism of snake venom phospholipase A2 enzymes. Toxicon 42:827–840PubMedCrossRefGoogle Scholar
  59. Kocher SD, Grozinger CM (2011) Cooperation, conflict, and the evolution of queen pheromones. J Chem Ecol 37:1263–1275PubMedCrossRefGoogle Scholar
  60. Korb J, Heinze J (2008) The ecology of social life: a synthesis. In: Korb J, Heinze J (eds) Ecology of social evolution. Springer, HeidelbergCrossRefGoogle Scholar
  61. Korb J, Heinze J (2016) Major hurdles for the evolution of sociality. Annu Rev Entomol 61:297–316PubMedCrossRefGoogle Scholar
  62. Korb J, Thorne BL (2017) Sociality in termites. In: Rubenstein D, Abbot P (eds) Comparative social evolution. Cambridge University Press, CambridgeGoogle Scholar
  63. Kutsukake M, Shibao H, Nikoh N, Morioka M, Tamura T, Hoshino T et al (2004) Venomous protease of aphid soldier for colony defense. Proc Natl Acad Sci U S A 101:11338–11343PubMedPubMedCentralCrossRefGoogle Scholar
  64. Kutsukake M, Nikoh N, Shibao H, Rispe C, Simon J-C, Fukatsu T (2008) Evolution of soldier-specific venomous protease in social aphids. Mol Biol Evol 25:2627–2641PubMedCrossRefGoogle Scholar
  65. Kutsukake M, Shibao H, Uematsu K, Fukatsu T (2009) Scab formation and wound healing of plant tissue by soldier aphid. Proc R Soc Lond B Biol Sci 276:1555–1563CrossRefGoogle Scholar
  66. Kutsukake M, Meng XY, Katayama N, Nikoh N, Shibao H, Fukatsu T (2012) An insect-induced novel plant phenotype for sustaining social life in a closed system. Nat Commun 3:1187PubMedPubMedCentralCrossRefGoogle Scholar
  67. Lawson SP, Legan AW, Graham C, Abbot P (2014) Comparative phenotyping across a social transition in aphids. Anim Behav 96:117–125CrossRefGoogle Scholar
  68. Lawson SP, Sigle LT, Lind AL, Legan AW, Mezzanotte JN, Honegger HW et al (2017) An alternative pathway to eusociality: exploring the molecular and functional basis of fortress defense. Evolution 71:1986–1998PubMedCrossRefGoogle Scholar
  69. Leonhardt SD, Menzel F, Nehring V, Schmitt T (2016) Ecology and evolution of communication in social insects. Cell 164:1277–1287PubMedCrossRefGoogle Scholar
  70. Madey E, Nowack L, Thompson J (2002) Isolation and characterization of lipid in phloem sap of canola. Planta 214:625–634PubMedCrossRefGoogle Scholar
  71. Miller DG III (1998) Consequences of communal gall occupation and a test for kin discrimination in the aphid Tamalia coweni (Cockerell) (Homoptera: Aphididae). Behav Ecol Sociobiol 43:95–103CrossRefGoogle Scholar
  72. Mondor EB, Roitberg BD (2004) Inclusive fitness benefits of scent-marking predators. Proc R Soc Lond B Biol Sci 271:341–343CrossRefGoogle Scholar
  73. Mondor EB, Rosenheim JA, Addicott JF (2004) Predator-induced transgenerational phenotypic plasticity in the cotton aphid. Oecologia 142:104–108PubMedCrossRefGoogle Scholar
  74. Moran N (1992) The evolution of aphid life cycles. Annu Rev Entomol 37:321–348CrossRefGoogle Scholar
  75. Moran NA, McCutcheon JP, Nakabachi A (2008) Genomics and evolution of heritable bacterial symbionts. Annu Rev Genet 42:165–190PubMedCrossRefGoogle Scholar
  76. Müller CB, Williams IS, Hardie J (2001) The role of nutrition, crowding and interspecific interactions in the development of winged aphids. Ecol Entomol 26:330–340CrossRefGoogle Scholar
  77. Nijhout HF (2003) Development and evolution of adaptive polyphenisms. Evol Dev 5:9–18PubMedCrossRefGoogle Scholar
  78. Nishida R (2014) Chemical ecology of insect-plant interactions: ecological significance of plant secondary metabolites. Biosci Biotechnol Biochem 78:1–13PubMedCrossRefGoogle Scholar
  79. Nyman T, Julkunen-Tiitto R (2000) Manipulation of the phenolic chemistry of willows by gall-inducing sawflies. Proc Natl Acad Sci U S A 97:13184–13187PubMedPubMedCentralCrossRefGoogle Scholar
  80. Peccoud J, Simon JC, von Dohlen C, Coeur d'acier A, Plantegenest M, Vanlerberghe-Masutti F, Jousselin E (2010) Evolutionary history of aphid-plant associations and their role in aphid diversification. C R Biol 333:474–487PubMedCrossRefGoogle Scholar
  81. Philippe RN, Bohlmann J (2007) Poplar defense against insect herbivores. Can J Bot 85:1111–1126CrossRefGoogle Scholar
  82. Pike N, Braendle C, Foster WA (2004) Seasonal extension of the soldier instar as a route to increased defence investment in the social aphid Pemphigus spyrothecae. Ecol Entomol 29:89–95CrossRefGoogle Scholar
  83. Pike N, Whitfield JA, Foster WA (2007) Ecological correlates of sociality in Pemphigus aphids, with a partial phylogeny of the genus. BMC Evol Biol 7:185PubMedPubMedCentralCrossRefGoogle Scholar
  84. Podjasek JO, Bosnjak LM, Brooker DJ, Mondor EB (2011) Alarm pheromone induces a transgenerational wing polyphenism in the pea aphid, Acyrthosiphon pisum. Can J Zool 83:1138–1141CrossRefGoogle Scholar
  85. Powell G, Tosh CR, Hardie J (2006) Host plant selection by aphids: Behavioral, evolutionary, and applied perspectives. Annu Rev Entomol 51:309–330PubMedCrossRefGoogle Scholar
  86. Prestwich GD (1984) Defense mechanisms of termites. Annu Rev Entomol 29:201–232CrossRefGoogle Scholar
  87. Purandare SR, Bickel RD, Jaquiéry J, Rispe C, Brisson JA (2014) Accelerated evolution of morph-biased genes in pea aphids. Mol Biol Evol 31:2073–2083PubMedPubMedCentralCrossRefGoogle Scholar
  88. Queller DC, Strassmann JE (1998) Kin selection and social insects. Bioscience 48:165–175CrossRefGoogle Scholar
  89. Ramsewak RS, Nair MG, Murugesan S, Mattson WJ, Zasada J (2001) Insecticidal fatty acids and triglycerides from Dirca palustris. J Agric Food Chem 49:5852–5856PubMedCrossRefGoogle Scholar
  90. Rubenstein DR, Abbot P (2017) Comparative social evolution. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  91. Salazar A, Furstenau B, Quero C, Perez-Hidalgo N, Carazo P, Font E, Martinez-Torres D (2015) Aggressive mimicry coexists with mutualism in an aphid. Proc Natl Acad Sci U S A 112:1101–1106PubMedPubMedCentralCrossRefGoogle Scholar
  92. Schwartzberg EG, Kunert G, Westerlund SA, Hoffmann KH, Weisser WW (2008) Juvenile hormone titres and winged offspring production do not correlate in the pea aphid, Acyrthosiphon pisum. J Insect Physiol 54:1332–1336PubMedCrossRefGoogle Scholar
  93. Shibao H (1999) Reproductive schedule and factors affecting soldier production in the eusocial bamboo aphid Pseudoregma bambucicola (Homoptera, Aphididae). Insect Soc 46:378–386CrossRefGoogle Scholar
  94. Shibao H, Kutsukake M, Lee JM, Fukatsu T (2002) Maintenance of soldier-producing aphids on an artificial diet. J Insect Physiol 48:495–505PubMedCrossRefGoogle Scholar
  95. Shibao H, Kutsukake M, Fukatsu T (2004a) Density triggers soldier production in a social aphid. Proc R Soc Lond B Biol Sci 271:S71–S74CrossRefGoogle Scholar
  96. Shibao H, Kutsukake M, Fukatsu T (2004b) The proximate cue of density-dependent soldier production in a social aphid. J Insect Physiol 50:143–147PubMedCrossRefGoogle Scholar
  97. Shibao H, Kutsukake M, Matsuyama S, Fukatsu T, Shimada M (2010) Mechanisms regulating caste differentiation in an aphid social system. Commun Integr Biol 3:1–5PubMedPubMedCentralCrossRefGoogle Scholar
  98. Shibao H, Takanashi T, Kutsukake M, Matsuyama S, Shimada M, Fukatsu T (2016) Social aphids use their antennae to perceive density cue for soldier production. Entomol Sci 19:147–151CrossRefGoogle Scholar
  99. Shingleton AW, Foster WA (2000) Ant tending influences soldier production in a social aphid. Proc Biol Sci 267:1863–1868PubMedPubMedCentralCrossRefGoogle Scholar
  100. Simon JC, Stoeckel S, Tagu D (2010) Evolutionary and functional insights into reproductive strategies of aphids. C R Biol 333:488–496PubMedCrossRefGoogle Scholar
  101. Simon JC, d'Alencon E, Guy E, Jacquin-Joly E, Jaquiery J, Nouhaud P et al (2015) Genomics of adaptation to host-plants in herbivorous insects. Brief Funct Genomics 14:413–423PubMedCrossRefGoogle Scholar
  102. Simpson SJ, Sword GA, Lo N (2011) Polyphenism in insects. Curr Biol 21:738–749CrossRefGoogle Scholar
  103. Sivakumar R, Jebanesan A, Govindarajan M, Rajasekar P (2011) Larvicidal and repellent activity of tetradecanoic acid against Aedes aegypti (Linn.) and Culex quinquefasciatus (Say.) (Diptera:Culicidae). Asian Pac J Trop Med 4:706–710PubMedCrossRefGoogle Scholar
  104. Smith CM, Liu X, Wang LJ, Liu X, Chen MS, Starkey S et al (2010) Aphid feeding activates expression of a transcriptome of oxylipin-based defense signals in wheat involved in resistance to herbivory. J Chem Ecol 36:260–276PubMedCrossRefGoogle Scholar
  105. Srinivasan DG, Brisson JA (2012) Aphids: A model for polyphenism and epigenetics. Genet Res Int 2012:1–12CrossRefGoogle Scholar
  106. Stern DL (1994) A phylogenetic analysis of soldier evolution in the aphid family Hormaphididae. Proc R Soc Lond B Biol Sci 256:203–209CrossRefGoogle Scholar
  107. Stern DL (1998) Phylogeny of the tribe Cerataphidini (Homoptera) and the evolution of the horned soldier aphids. Evolution 52:155PubMedCrossRefGoogle Scholar
  108. Stern DL, Foster WA (1996) The evolution of soldiers in aphids. Biol Rev Camb Philos Soc 71:27–79PubMedCrossRefGoogle Scholar
  109. Strong IE (1963) Studies on lipids in some homopterous insects. Hilgardia 34:43–61CrossRefGoogle Scholar
  110. Tagu D, Sabater-Muñoz B, Simon JC (2005) Deciphering reproductive polyphenism in aphids. Invertebr Reprod Dev 48:71–80CrossRefGoogle Scholar
  111. Tagu D, Dugravot S, Outreman Y, Rispe C, Simon JC, Colella S (2010) The anatomy of an aphid genome: from sequence to biology. C R Biol 333:464–473PubMedCrossRefGoogle Scholar
  112. Tooker JF, De Moraes CM (2009) A gall-inducing caterpillar species increases essential fatty acid content of its host plant without concomitant increases in phytohormone levels. Mol Plant-Microbe Interact 22:551–559PubMedCrossRefGoogle Scholar
  113. Tooker JF, Helms AM (2014) Phytohormone dynamics associated with gall insects, and their potential role in the evolution of the gall-inducing habit. J Chem Ecol 40:742–753PubMedCrossRefGoogle Scholar
  114. Tooker JF, Rohr JR, Abrahamson WG, De Moraes CM (2008) Gall insects can avoid and alter indirect plant defenses. New Phytol 178:657–671Google Scholar
  115. Toth AL, Rehan SM (2017) Molecular evolution of insect sociality: an eco-evo-devo perspective. Annu Rev Entomol 62:419–442PubMedCrossRefGoogle Scholar
  116. Trible W, Olivos-Cisneros L, McKenzie SK, Saragosti J, Chang NC, Matthews BJ et al (2017) orco mutagenesis causes loss of antennal lobe glomeruli and impaired social behavior in ants. Cell 170:727–732PubMedCrossRefGoogle Scholar
  117. Uematsu K, Kutsukake M, Fukatsu T, Shimada M, Shibao H (2010) Altruistic colony defense by menopausal female insects. Curr Biol 20:1182–1186PubMedCrossRefGoogle Scholar
  118. Vandermoten S, Mescher MC, Francis F, Haubruge E, Verheggen FJ (2012) Aphid alarm pheromone: An overview of current knowledge on biosynthesis and functions. Insect Biochem Mol Biol 42:155–163PubMedCrossRefGoogle Scholar
  119. Vantaux A, Billen J, Wenseleers T (2011) Levels of clonal mixing in the black bean aphid Aphis fabae, a facultative ant mutualist. Mol Ecol 20:4772–4785PubMedCrossRefGoogle Scholar
  120. Vellichirammal NN, Madayiputhiya N, Brisson JA (2016) The genome wide transcriptional response underlying the pea aphid wing polyphenism. Mol Ecol 25:4146–4160PubMedPubMedCentralCrossRefGoogle Scholar
  121. Vellichirammal NN, Gupta P, Hall TA, Brisson JA (2017) Ecdysone signaling underlies the pea aphid transgenerational wing polyphenism. Proc Natl Acad Sci U S A 114:1419–1423PubMedPubMedCentralCrossRefGoogle Scholar
  122. Verheggen FJ, Haubruge E, De Moraes CM, Mescher MC (2009) Social environment influences aphid production of alarm pheromone. Behav Ecol 20:283–288CrossRefGoogle Scholar
  123. Wang CC, Tsaur SC, Kurosu U, Aoki S, Lee HJ (2008) Social parasitism and behavioral interactions between two gall-forming social aphids. Insect Soc 55:147–152CrossRefGoogle Scholar
  124. Ward A, Webster M (2016) Sociality: the behaviour of group-living animals. Springer, SwitzerlandCrossRefGoogle Scholar
  125. Ward SA, Leather SR, Pickup J, Harrington R (1998) Mortality during dispersal and the cost of host-specificity in parasites: how many aphids find hosts? J Anim Ecol 67:763–773CrossRefGoogle Scholar
  126. Way MJ (1963) Mutualism between ants and honeydew-producing Homoptera. Annu Rev Entomol 8:307–344CrossRefGoogle Scholar
  127. Webster B (2012) The role of olfaction in aphid host location. Physiol Entomol 37:10–18CrossRefGoogle Scholar
  128. Webster B, Bruce T, Pickett J, Hardie J (2010) Volatiles functioning as host cues in a blend become nonhost cues when presented alone to the black bean aphid. Anim Behav 79:451–457CrossRefGoogle Scholar
  129. Whitham TG (1986) Cost of benefits of territoriality: behavioral and reproductive release by competing aphids. Ecology 67:139CrossRefGoogle Scholar
  130. Wilch MH (1999). Predation and prey response in the galls of Pemphigus nr. populi-ramulorum. Masters thesis, University of ArizonaGoogle Scholar
  131. Will T, Furch ACU, Zimmermann MR (2013) How phloem-feeding insects face the challenge of phloem-located defenses. Front Plant Sci 4:336PubMedPubMedCentralCrossRefGoogle Scholar
  132. Withgott JH, Abbot DK, Moran NA, Moran NA (1997) Maternal death relaxes developmental inhibition in nymphal aphid defenders. Proc R Soc B Biol Sci 264:1197–1202CrossRefGoogle Scholar
  133. Wool D (2004) Galling aphids: specialization, biological complexity, and variation. Annu Rev Entomol 49:175–192PubMedCrossRefGoogle Scholar
  134. Yan H, Opachaloemphan C, Mancini G, Yang H, Gallitto M, Mlejnek J et al (2017) An engineered orco mutation produces aberrant social behavior and defective neural development in ants. Cell 170:736–742PubMedCrossRefGoogle Scholar
  135. Zhou XF, Slone JD, Rokas A, Berger SL, Liebig J, Ray A et al (2012) Phylogenetic and transcriptomic analysis of chemosensory receptors in a pair of divergent ant species reveals sex-specific signatures of odor coding. PLoS Genet 8:e1002930PubMedPubMedCentralCrossRefGoogle Scholar
  136. Züst T, Agrawal AA (2015) Population growth and sequestration of plant toxins along a gradient of specialization in four aphid species on the common milkweed Asclepias syriaca. Funct Ecol 30:547–556CrossRefGoogle Scholar

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Authors and Affiliations

  1. 1.Department of Biological SciencesVanderbilt UniversityNashvilleUSA
  2. 2.Department of EntomologyThe Pennsylvania State UniversityUniversity ParkUSA
  3. 3.Department of Biological SciencesUniversity of New HampshireDurhamUSA

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