The Ecology of Altruism in a Clonal Insect

  • Nathan Pike
  • William A. Foster

Social aphids are an ideal animal group in which to demonstrate the relative importance of ecological versus genetic factors in the evolution of sociality for several reasons: (1) Since aphids are clonal, the genetics of a colony is starkly simple (the aphids are either from the same clone or they are not) and, in principle, easy to measure; (2) Because good phylogeni es are available for several aphid taxa and there is clear evidence that there have been more independent origins of sociality in aphids than in any other social clade, it is possible to test for associations between ecological factors and the evolution of sociality; (3) Recent developments, in the understanding of the mechanism of the proximate control of soldier development, in the genetic basis of sociality, and in models of social evolution, make the social aphids an ideal group for experimental work on the evolution of social behavior; (4) The social aphids are of special ecological interest because they include the only organisms that have evolved sterile castes in societies that do not occupy some kind of nest (the secondary-host generations of the Hormaphidinae).

The ecological context of altruism in social aphids has been shown to be quite intricate since it is now clear that colony defense is not the only costly behavior that they perform: they also have vital roles in keeping the colony clean, migrating to new colonies, and repairing their nest. Numerous ecological factors are highly pertinent in aphid social evolution including (1) the fact that all social aphids have at some stage in their life cycle a valuable and defensive fortress in the form of a plant gall, (2) population size and density, (3) birth rate, (4) the level of exposure to specialized predation, and (5) variation in the level of tending provided by ants. Kin selection in social aphids has given rise not only to a range of elaborate adaptations in behavior and morphology but also to impressive short-term flexibility in social investment. For example, in species that have specialized defenders that can mature to make a direct contribution to their colony’s fitness, defense investment can be increased both through heightened production of defenders at birth and prolongation of the defender stage.

We demonstrate that ecological factors are essential in any attempt to understand the role of kin selection in the evolution of social behavior in a group of organisms: ecology determines the extent to which groups consist of related individuals and the context in which these individuals can give and receive help.


Aphid Species Defensive Behavior Aphid Density Behav Ecol Aphid Colony 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Abbot P, Withgott JH, Moran NA (2001) Genetic conflict and conditional altruism in social aphid colonies. Proc Natl Acad Sci USA 98:12068-12071CrossRefPubMedGoogle Scholar
  2. Akimoto S (1983) A revision of the genus Eriosoma and its allied genera in Japan (Homoptera: Aphidoidea). Ins Mats 27:37-106Google Scholar
  3. 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
  4. Akimoto S (1996) Ecological factors promoting the evolution of colony defense in aphids: computer simulations. Insectes Soc 43:1-15CrossRefGoogle Scholar
  5. Akimoto S, Ozaki K, Matsumoto Y (1996) Production of first-instar defenders by the hormaphidid gall-forming aphid Hamamelistes cristafoliae living anholocyclically on Betula maximowic-ziana. Jpn J Entomol 64:879-888Google Scholar
  6. Aoki S (1977) Colophina clematis (Homoptera, Pemphigidae), an aphid species with “soldiers”. Kontyû 45:276-282Google Scholar
  7. Aoki S (1980) Occurrence of a simple labor in a gall aphid, Pemphigus dorocola (Homoptera, Pemphigidae). Kontyû 48:71-73Google Scholar
  8. Aoki S (1982) Soldiers and altruistic dispersal in aphids. In: Breed MD, Michener CD, Evans HE (eds) The biology of social insects. Westview Press, Boulder, pp 154-158Google Scholar
  9. Aoki S, Imai M (2005) Factors affecting the proportion of sterile soldiers in growing aphid colonies. Pop Ecol 47:127-136CrossRefGoogle Scholar
  10. Aoki S, Kurosu U (1989a) Soldiers of Astegopteryx styraci (Homoptera, Aphidoidea) clean their gall. Jpn J Entomol 57:407-416Google Scholar
  11. Aoki S, Kurosu U (1989b) Two kinds of soldier in the tribe Cerataphidini(Homoptera: Aphidoidea). J Aphidol 3:1-7Google Scholar
  12. Aoki S, Kurosu U (1991) Galls of the soldier-producing aphid Ceratoglyphina bambusae broken by vertebrates (Homoptera, Aphidoidea). Jpn J Entomol 59:743-746Google Scholar
  13. Aoki S, Kurosu U (1992a) Gall generations of the soldier-producing aphid Pseudoregma bambucicola (Homoptera). Jpn J Entomol 60:359-368Google Scholar
  14. Aoki S, Kurosu U (1992b) No attack on conspecifics by soldiers of the gall aphid Ceratoglyphina bambusae (Homoptera) late in the season. Jpn J Entomol 60:707-713Google Scholar
  15. Aoki S, Kurosu U (2003) Logistic model for soldier production in aphids. Insectes Soc 50:256-261CrossRefGoogle Scholar
  16. Aoki S, Kurosu U (2004) How many soldiers are optimal for an aphid colony? J Theor Biol 230:313-317CrossRefPubMedGoogle Scholar
  17. Aoki S, Miyazaki M (1978) Notes on the pseudoscorpion-like larvae of Pseudoregma alexanderi (Homoptera, Aphidoidea). Kontyû 46:433-438Google Scholar
  18. Aoki S, Akimoto S, Yamane S (1981) Observations on Pseudoregma alexanderi (Homoptera, Pemphigidae), an aphid species producing pseudoscorpion-like soldiers on bamboos. Kontyû 49:355-366Google Scholar
  19. Aoki S, Kurosu U, Usuba S (1984) First instar larvae of the Sugar-Cane Wooly Aphid, Ceratovacuna lanigera (Homoptera, Pemphigidae), attack its predators. Kontyû 52:458-460Google Scholar
  20. 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
  21. Aoki S, Kurosu U, von Dohlen CD (2001) Colony defense by wingpadded nymphs in Grylloprociphilus imbricator (Hemiptera: Aphididae). Fla Entomol 84:431-434CrossRefGoogle Scholar
  22. Benton TG, Foster WA (1992) Altruistic housekeeping in a social aphid. Proc R Soc Lond B 247:199-202CrossRefGoogle Scholar
  23. Carlin NF, Gladstein DS, Berry AJ, Pierce NE (1994) Absence of kin discrimination behavior in a soldier-producing aphid, Ceratovacuna japonica (Hemiptera: Pemphigidae; Cerataphidini). J NY Entomol Soc 102:287-298Google Scholar
  24. Crespi BJ (2001) The evolution of social behavior in microorganisms. Trends Ecol Evol 16:178-183CrossRefPubMedGoogle Scholar
  25. Cruz YP, Oelhaf Jr. RC, Jockusch EL (1990) Polymorphic precocious larvae in the polyembryonic parasitoid (Hymenoptera: Encyrtidae). Ann Entomol Soc Am 83:549-554Google Scholar
  26. Duffy JE, Morrison CL, Macdonald KS (2002) Colony defense, division of labor, and productivity in the eusocial shrimp Synalpheus regalis. Behav Ecol Sociobiol 51:488-495CrossRefGoogle Scholar
  27. Foster WA (1990) Experimental evidence for effective and altruistic colony defence against natu-ral predators by soldiers of the gall-forming aphid Pemphigus spyrothecae (Hemiptera: Pemphigidae). Behav Ecol Sociobiol 27:421-430CrossRefGoogle Scholar
  28. Foster WA (2003) Soldier aphids go cuckoo. Trends Ecol Evol 17:199-200CrossRefGoogle Scholar
  29. Foster WA, Northcott PA (1994) Galls and the evolution of social behaviour in aphids. In: Williams MAJ (ed) Plant galls: organisms, interactions, populations. Clarendon Press, Oxford, pp 161-182Google Scholar
  30. Fukatsu T, Aoki S, Kurosu U, Ishikawa H (1994) Phylogeny of Cerataphidini aphids revealed by their symbiotic microorganisms and basic structure of their galls: implications for host-symbiont coevolution and evolution of sterile soldier castes. Zool Sci 11:613-623Google Scholar
  31. Griffin AS, West SA, Buckling A (2004) Cooperation and competition in pathogenic bacteria. Nature 430:1024-1027CrossRefPubMedGoogle Scholar
  32. Gullan PJ, Cranston PS (1994) The insects: an outline of entomology. Chapman and Hall, London Hamilton WD (1964) The genetical evolution of social behaviour. II. J Theor Biol 7:17-52Google Scholar
  33. Hamilton WD (1972) Altruism and related phenomena mainly in social insects. Annul Rev Ecol Syst 3:193-232CrossRefGoogle Scholar
  34. Hamilton WD (1987) Kinship, recognition, disease, and intelligence: constraints of social evolu-tion. In: Itô Y, Brown JL, Kikkawa J (eds) Animal societies: theories and facts. Jpn Sci Soc Press, Tokyo, pp 81-102Google Scholar
  35. Hölldobler B, Wilson EO (1990) The ants. Springer, Berlin Heidelberg New York, 732 ppGoogle Scholar
  36. Ijichi N, Shibao H, Miura T, Matsumoto T, Fukatsu T (2004) Soldier differentiation during embryogenesis of a social aphid, Pseudoregma bambucicola. Entomol Sci 7:143-155CrossRefGoogle Scholar
  37. Ijichi N, Shibao H, Miura T, Matsumoto T, Fukatsu T (2005) Comparative analysis of caste dif-ferentiation during embryogenesis of social aphids whose soldier castes evolved independ-ently. Insectes Soc 52:177-185CrossRefGoogle Scholar
  38. Inbar M (1998) Competition, territoriality and maternal defense in a gall-forming aphid. Ethol Ecol Evol 10:159-170Google Scholar
  39. Itô Y, Tanaka S, Yukawa J, Tsuji K (1995) Factors affecting the proportion of soldiers in eusocial bamboo aphid, Pseudoregma bambucicola, colonies. Ethol Ecol Evol 7:335-345Google Scholar
  40. Johnson PCD, Whitfield JA, Foster WA, Amos W (2002) Clonal mixing in the soldier-producing aphid Pemphigus spyrothecae (Hemiptera: Aphididae). Mol Ecol 11:1525-1531CrossRefPubMedGoogle Scholar
  41. Krebs JR, Davies NB (1993) An introduction to behavioural ecology, 3rd edn. Blackwell, OxfordGoogle Scholar
  42. Kurosu U, Aoki S (1988) First-instar aphids produced late by the fundatrix of Ceratovacuna nekoashi (Homoptera) defend their closed gall outside. J Ethol 6:99-104CrossRefGoogle Scholar
  43. Kurosu U, Aoki S (1991) Gall cleaning by the aphid Hormaphis betulae. J Ethol 9:51-55CrossRefGoogle Scholar
  44. Kurosu U, Aoki S, Fukatsu T (2003) Self-sacrificing gall repair by aphid nymphs. Proc R Soc Lond B (Suppl) 270:S12-S14CrossRefGoogle Scholar
  45. Kurosu U, Buranapanichpan S, Aoki S (2006a) AAstegopteryx spinocephala(Hemiptera: Aphididae), a new aphid species producing sterile soldiers that guard eggs laid in their gall. Entomol Sci 9:181-190CrossRefGoogle Scholar
  46. Kurosu U, Narukawa J, Buranapanichpan S, Aoki S (2006b) Head-plug defense in a gall aphid. Insectes Soc 53:86-91CrossRefGoogle Scholar
  47. Kutsukake M, Shibao H, Nikoh N, Morioka M, Tamura T, Hoshino T, Ohgiya S, Fukatsu T (2004) Venomous protease of aphid soldier for colony defense. Proc Natl Acad Sci USA 101:11338-11343CrossRefPubMedGoogle Scholar
  48. Ortiz-Rivas B, Moya A, Martinez-Torres D (2004) Molecular systematics of aphids (Homoptera: Aphididae): new insight from the long-wavelength opsin gene. Mol Phylogenet Evol 30:24-37CrossRefPubMedGoogle Scholar
  49. Pike N (2002) Defence investment and altruism in Pemphigus Aphids. PhD Thesis, University of Cambridge, CambridgeGoogle Scholar
  50. Pike N (2007) Specialised placement of morphs within the gall of the social aphid Pemphigus spyrothecae. BMC Evol Biol 7:18CrossRefPubMedGoogle Scholar
  51. Pike N, Foster WA (2004) Fortress repair in the social aphid species, Pemphigus spyrothecae. Anim Behav 67:909-914CrossRefGoogle Scholar
  52. Pike N, Manica A (2006a) The optimal balance of defence investment strategies in clonal colonies of social aphids. Behav Ecol Sociobiol 60:803-814CrossRefGoogle Scholar
  53. Pike N, Manica A (2006b) The basis of cowardice in social defenders. Ecol Model 196:275-282CrossRefGoogle Scholar
  54. Pike N, Richard D, Foster WA, Mahadevan L (2002) How aphids lose their marbles. Proc R Soc Lond B 269:1211-1215CrossRefGoogle Scholar
  55. 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
  56. Price PW, Fernandes GW, Waring GL (1987) Adaptive nature of insect galls. Environ Entomol 16:15-24Google Scholar
  57. Queller DC (2004) Kinship is relative. Nature 430:975-976CrossRefPubMedGoogle Scholar
  58. Queller DC, Strassmann JE (1998) Kin selection and social insects. Bioscience 48:165-175CrossRefGoogle Scholar
  59. Remaudière G, Remaudière M (1997) Catalogue des aphides du monde. INRA, ParisGoogle Scholar
  60. Rhoden PK, Foster WA (2002) Soldier behaviour and division of labour in the aphid genus Pemphigus (Hemiptera: Aphididae). Insects Sociaux 49:257-263CrossRefGoogle Scholar
  61. Sakata K, Itô Y, Yukawa J, Yamane S (1991) Ratio of sterile soldiers in the Bamboo Aphid, Pseudoregma bambucicola (Homoptera: Aphididae), colonies in relation to social and habitat conditions. Appl Entomol Zool 26:463-468Google Scholar
  62. Schütze M, Maschwitz U (1991) Enemy recognition and defence within trophobiotic associations with ants by the soldier caste of Pseudoregma sundanica (Homoptera: Aphidoidea). Entomol Gener 16:1-12Google Scholar
  63. Setzer RW (1980) Intergall migration in the aphid genus Pemphigus. Ann Entomol Soc Am 73:327-331Google Scholar
  64. Shibao H (1998) Social structure and the defensive role of soldiers in a eusocial bamboo aphid, Pseudoregma bambucicola (Homoptera: Aphididae): a test of the defence-optimization hypothesis. Res Popul Ecol 40:325-333CrossRefGoogle Scholar
  65. Shibao H (1999a) Reproductive schedule and factors affecting soldier production in the eusocial bamboo aphid, Pseudoregma bambucicola (Homoptera: Aphididae). Insectes Soc 46:378-386CrossRefGoogle Scholar
  66. Shibao H (1999b) Lack of kin discrimination in the eusocial aphid Pseudoregma bambucicola (Homoptera: Aphididae). J Ethol 17:17-24CrossRefGoogle Scholar
  67. Shibao H, Kutsukake M, Lee J-M, Fukatsu T (2002) Maintenance of soldier-producing aphids on an artificial diet. J Insect Physiol 48:495-505CrossRefPubMedGoogle Scholar
  68. Shibao H, Lee J, Kutsukake M, Fukatsu T (2003) Aphid soldier differentiation: density acts on both embryos and newborn nymphs. Naturwissenschaften 90:501-504CrossRefPubMedGoogle Scholar
  69. Shibao H, Kutsukake M, Fukatsu T (2004a) Density triggers soldier production in a social aphid. Proc R Soc Lond B (Suppl) 271:S71-S74CrossRefGoogle Scholar
  70. Shibao H, Kutsukake M, Fukatsu T (2004b) Density-dependent induction and suppression of soldier differentiation in an aphid social system. J Insect Physiol 50:995-1000CrossRefPubMedGoogle Scholar
  71. Shingleton AW, Foster WA (2000) Ant-tending influences soldier production in a social aphid. Proc R Soc Lond B 267:1863-1868CrossRefGoogle Scholar
  72. Shingleton AW, Foster WA (2001) Behaviour, morphology and the division of labour in two soldier-producing aphids. Anim Behav 62:671-679CrossRefGoogle Scholar
  73. Stern DL (1998) Phylogeny of the tribe Cerataphidini (Homoptera) and the evolution of the horned soldier aphids. Evolution 52:155-165CrossRefGoogle Scholar
  74. Stern DL, Foster WA (1996) The evolution of soldiers in aphids. Biol Rev Camb Philos Soc 71:27-79CrossRefPubMedGoogle Scholar
  75. Stern DL, Foster WA (1997) The evolution of sociality in aphids: a clone’s-eye view. In: Choe JC, Crespi BJ (eds) Social behaviour in insects and arachnids. Cambridge University Press, Cambridge, pp 150-165Google Scholar
  76. Stern DL, Aoki S, Kurosu U (1994) A test of geometric hypotheses for soldier investment patterns in the gall producing tropical aphid Cerataphis fransseni (Homoptera, Hormaphididae). Insectes Soc 41:457-460CrossRefGoogle Scholar
  77. Sunose T, Tsuda K, Ohseko S (1982) Seasonal change in ratios of soldier in a population of the bamboo aphid, Psuedoregma bambucicola. Bull Soc Popul Ecol 35:59-61Google Scholar
  78. Tyerman JB, Roitberg BD (2004) Factors affecting soldier allocation in clonal aphids: a life-history model and test. Behav Ecol 15:94-101CrossRefGoogle Scholar
  79. Withgott JH, Abbot DK, Moran NA (1997) Maternal death relaxes developmental inhibition in nymphal aphid defenders. Proc R Soc Lond B 264:1197-1202CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2008

Authors and Affiliations

  • Nathan Pike
    • 1
  • William A. Foster
    • 2
  1. 1.Department of ZoologyOxford UniversityUK
  2. 2.Department of ZoologyUniversity of CambridgeUK

Personalised recommendations