Skip to main content
Log in

Chemical Ecology and Sociality in Aphids: Opportunities and Directions

  • Review Article
  • Published:
Journal of Chemical Ecology Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • 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 163–188

    Chapter  Google Scholar 

  • Abbot P, Chapman TC (2017) Sociality in aphids and thrips. In: Rubenstein D, Abbot P (eds) Comparative social evolution. Cambridge University Press, Cambridge, pp 154–187

    Chapter  Google Scholar 

  • Abbot P, Chhatre V (2007) Kin structure provides no explanation for intruders in social aphids. Mol Ecol 16:3659–3670

    Article  PubMed  CAS  Google Scholar 

  • Abbot P, Withgott JH, Moran NA (2001) Genetic conflict and conditional altruism in social aphid colonies. Proc Natl Acad Sci U S A 98:12068–12071

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Akçay E, Linksvayer TA, Van Cleve J (2015) Bridging social evolution theory and emerging empirical approaches to social behavior. Curr Opin Behav Sci 6:1–6

    Article  Google Scholar 

  • 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 34:359–372

    Article  Google Scholar 

  • 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 64:879–888

    Google Scholar 

  • Alfaress S, Hijaz F, Killiny N (2015) Chemical composition of cornicle secretion of the brown citrus aphid Toxoptera citricida. Physiol Entomol 41:38–47

    Article  CAS  Google Scholar 

  • Aoki S (1976) Occurrence of dimorphism in the first instar larva of Colophina clematis (Homoptera, Aphidoidea). Kontyû 44:130–137

    Google Scholar 

  • 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 2010:1–34

    Article  Google Scholar 

  • Aoki S, Makino S (1982) Gall usurpation and lethal fighting among fundatrices of the aphid Epipemphigus niisimae (Homoptera, Pemphigidae). Kontyû 50:365–376

    Google Scholar 

  • 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 42:865–866

    Article  Google Scholar 

  • Arakaki N (1989) Alarm pheromone eliciting attack and escape responses in the sugar-cane woolly aphid, Ceratovacuna lanigera (Homoptera, Pemphigidae). J Ethol 7:83–90

    Article  Google Scholar 

  • Atkins CA, Smith PMC, Rodriguez-Medina C (2011) Macromolecules in phloem exudates—a review. Protoplasma 248:165–172

    Article  PubMed  CAS  Google Scholar 

  • Behmer ST (2008) Nutrition in insects. In: Capinera JL (ed) Encyclopedia of entomology. Springer, Dordrecht

    Google Scholar 

  • Benning UF, Tamot B, Guelette BS, Hoffmann-Benning S (2012) New aspects of phloem-mediated long-distance lipid signaling in plants. Front Plant Sci 3:53

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Billen J, Sobotník J (2015) Insect exocrine glands. Arthropod Struct Dev 44:399–400

    Article  PubMed  Google Scholar 

  • Birnbaum SSL, Abbot P (2018) Insect adaptations towards plant toxins in milkweed-herbivore systems. Entomol Exp Appl, in press

  • 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 26:6742–6741

    Article  PubMed  CAS  Google Scholar 

  • Blackman RL, Eastop VF (1994) Aphids on the world's trees: an identification and information guide. University Press, London

    Google Scholar 

  • Bourke AFD (2011) Principles of social evolution. Oxford University Press, Oxford

    Book  Google Scholar 

  • Braendle C, Davis GK, Brisson JA, Stern DL (2006) Wing dimorphism in aphids. Heredity 97:192–199

    Article  PubMed  CAS  Google Scholar 

  • Brisson JA (2010) Aphid wing dimorphisms: linking environmental and genetic control of trait variation. Philos Trans R Soc Lond Ser B Biol Sci 365:605–616

    Article  Google Scholar 

  • Brisson JA, Davis GK (2016) The right tools for the job: regulating polyphenic morph development in insects. Curr Opin Insect Sci 13:1–6

    Article  PubMed  PubMed Central  Google Scholar 

  • Brisson JA, Stern DL (2006) The pea aphid, Acyrthosiphon pisum: an emerging genomic model system for ecological, developmental and evolutionary studies. BioEssays 28:747–755

    Article  PubMed  CAS  Google Scholar 

  • Bruce TJA, Wadhams LJ, Woodcock CM (2005) Insect host location: a volatile situation. Trends Plant Sci 10:269–274

    Article  PubMed  CAS  Google Scholar 

  • Byers JA (2005) A cost of alarm pheromone production in cotton aphids, Aphis gossypii. Naturwissenschaften 92:69–72

    Article  PubMed  CAS  Google Scholar 

  • Callow RK, Greenway AR, Griffiths DC (1973) Chemistry of secretion from cornicles of various species of aphids. J Insect Physiol 19:737–748

    Article  CAS  Google Scholar 

  • Camazine S, Deneubourg JL, Franks N, Sneyd J, Theraulaz G, Bonabeau E (2002) Self-organization in biological systems. Princeton University Press, Princeton

    Google Scholar 

  • 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 6:21954

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Cooper LC, Desjonqueres C, Leather SR (2014) Cannibalism in the pea aphid, Acyrthosiphon pisum. Insect Sci 21:750–758

    Article  PubMed  Google Scholar 

  • Crespi BJ (1994) Three conditions for the evolution of eusociality: are they sufficient? Insect Soc 41:395–400

    Article  Google Scholar 

  • Davis GK (2012) Cyclical parthenogenesis and viviparity in aphids as evolutionary novelties. J Exp Zool B Mol Dev Evol 318:448–459

    Article  PubMed  Google Scholar 

  • De Vos M, Jander G (2009) Myzus persicae (green peach aphid) salivary components induce defence responses in Arabidopsis thaliana. Plant Cell Environ 32:1548–1560

    Article  PubMed  CAS  Google Scholar 

  • Dixon AFG (1998) Aphid ecology. Springer, New York

    Google Scholar 

  • Döring TF (2014) How aphids find their host plants, and how they don't. Ann Appl Biol 165:3–26

    Article  Google Scholar 

  • Elzinga DA, Jander G (2013) The role of protein effectors in plant–aphid interactions. Curr Opin Plant Biol 16:451–456

    Article  PubMed  CAS  Google Scholar 

  • 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 27:747–756

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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 21:103–118

    Article  CAS  Google Scholar 

  • 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, Oxford

    Google Scholar 

  • 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 10:483–511

    Article  PubMed  CAS  Google Scholar 

  • Gäde G (2009) Peptides of the adipokinetic hormone/red pigment-concentrating hormone family: a new take on biodiversity. Ann N Y Acad Sci 1163:125–136

    Article  PubMed  CAS  Google Scholar 

  • Gao N, Hardie J (1997) Melatonin and the pea aphid, Acyrthosiphon pisum. J Insect Physiol 43:615–620

    Article  PubMed  CAS  Google Scholar 

  • 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 170:748–752

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Greenway AR, Griffiths DC (1973) A comparison of triglycerides from aphids and their cornicle secretions. J Insect Physiol 19:1649–1655

    Article  CAS  Google Scholar 

  • Guelette BS, Benning U, Hoffmann-Benning S (2012) Identification of lipids and lipid-binding proteins in phloem exudates from Arabidopsis thaliana. J Exp Bot 63:3603–3616

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Hattori M, Kishida O, Itino T (2013) Soldiers with large weapons in predator-abundant midsummer: phenotypic plasticity in a eusocial aphid. Evol Ecol 27:847–862

    Article  Google Scholar 

  • Hölldobler B, Wilson EO (2008) The superorganism: the beauty, elegance, and strangeness of insect societies. W.W. Norton & Co, New York

    Google Scholar 

  • Ijichi N, Shibao H, Miura T, Matsumoto T (2004) Soldier differentiation during embryogenesis of a social aphid, Pseudoregma bambucicola. Entomol Sci 7:143–155

    Article  Google Scholar 

  • 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 40:239–245

    Article  Google Scholar 

  • Ishikawa A, Miura T (2013) Transduction of high-density signals across generations in aphid wing polyphenism. Physiol Entomol 38:150–156

    Article  Google Scholar 

  • 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 21:49–60

    Article  PubMed  CAS  Google Scholar 

  • 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 223:38–46

    Article  PubMed  CAS  Google Scholar 

  • Johnson BR, Linksvayer TA (2010) Deconstructing the superorganism: social physiology, groundplans, and sociogenomics. Q Rev Biol 85:57–79

    Article  PubMed  Google Scholar 

  • Kachroo A, Kachroo P (2009) Fatty acid–derived signals in plant defense. Annu Rev Phytopathol 47:153–176

    Article  PubMed  CAS  Google Scholar 

  • Kim JH, Jander G (2007) Myzus persicae (green peach aphid) feeding on Arabidopsis induces the formation of a deterrent indole glucosinolate. Plant J 49:1008–1019

    Article  PubMed  CAS  Google Scholar 

  • Kini RM (2003) Excitement ahead: structure, function and mechanism of snake venom phospholipase A2 enzymes. Toxicon 42:827–840

    Article  PubMed  CAS  Google Scholar 

  • Kocher SD, Grozinger CM (2011) Cooperation, conflict, and the evolution of queen pheromones. J Chem Ecol 37:1263–1275

    Article  PubMed  CAS  Google Scholar 

  • Korb J, Heinze J (2008) The ecology of social life: a synthesis. In: Korb J, Heinze J (eds) Ecology of social evolution. Springer, Heidelberg

    Chapter  Google Scholar 

  • Korb J, Heinze J (2016) Major hurdles for the evolution of sociality. Annu Rev Entomol 61:297–316

    Article  PubMed  CAS  Google Scholar 

  • Korb J, Thorne BL (2017) Sociality in termites. In: Rubenstein D, Abbot P (eds) Comparative social evolution. Cambridge University Press, Cambridge

    Google Scholar 

  • 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 101:11338–11343

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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 25:2627–2641

    Article  PubMed  CAS  Google Scholar 

  • 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 276:1555–1563

    Article  Google Scholar 

  • 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 3:1187

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lawson SP, Legan AW, Graham C, Abbot P (2014) Comparative phenotyping across a social transition in aphids. Anim Behav 96:117–125

    Article  Google Scholar 

  • 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 71:1986–1998

    Article  PubMed  Google Scholar 

  • Leonhardt SD, Menzel F, Nehring V, Schmitt T (2016) Ecology and evolution of communication in social insects. Cell 164:1277–1287

    Article  PubMed  CAS  Google Scholar 

  • Madey E, Nowack L, Thompson J (2002) Isolation and characterization of lipid in phloem sap of canola. Planta 214:625–634

    Article  PubMed  CAS  Google Scholar 

  • 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 43:95–103

    Article  Google Scholar 

  • Mondor EB, Roitberg BD (2004) Inclusive fitness benefits of scent-marking predators. Proc R Soc Lond B Biol Sci 271:341–343

    Article  Google Scholar 

  • Mondor EB, Rosenheim JA, Addicott JF (2004) Predator-induced transgenerational phenotypic plasticity in the cotton aphid. Oecologia 142:104–108

    Article  PubMed  Google Scholar 

  • Moran N (1992) The evolution of aphid life cycles. Annu Rev Entomol 37:321–348

    Article  Google Scholar 

  • Moran NA, McCutcheon JP, Nakabachi A (2008) Genomics and evolution of heritable bacterial symbionts. Annu Rev Genet 42:165–190

    Article  PubMed  CAS  Google Scholar 

  • Müller CB, Williams IS, Hardie J (2001) The role of nutrition, crowding and interspecific interactions in the development of winged aphids. Ecol Entomol 26:330–340

    Article  Google Scholar 

  • Nijhout HF (2003) Development and evolution of adaptive polyphenisms. Evol Dev 5:9–18

    Article  PubMed  Google Scholar 

  • Nishida R (2014) Chemical ecology of insect-plant interactions: ecological significance of plant secondary metabolites. Biosci Biotechnol Biochem 78:1–13

    Article  PubMed  CAS  Google Scholar 

  • Nyman T, Julkunen-Tiitto R (2000) Manipulation of the phenolic chemistry of willows by gall-inducing sawflies. Proc Natl Acad Sci U S A 97:13184–13187

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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 333:474–487

    Article  PubMed  Google Scholar 

  • Philippe RN, Bohlmann J (2007) Poplar defense against insect herbivores. Can J Bot 85:1111–1126

    Article  CAS  Google Scholar 

  • 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 29:89–95

    Article  Google Scholar 

  • Pike N, Whitfield JA, Foster WA (2007) Ecological correlates of sociality in Pemphigus aphids, with a partial phylogeny of the genus. BMC Evol Biol 7:185

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 83:1138–1141

    Article  Google Scholar 

  • Powell G, Tosh CR, Hardie J (2006) Host plant selection by aphids: Behavioral, evolutionary, and applied perspectives. Annu Rev Entomol 51:309–330

    Article  PubMed  CAS  Google Scholar 

  • Prestwich GD (1984) Defense mechanisms of termites. Annu Rev Entomol 29:201–232

    Article  CAS  Google Scholar 

  • Purandare SR, Bickel RD, Jaquiéry J, Rispe C, Brisson JA (2014) Accelerated evolution of morph-biased genes in pea aphids. Mol Biol Evol 31:2073–2083

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Queller DC, Strassmann JE (1998) Kin selection and social insects. Bioscience 48:165–175

    Article  Google Scholar 

  • Ramsewak RS, Nair MG, Murugesan S, Mattson WJ, Zasada J (2001) Insecticidal fatty acids and triglycerides from Dirca palustris. J Agric Food Chem 49:5852–5856

    Article  PubMed  CAS  Google Scholar 

  • Rubenstein DR, Abbot P (2017) Comparative social evolution. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • 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 112:1101–1106

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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 54:1332–1336

    Article  PubMed  CAS  Google Scholar 

  • Shibao H (1999) Reproductive schedule and factors affecting soldier production in the eusocial bamboo aphid Pseudoregma bambucicola (Homoptera, Aphididae). Insect Soc 46:378–386

    Article  Google Scholar 

  • Shibao H, Kutsukake M, Lee JM, Fukatsu T (2002) Maintenance of soldier-producing aphids on an artificial diet. J Insect Physiol 48:495–505

    Article  PubMed  CAS  Google Scholar 

  • Shibao H, Kutsukake M, Fukatsu T (2004a) Density triggers soldier production in a social aphid. Proc R Soc Lond B Biol Sci 271:S71–S74

    Article  Google Scholar 

  • Shibao H, Kutsukake M, Fukatsu T (2004b) The proximate cue of density-dependent soldier production in a social aphid. J Insect Physiol 50:143–147

    Article  PubMed  CAS  Google Scholar 

  • Shibao H, Kutsukake M, Matsuyama S, Fukatsu T, Shimada M (2010) Mechanisms regulating caste differentiation in an aphid social system. Commun Integr Biol 3:1–5

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 19:147–151

    Article  Google Scholar 

  • Shingleton AW, Foster WA (2000) Ant tending influences soldier production in a social aphid. Proc Biol Sci 267:1863–1868

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Simon JC, Stoeckel S, Tagu D (2010) Evolutionary and functional insights into reproductive strategies of aphids. C R Biol 333:488–496

    Article  PubMed  Google Scholar 

  • 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 14:413–423

    Article  PubMed  CAS  Google Scholar 

  • Simpson SJ, Sword GA, Lo N (2011) Polyphenism in insects. Curr Biol 21:738–749

    Article  CAS  Google Scholar 

  • 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 4:706–710

    Article  PubMed  CAS  Google Scholar 

  • 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 36:260–276

    Article  PubMed  CAS  Google Scholar 

  • Srinivasan DG, Brisson JA (2012) Aphids: A model for polyphenism and epigenetics. Genet Res Int 2012:1–12

    Article  CAS  Google Scholar 

  • Stern DL (1994) A phylogenetic analysis of soldier evolution in the aphid family Hormaphididae. Proc R Soc Lond B Biol Sci 256:203–209

    Article  CAS  Google Scholar 

  • Stern DL (1998) Phylogeny of the tribe Cerataphidini (Homoptera) and the evolution of the horned soldier aphids. Evolution 52:155

    Article  PubMed  Google Scholar 

  • Stern DL, Foster WA (1996) The evolution of soldiers in aphids. Biol Rev Camb Philos Soc 71:27–79

    Article  PubMed  CAS  Google Scholar 

  • Strong IE (1963) Studies on lipids in some homopterous insects. Hilgardia 34:43–61

    Article  CAS  Google Scholar 

  • Tagu D, Sabater-Muñoz B, Simon JC (2005) Deciphering reproductive polyphenism in aphids. Invertebr Reprod Dev 48:71–80

    Article  Google Scholar 

  • 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 333:464–473

    Article  PubMed  CAS  Google Scholar 

  • 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 22:551–559

    Article  PubMed  CAS  Google Scholar 

  • 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 40:742–753

    Article  PubMed  CAS  Google Scholar 

  • Tooker JF, Rohr JR, Abrahamson WG, De Moraes CM (2008) Gall insects can avoid and alter indirect plant defenses. New Phytol 178:657–671

  • Toth AL, Rehan SM (2017) Molecular evolution of insect sociality: an eco-evo-devo perspective. Annu Rev Entomol 62:419–442

    Article  PubMed  CAS  Google Scholar 

  • 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 170:727–732

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Uematsu K, Kutsukake M, Fukatsu T, Shimada M, Shibao H (2010) Altruistic colony defense by menopausal female insects. Curr Biol 20:1182–1186

    Article  PubMed  CAS  Google Scholar 

  • 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 42:155–163

    Article  PubMed  CAS  Google Scholar 

  • Vantaux A, Billen J, Wenseleers T (2011) Levels of clonal mixing in the black bean aphid Aphis fabae, a facultative ant mutualist. Mol Ecol 20:4772–4785

    Article  PubMed  CAS  Google Scholar 

  • Vellichirammal NN, Madayiputhiya N, Brisson JA (2016) The genome wide transcriptional response underlying the pea aphid wing polyphenism. Mol Ecol 25:4146–4160

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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 114:1419–1423

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Verheggen FJ, Haubruge E, De Moraes CM, Mescher MC (2009) Social environment influences aphid production of alarm pheromone. Behav Ecol 20:283–288

    Article  Google Scholar 

  • Wang CC, Tsaur SC, Kurosu U, Aoki S, Lee HJ (2008) Social parasitism and behavioral interactions between two gall-forming social aphids. Insect Soc 55:147–152

    Article  Google Scholar 

  • Ward A, Webster M (2016) Sociality: the behaviour of group-living animals. Springer, Switzerland

    Book  Google Scholar 

  • 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 67:763–773

    Article  Google Scholar 

  • Way MJ (1963) Mutualism between ants and honeydew-producing Homoptera. Annu Rev Entomol 8:307–344

    Article  Google Scholar 

  • Webster B (2012) The role of olfaction in aphid host location. Physiol Entomol 37:10–18

    Article  Google Scholar 

  • 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 79:451–457

    Article  Google Scholar 

  • Whitham TG (1986) Cost of benefits of territoriality: behavioral and reproductive release by competing aphids. Ecology 67:139

    Article  Google Scholar 

  • Wilch MH (1999). Predation and prey response in the galls of Pemphigus nr. populi-ramulorum. Masters thesis, University of Arizona

  • Will T, Furch ACU, Zimmermann MR (2013) How phloem-feeding insects face the challenge of phloem-located defenses. Front Plant Sci 4:336

    Article  PubMed  PubMed Central  Google Scholar 

  • Withgott JH, Abbot DK, Moran NA, Moran NA (1997) Maternal death relaxes developmental inhibition in nymphal aphid defenders. Proc R Soc B Biol Sci 264:1197–1202

    Article  Google Scholar 

  • Wool D (2004) Galling aphids: specialization, biological complexity, and variation. Annu Rev Entomol 49:175–192

    Article  PubMed  CAS  Google Scholar 

  • 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 170:736–742

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • 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:e1002930

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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 30:547–556

    Article  Google Scholar 

Download references

Acknowledgments

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

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Patrick Abbot.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Abbot, P., Tooker, J. & Lawson, S.P. Chemical Ecology and Sociality in Aphids: Opportunities and Directions. J Chem Ecol 44, 770–784 (2018). https://doi.org/10.1007/s10886-018-0955-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10886-018-0955-z

Keywords

Navigation