Intragenomic conflict over queen determination favours genomic imprinting in eusocial hymenoptera

Proceedings of the Royal Society B: Biological Sciences

Volumn 279, Issue 1738, 2012, Pages 2553-2560

  Dobata, Shigeto ^a   Tsuji, Kazuki ^a,b  

^a UNIVERSITY OF THE RYUKYUS   (Japan)

^b KAGOSHIMA UNIVERSITY   (Japan)

Author keywords

DNA methylation; Genetic caste determination; Intralocus sexual conflict; Polyandry; Social hybridogenesis; Tragedy of the commons

Indexed keywords

APOCRITA; FORMICIDAE; HYMENOPTERA; LINEPITHEMA HUMILE;

ANIMAL; ANT; ARTICLE; BIOLOGICAL MODEL; FEMALE; GENETICS; GENOME IMPRINTING; HYMENOPTERA; MALE; MUTATION; PHYSIOLOGY; SEX RATIO; SEXUAL BEHAVIOR; SOCIAL BEHAVIOR; SOCIAL DOMINANCE;

ANIMALS; ANTS; FEMALE; GENOMIC IMPRINTING; HIERARCHY, SOCIAL; HYMENOPTERA; MALE; MODELS, GENETIC; MUTATION; SEX RATIO; SEXUAL BEHAVIOR, ANIMAL; SOCIAL BEHAVIOR;

EID: 84987741078     PISSN: 09628452     EISSN: 14712954     Source Type: Journal    
DOI: 10.1098/rspb.2011.2673     Document Type: Article

References (46)

1. Maynard Smith, J. & Szathmáry, E. 1995 The major transitions in evolution. Oxford, UK: Oxford University Press.
2. Burt, A. & Trivers, R. 2006 Genes in conflict. Cambridge, MA: Harvard University Press.
3. Arnqvist, G. & Rowe, L. 2005 Sexual conflict. Princeton, NJ: Princeton University Press.
4. Crozier, R. H. & Pamilo, P. 1996 Evolution of social insect colonies. Oxford, UK: Oxford University Press.
5. Haig, D. & Westoby, M. 1989 Parent specific gene expression and the triploid endosperm. Am. Nat. 134, 147–155. (doi:10.1086/284971)
6. Haig, D. 2000 The kinship theory of genomic imprinting. Ann. Rev. Ecol. Syst. 31, 9–32. (doi:10.1146/annurev. ecolsys.31.1.9)
7. Queller, D. C. 2003 Theory of genomic imprinting conflict in social insects. BMC Evol. Biol. 3, 15. (doi:10. 1186/1471-2148-3-15)
8. Haig, D. & Graham, C. 1991 Genomic imprinting and the strange case of the insulin-like growth factor II receptor. Cell 64, 1045–1046. (doi:10.1016/0092-8674 (91)90256-X)
9. Ratnieks, F. L. W., Foster, K. R. & Wenseleers, T. 2006 Conflict resolution in insect societies. Ann. Rev. Entomol. 51, 581–608. (doi:10.1146/annurev.ento.51.110104. 15100)
10. Kronforst, M. R., Gilley, D. C., Strassmann, J. E. & Queller, D. C. 2008 DNA methylation is widespread across social Hymenoptera. Curr. Biol. 18, R287–R288. (doi:10.1016/j.cub.2008.02.015)
11. Wang, Y., Jorda, M., Jones, P. L., Maleszka, R., Ling, X., Robertson, H. M., Mizzen, C. A., Peinado, M. A. & Robinson, G. E. 2006 Functional CpG methylation system in a social insect. Science 314, 645–647. (doi:10. 1126/science.1135213)
12. Bonasio, R. et al. 2010 Genomic comparison of the ants Camponotus floridanus and Harpegnathos saltator. Science 329, 1068–1071. (doi:10.1126/science.1192428)
13. Suen, G. et al. 2011 The genome sequence of the leaf-cutter ant Atta cephalotes reveals insights into its obligate symbiotic lifestyle. PLoS Genet. 7, e1002007. (doi:10. 1371/journal.pgen.1002007)
14. Smith, C. R. et al. 2011 Draft genome of the red harvester ant Pogonomyrmex barbatus. Proc. Natl Acad. Sci. USA 108, 5667–5672. (doi:10.1073/pnas.1007901108)
15. Smith, C. D. et al. 2011 Draft genome of the globally widespread and invasive Argentine ant (Linepithema humile). Proc. Natl Acad. Sci. USA 108, 5673–5678. (doi:10.1073/pnas.1008617108)
16. Wurm, Y. et al. 2011 The genome of the fire ant Solenopsis invicta. Proc. Natl Acad. Sci. USA 108, 5679–5684. (doi:10.1073/pnas.1009690108)
17. Nygaard, S. et al. 2011 The genome of the leaf-cutting ant Acromyrmex echinatior suggests key adaptations to advanced social life and fungus farming. Genome Res. 21, 1339–1348. (doi:10.1101/gr.121392.111)
18. Haig, D. 1992 Intragenomic conflict and the evolution of eusociality. J. Theor. Biol. 156, 401–403. (doi:10.1016/ S0022-5193(05)80683-6)
19. Queller, D. C. & Strassman, J. E. 2002 The many selves of social insects. Science 296, 311–313. (doi:10.1126/ science.1070671)
20. Kronauer, D. J. C. 2008 Genomic imprinting and kinship in the social Hymenoptera: what are the predictions? J. Theor. Biol. 254, 737–740. (doi:10.1016/j.jtbi.2008. 06.019)
21. Wild, G. & West, S. A. 2009 Genomic imprinting and sex allocation. Am. Nat. 173, E1–E14. (doi:10.1086/ 593305)
22. Guzman-Novoa, E., Hunt, G. J., Page, R. E., Uribe-Rubio, J. L., Prieto-Merlos, D. & Becerra-Guzman, F. 2005 Paternal effects on the defensive behavior of honeybees. J. Heredity 96, 376–380. (doi:10.1093/jhered/ esi038)
23. Libbrecht, R., Schwander, T. & Keller, L. 2011 Genetic components to caste allocation in a multiple-queen ant species. Evolution 65, 2907–2915. (doi:10.1111/j.1558-5646.2011.01348.x)
24. Hardin, G. 1968 The tragedy of the commons. Science 162, 1243–1244. (doi:10.1126/science.162. 3859.1243)
25. Mochizuki, A., Takada, Y. & Iwasa, Y. 1996 The evolution of genomic imprinting. Genetics 144, 1283–1295.
26. Iwasa, Y., Nee, S. & Pomiankowski, A. 1991 The evolution of costly mate preferences. II. The handicap principle. Evolution 45, 1431–1442.
27. Iwasa, Y. & Pomiankowski, A. 2001 The evolution of X-linked genomic imprinting. Genetics 158, 1801–1809.
28. Dobata, S. Submitted. Arms race between selfishness and policing: two-trait quantitative genetic model for caste fate conflict in eusocial Hymenoptera.
29. Wenseleers, T., Ratnieks, F. L. W. & Billen, J. 2003 Caste fate conflict in swarm-founding social Hymenoptera: an inclusive fitness analysis. J. Evol. Biol. 16, 647–658. (doi:10.1046/j.1420-9101.2003.00574.x)
30. Schwander, T., Lo, N., Beekman, M., Oldroyd, B. P. & Keller, L. 2010 Nature versus nurture in social insect caste differentiation. Trends Ecol. Evol. 25, 275–282. (doi:10.1016/j.tree.2009.12.001)
31. Kronauer, D. J. C. 2009 Recent advances in army ant biology (Hymenoptera: Formicidae). Myrmecol. News 12, 51–65.
32. Boomsma, J. J., Kronauer, D. J. C. & Pedersen, J. S. 2009 The evolution of social insect mating systems. In Organization of insect societies: from genome to sociocomplexity (eds J. Gadau & J. Fewell), pp. 3–25. Cambridge, MA: Harvard University Press.
33. Schwander, T. & Keller, L. 2008 Genetic compatibility affects queen and worker caste determination. Science 322, 552. (doi:10.1126/science.1162590)
34. Tilley, C. A. & Oldroyd, B. P. 1997 Unequal subfamily proportions among honeybee queen and worker brood. Anim. Behav. 54, 1483–1490. (doi:10.1006/anbe.1997. 0546)
35. Osborne, K. E. & Oldroyd, B. P. 1999 Possible causes of reproductive dominance during emergency queen rearing by honeybees. Anim. Behav. 58, 267–272. (doi:10.1006/ anbe.1999.1139)
36. Châline, N., Arnold, G., Papin, C. & Ratnieks, F. L. W. 2003 Patriline differences in emergency queen rearing in the honey bee, Apis mellifera. Insect Soc. 50, 234–236. (doi:10.1007/s00040-003-0664-6)
37. Moritz, R., Lattorff, H., Neumann, P., Kraus, F., Radloff, S. & Hepburn, H. 2005 Rare royal families in honeybees, Apis mellifera. Naturwissenschaften 92, 488–491. (doi:10.1007/s00114-005-0025-6)
38. Nanork, P., Low, P. A., Proft, K. M., Lim, J., Deowanish, S., Wongsiri, S. & Oldroyd, B. P. 2011 Actual reproductive conflict during emergency queen rearing in Apis florea. Apidologie 42, 206–210. (doi:10.1051/apido/ 2010052)
39. Hughes, W. O. H. & Boomsma, J. J. 2008 Genetic royal cheats in leaf-cutting ant societies. Proc. Natl Acad. Sci. USA 105, 5150–5153. (doi:10.1073/pnas.0710262105)
40. Julian, G. E., Fewell, J. H., Gadau, J., Johnson, R. A. & Larrabee, D. 2002 Genetic determination of the queen caste in an ant hybrid zone. Proc. Natl Acad. Sci. USA 99, 8157–8160. (doi:10.1073/pnas.112222099)
41. Rice, W. R. & Chippindale, A. K. 2001 Intersexual ontogenetic conflict. J. Evol. Biol. 14, 685–693. (doi:10.1046/ j.1420-9101.2001.00319.x)
42. Bonduriansky, R. & Chenoweth, S. F. 2009 Intralocus sexual conflict. Trends Ecol. Evol. 24, 280–288. (doi:10. 1016/j.tree.2008.12.005)
43. Reuter, M. & Keller, L. 2001 Sex ratio conflict and worker production in eusocial Hymenoptera. Am. Nat. 158, 166–177. (doi:10.1086/321311)
44. Ohtsuki, H. & Tsuji, K. 2009 Adaptive reproduction schedule as a cause of worker policing in social Hymenoptera: a dynamic game analysis. Am. Nat. 173, 747–758. (doi:10.1086/598488)
45. Kucharski, R., Maleszka, J., Foret, S. & Maleszka, R. 2008 Nutritional control of reproductive status in honeybees via DNA methylation. Science 319, 1827–1830. (doi:10.1126/science.1153069)
46. Elango, N., Hunt, B. G., Goodisman, M. A. D. & Yi, S. V. 2009 DNA methylation is widespread and associated with differential gene expression in castes of the honeybee, Apis mellifera. Proc. Natl Acad. Sci. USA 106, 11 206–11 211. (doi:10.1073/pnas.0900301106)