Advertisement

Insectes Sociaux

, Volume 61, Issue 4, pp 395–402 | Cite as

High mean relatedness among communally galling Tamalia aphids revealed by AFLP analysis

  • B. G. Taylor
  • D. G. MillerEmail author
Research Article

Abstract

Cooperative or eusocial behavior occurs in gall-inducing insects, but the ecological and evolutionary contexts for these behaviors vary in their details. Foundresses of the manzanita leaf-gall aphid, Tamalia coweni, regularly share galls. Because aphids undergo parthenogenesis, communal foundresses are potential clone mates. Under the kin selection hypothesis, a high level of relatedness is predicted to lower genetically based conflict among females in a group and thereby favor communal gall occupation. We recorded the frequency of communal behavior in a population of T. coweni on its host plant, Arctostaphylos patula, and measured reproductive output in single- and multiple-occupant galls. Eleven percent of the 375 galls examined were communally occupied, with double-foundress galls the commonest class, up to a maximum of five foundresses within galls. Total productivity of communal galls (measured by numbers of offspring per gall) was higher than for single-foundress galls on a per-gall basis, but lower per capita. We genotyped foundresses with amplified fragment length polymorphism (AFLP)-PCR markers, to estimate relatedness among gall co-occupants and foundresses from randomly selected galls in the population. Analysis of genetic distance between communal foundresses revealed that relatedness among gall cohabitants was significantly higher, on average, than for foundresses drawn from the population at random (P < 0.001). Phylogenetic analysis using parsimony (PAUP) of the AFLP profiles indicated that half the foundresses sharing galls were most closely related to their gall mates. Our results are consistent with kin selection theory, and suggest that communal gall occupation in this species may be interpreted as cooperative behavior.

Keywords

Galling aphids Communal Kin selection Relatedness Tamalia 

Notes

Acknowledgments

This work was performed in partial fulfillment of a Master’s degree in Biological Sciences at California State University, Chico, and was supported by the Big Chico Creek Ecological Reserve and the CSU, Chico Office of Graduate studies. BGT is grateful to Kristina Schierenbeck and Andrea White for their assistance and support, and would like to thank David H. Kistner, the staff of the CSU, Chico Aquatic Bioassessment Lab and the staff of the CSUC Department of Biological Sciences.

References

  1. Abbot P., Withgott J.H. and Moran N. 2001. Genetic conflict and conditional altruism in social aphid colonies. Proc. Natl Acad. Sci. USA 98: 12068-12071Google Scholar
  2. Abbot P. et al. 2011. Inclusive fitness theory and eusociality. Nature 471: E1-E4Google Scholar
  3. Addicott J.F. 1979. On the population biology of aphids. Am. Nat. 114: 760-763Google Scholar
  4. Akçay E., Meirowitz A., Ramsay K.W. and Levin S.A. 2012. Evolution of cooperation and skew under imperfect information. Proc. Natl Acad. Sci. USA 109: 14936-14941Google Scholar
  5. Aoki S., Kurosu U. and Stern D.L. 1991. Aphid soldiers discriminate between soldiers and non-soldiers, rather than between kin and non-kin, in Ceratoglyphina bambusae. Anim. Behav. 42: 865-866Google Scholar
  6. Aoki S. and Makino S. 1982. Gall usurpation and lethal fighting among fundatrices of the aphid Epipemphigus niisimae (Homoptera, Pemphigidae). Kontyû 45: 276-282Google Scholar
  7. Blackman R.L. 1994. The simplification of aphid terminology. Eur. J. Entomol. 91: 139-141Google Scholar
  8. Bourke A.F.G. 2011. The validity and value of inclusive fitness theory. Proc. R. Soc. B 278: 3313-3320Google Scholar
  9. Bryden J. and Jansen V.A.A. 2010. The impact of clonal mixing on the evolution of social behaviour in aphids. Proc. R. Soc. B 277: 1651-1657Google Scholar
  10. Cole B.J. 1984. Colony efficiency and the reproductivity effect in Leptothorax allardycei (Mann). Insect. Soc. 31: 403-407Google Scholar
  11. Dixon A.F.G. 1998. Aphid Ecology, 2nd ed. Chapman & Hall, LondonGoogle Scholar
  12. Fletcher J.A. and Zwick M. 2006. Unifying the theories of inclusive fitness and reciprocal altruism. Am. Nat. 168: 252-262Google Scholar
  13. Foster W.A. and Northcutt P.K. 1994. Galls and the evolution of social behavior in aphids. Syst. Assoc. 49: 161-182Google Scholar
  14. Hamilton W.D. 1963. The evolution of altruistic behavior. Am. Nat. 97: 354-356Google Scholar
  15. Hamilton W.D. 1964. The genetical evolution of social behavior. I. J. Theor. Biol. 7: 1-16Google Scholar
  16. Hamilton W.D. 1967. Extraordinary sex ratios. Science 156: 477-488Google Scholar
  17. Hamilton W.D. 1972. Altruism and related phenomena, mainly in the social insects. Annu. Rev. Ecol. Syst. 3: 193-232Google Scholar
  18. Hamilton W.D. 1987. Kinship, recognition and disease: constraints of social evolution. In: Animal Societies: Theories and Facts (Itô Y., Brown J.L. and Kikkawa K., Eds). Japan Scientific Societies Press, Tokyo, pp 81-102Google Scholar
  19. Hawthorne D.J. and Via S. 2001. Genetic linkage of ecological specialization and reproductive isolation in pea aphids. Nature 412: 904-907Google Scholar
  20. Holland B.R., Clarke A.C. and Meudt H.M. 2008. Optimizing automated AFLP scoring parameters to improve phylogenetic resolution. Syst. Biol. 57: 347-366Google Scholar
  21. Hölldobler B. and Wilson E.O. 1990. The Ants. Belknap Press, Cambridge, MAGoogle Scholar
  22. Inbar M. 1998. Competition, territoriality, and maternal defense in a gall-forming aphid. Ethol. Ecol. Evol. 10: 159-170Google Scholar
  23. Itô Y. 1989. The evolutionary biology of sterile soldiers in aphids. Trends Ecol. Evol. 4: 69-73Google Scholar
  24. Itô Y. 1993. Behaviour and Social Evolution of Wasps: The Communal Aggregation Hypothesis. Oxford University Press, OxfordGoogle Scholar
  25. Janzen D. 1977. What are dandelions and aphids? Am. Nat. 111: 586-589Google Scholar
  26. Johnson P.C.D., Whitfield J.A., Foster W.A. and Amos W. 2002. Clonal mixing in the soldier-producing aphid Pemphigus spyrothecae (Hemiptera: Aphididae). Mol. Ecol. 11: 1525-1531Google Scholar
  27. Leadbeater E., Carruthers J.M., Green J.P., Rosser N.S. and Field J. 2011. Nest inheritance is the missing source of direct fitness in a primitively social insect. Science 333: 874-876Google Scholar
  28. Loxdale H.D. 2008. The nature and reality of the aphid clone: genetic variation, adaptation and evolution. Agr. Forest Entomol. 10: 81-90Google Scholar
  29. Maynard Smith J. 1964. Group selection and kin selection. Nature 201: 1145-1147Google Scholar
  30. Maynard Smith J. and Szathmáry E. 1995. The Major Transitions in Evolution. Oxford University Press, NYGoogle Scholar
  31. Michener C.D. 1964. Reproductive efficiency in relation to colony size in hymenopterous societies. Insect. Soc. 11: 317-341Google Scholar
  32. Michener C.D. 1974. The Social Behavior of the Bees. Belknap Press, Cambridge, MAGoogle Scholar
  33. Michener C.D. and Lange R.B. 1958. Distinctive type of primitive social behavior among bees. Science 127: 1046-1047Google Scholar
  34. Miller D.G. III 1998a. Life history, ecology and communal gall occupation in the manzanita leaf-gall aphid, Tamalia coweni (Cockerell) (Homoptera: Aphididae). J. Nat. Hist. 32: 95-103Google Scholar
  35. Miller D.G. III 1998b. Consequences of communal gall occupation and a test for kin discrimination in the aphid Tamalia coweni (Cockerell) (Homoptera: Aphididae). Behav. Ecol. Sociobiol. 43: 95-103Google Scholar
  36. Miller D.G. III 2004. The ecology of inquilinism in communally parasitic Tamalia aphids (Hemiptera: Aphididae). Ann. Entomol. Soc. Am. 97: 1233-1241Google Scholar
  37. Miller D.G. III 2005. Ecology and radiation of galling aphids (Tamalia; Hemiptera: Aphididae) on their host plants (Ericaceae). Basic Appl. Ecol. 6: 463-469Google Scholar
  38. Miller D.G. III and Avilés L. 2000. Sex ratio and brood size in a monophagous outcrossing gall aphid, Tamalia coweni. Evol. Ecol. Res. 2: 745-759Google Scholar
  39. Miller D.G. III and Crespi B. 2003. The evolution of inquilinism, host-plant use, and mitochondrial substitution rates in Tamalia gall aphids. J. Evol. Biol. 16: 731-743Google Scholar
  40. Monti V., Mandrioli M., Rivi M. and Manicardi G.C. 2012. The vanishing clone: karyotypic evidence for extensive intraclonal genetic variation in the peach potato aphid, Myzus persicae (Hemiptera: Aphididae). Biol. J. Linn. Soc. 105: 350-358Google Scholar
  41. Mueller U.G. and Wolfenbarger L.L. 1999. AFLP genotyping and fingerprinting. Trends Ecol. Evol. 14: 389-394Google Scholar
  42. Nei M.and Li W. 1979. Mathematical model for studying genetic variation in terms of restriction endonucleases. Proc. Natl Acad. Sci. USA 76: 5269-5273Google Scholar
  43. Nowak M.A., Tarnita C.E. and Wilson E.O. 2010. The evolution of eusociality. Nature 466: 1057-1062Google Scholar
  44. Oliveira P.S., Camargo R.X. and Fourcassié V. 2011. Nesting patterns, ecological correlates of polygyny and social organization in the neotropical arboreal ant Odontomachus hastatus (Formicidae, Ponerinae). Insect. Soc. 58: 207-217Google Scholar
  45. Ren N. and Timko M.P. 2001. AFLP analysis of genetic polymorphism and evolutionary relationships among cultivated and wild Nicotiana species. Genome 44: 559-571Google Scholar
  46. Ross K.G. and Matthews R.W. (Eds) 1991. The Social Biology of Wasps. Comstock Publisher Associates, Ithaca, NYGoogle Scholar
  47. Seger J. 1993. Opportunities and pitfalls in cooperative reproduction. In: Queen Number and Sociality in Insects (Keller L., Ed). Oxford University Press, Oxford, pp 1-15Google Scholar
  48. Sherman P.W., Lacey E.A., Reeve H.K. and Keller L. 1995. The eusociality continuum. Behav. Ecol. 6: 102-108Google Scholar
  49. Shibao H. 1999. Lack of kin discrimination in the eusocial aphid Pseudoregma bambucicola (Homoptera: Aphididae). J. Ethol. 17: 17-24Google Scholar
  50. Stern D.L. and Foster W.A. 1996. The evolution of soldiers in aphids. Biol. Rev. 71: 27-79Google Scholar
  51. Timm A.E., Pringlea K.L. and Warnicha L. 2005. Genetic diversity of woolly apple aphid Eriosoma lanigerum (Hemiptera: Aphididae) populations in the Western Cape, South Africa. Bull. Entomol. Res. 95: 187-191Google Scholar
  52. Valenti M.A., Berryman A.A. and Ferrel G.T. 1996. Arthropods associated with a manzanita gall induced by the aphid Tamalia coweni (Cockerell) (Homoptera: Aphididae). Can. Entomol. 128: 839-847Google Scholar
  53. Vargo E.L. 1993. Colony reproductive structure in a polygyne population of Solenopsis geminata (Hymenoptera: Formicidae). Ann. Entomol. Soc. Am. 86: 441-449Google Scholar
  54. Vorwerk S. 2007. Molecular evidence of intraclonal variation and implications for adaptational traits of grape phylloxera populations (Daktulosphaira vitifoliae, Fitch). Dissertation, University of HohenheimGoogle Scholar
  55. Vorwerk S. and Forneck A. 2007. Analysis of genetic variation within clonal lineages of grape phylloxera (Daktulosphaira vitifoliae Fitch) using AFLP fingerprinting and DNA sequencing. Genome 50: 660-667Google Scholar
  56. Vos P., Hogers R., Bleeker M., Reijans M., Lee T., Hornes M., Frijters A., Pot J., Peleman J., Kuiper M. and Zabeau M. 1995. AFLP: a new technique for DNA fingerprinting. Nucl. Acids Res. 23: 4407-4414Google Scholar
  57. Vuylsteke M., Peleman J.D. and van Eijk M.J.T. 2007. AFLP technology for DNA fingerprinting. Nature Protocols 2: 1387-1398Google Scholar
  58. Wang C.C., Tsaur S.-C., Kurosu U., Aoki S. and Lee H.-J. 2008. Social parasitism and behavioral interactions between two gall-forming social aphids. Insect. Soc. 55: 147-152Google Scholar
  59. Weisser W.W. and Stadler B. 1994. Phenotypic plasticity and fitness in aphids. Eur. J. Entomol. 91: 71-78Google Scholar
  60. West S.A, Pen I. and Griffin A.S. 2002. Cooperation and conflict between relatives. Science 296: 72-75Google Scholar
  61. Wilson E.O. 1971. The Insect Societies. Belknap Press, Cambridge, MAGoogle Scholar
  62. Whitham T.G. 1978. Habitat selection by Pemphigus aphids in response to resource limitation and competition. Ecology 59: 1164-1176Google Scholar
  63. Whitham T.G. 1979. Territorial behavior of Pemphigus gall aphids. Nature 279: 324-325Google Scholar

Copyright information

© International Union for the Study of Social Insects (IUSSI) 2014

Authors and Affiliations

  1. 1.Department of Biological Sciences, and Center for Water and the EnvironmentCalifornia State UniversityChicoUSA

Personalised recommendations