Social parasitism and the molecular basis of phenotypic evolution

Frontiers in Genetics

Volumn 6, Issue FEB, 2015, Pages

  Cini, Alessandro ^a,f,g   Patalano, Solenn ^b,c   Segonds Pichon, Anne ^c   Busby, George B J ^b,d   Cervo, Rita ^a   Sumner, Seirian ^b,e  

^a UNIVERSITY OF FLORENCE   (Italy)

^b INSTITUTE OF ZOOLOGY   (United Kingdom)

^c BABRAHAM INSTITUTE   (United Kingdom)

^d UNIVERSITY OF OXFORD   (United Kingdom)

^e UNIVERSITY OF BRISTOL   (United Kingdom)

^f ISTITUTO NAZIONALE DELLA NUTRIZIONE   (Italy)

^g Centro Nazionale Biodiversità Forestale 'Bosco Fontana'   (Italy)

Author keywords

Gene expression; Genomics; Phenotypic plasticity; Polistes; Social insects; Social parasites

Indexed keywords

HEXAPODA; POLISTES; POLISTES SULCIFER; POLISTINAE; VERTEBRATA;

EID: 84927129572     PISSN: None     EISSN: 16648021     Source Type: Journal    
DOI: 10.3389/fgene.2015.00032     Document Type: Article

References (112)

1. Achenbach, A., and Foitzik, S. (2009). First evidence for slave rebellion: enslaved ant workers systematically kill the brood of their social parasite Protomognathus americanus. Evolution 63, 1068-1075. doi: 10.1111/j.1558-5646.2009.00591.x
2. Alford, D. V. (1975). Bumblebees. London: Davis Poynter.
3. Arendt, J., and Reznick, D. (2008). Convergence and parallelism reconsidered: what have we learned about the genetics of adaptation? Trends Ecol. Evol. 23, 26-32. doi: 10.1016/j.tree.2007.09.011
4. Aubin-Horth, N., and Renn, S. C. P. (2009). Genomic reaction norms: using integrative biology to understand molecular mechanisms of phenotypic plasticity. Mol. Ecol. 18, 3763-3780. doi: 10.1111/j.1365-294X.2009.04313.x
5. Baba, R., Nagata, Y., and Yamagishi, S. (1990). Brood parasitism and egg robbing among three freshwater fish. Anim. Behav. 40, 776-778. doi: 10.1016/S0003-3472(05)80707-9
6. Bagnères, A. G., and Lorenzi, M. C. (2010). "Chemical deception/mimicry using cuticular hydrocarbons, "in Insect Hydrocarbons: Biology, Biochemistry and Chemical Ecology, eds G. J. Blomquist and A.-G. Bagnères (Cambridge, MA: Cambridge University Press), 282-324.
7. Begna, D., Han, B., Feng, M., Fang, Y., and Li, J. (2012). Differential expressions of nuclear proteomes between honeybee (Apis mellifera L.) Queen and worker larvae: a deep insight into caste pathway decisions. J. Proteome Res. 11, 1317-1329. doi: 10.1021/pr200974a
8. Beldade, P., Mateus, A. R. A., and Keller, R. A. (2011). Evolution and molecular mechanisms of adaptive developmental plasticity. Mol. Ecol. 20, 1347-1363. doi: 10.1111/j.1365-294X.2011.05016.x
9. Bonasio, R., Li, Q., Lian, J., Mutti, N. S., Jin, L., Zhao, H., et al. (2012). Genome-wide and caste-specific DNA methylomes of the Ants Camponotus floridanus and Harpegnathos saltator. Curr. Biol. 22, 1-10. doi: 10.1016/j.cub.2012.07.042
10. Brisson, J. A., and Stern, D. L. (2006). The pea aphid, Acyrthosiphon pisum: an emerging genomic model system for ecological, developmental and evolutionary studies. Bioessays 28, 747-755. doi: 10.1002/bies.20436
11. Bruschini, C., Cervo, R., and Turillazzi, S. (2010). Pheromones in social wasps. Vit. Horm. Phero 83, 447-492. doi: 10.1016/S0083-6729(10)83019-5
12. Burton, J., Bogitsh, C. E. C., and Oeltmann, T. N. (2012). Human Parasitology. Academic Press.
13. Buschinger, A. (2009). Social parasitism among ants: a review (Hymenoptera: Formicidae). Myrmec. News 12, 219-235.
14. Cameron, S. A., Hines, H. M., and Williams, P. H. (2007). A comprehensive phylogeny of the bumble bees (Bombus). Biol. J. Linnean Soc. 91, 161-188. doi: 10.1111/j.1095-8312.2007.00784.x
15. Carpenter, J. M., and Perera, E. P. (2006). Phylogenetic relationships among yellowjackets and the evolution of social parasitism (Hymenoptera: Vespidae, Vespinae). Am. Mus. Novit. 3507, 1-19. doi: 10.1206/0003-0082(2006)3507[1:PRAYAT]2.0.CO;2
16. Cervo, R. (1994). Morphological adaptations to the parasitic life in Polistes sulcifer and P. atrimandibularis (Hymenoptera Vespidae). Ethol. Ecol. Evol. 6, 61-66. doi: 10.1080/03949370.1994.10721975
17. Cervo, R. (2006). Polistes wasps and their social parasites: an overview. Ann. Zool. Fenn 43, 531-549.
18. Cervo, R., Bertocci, F., and Turillazzi, S. (1996). Olfactory cues in host nest detection by the social parasite Polistes sulcifer (Hymenoptera, Vespidae). Behav. Processes 36, 213-218. doi: 10.1016/0376-6357(95)00030-5
19. Cervo, R., and Dani, F. R. (1996). "Social parasitism and its evolution in Polistes, "in Natural History and Evolution of Paper-Wasps, eds S. Turillazzi and M. J. West-Eberhard (New York, NY: Oxford University Press), 98-112.
20. Cervo, R., and Lorenzi, M. C. (1996). Inhibition of host queen reproductive capacity by the obligate social parasite Polistes atrimandibularis (Hymenoptera, Vespidae). Ethology 102, 1042-1047. doi: 10.1111/j.1439-0310.1996.tb01180.x
21. Cervo, R., Lorenzi, M. C., and Turillazzi, S. (1990). Different strategies of host nest invasion in two species of Sulcopolistes (Hymenoptera, Vespidae). Ethol. Ecol. Evol. 3, 302-303 doi: 10.1080/08927014.1990.9525432
22. Cervo, R., and Turillazzi, S. (1996). Host nest preference and nest choice in the cuckoo paper wasp Polistes sulcifer (Hymenoptera: Vespidae). J. Insect Behav. 9, 297-306. doi: 10.1007/BF02213872
23. Chen, S., Krinsky, B. H., and Long, M. (2013). New genes as drivers of phenotypic evolution. Nat. Rev. Genet. 14, 645-660. doi: 10.1038/nrg3521
24. Choudhary, M., Strassmann, J. E., Queller, D. C., Turillazzi, S., and Cervo, R. (1994). Social parasites in Polistine wasps are monophyletic: implications for sympatric speciation. Proc. R. Soc. Lond. B 257, 31-35. doi: 10.1098/rspb.1994.0090
25. Cini, A., Bruschini, C., Poggi, L., and Cervo, R. (2011b). Fight or fool? physical strength, instead of sensory deception, matters in host nest invasion by a wasp social parasite. Anim. Behav. 81, 1139-1145. doi: 10.1016/j.anbehav.2011.02.017
26. Cini, A., Bruschini, C., Signorotti, L., Pontieri, L., Turillazzi, S., and Cervo, R. (2011a). The chemical basis of host nest detection and chemical integration in a cuckoo paper wasp. J. Exp. Biol. 214, 3698-3703. doi: 10.1242/jeb.059519
27. Cini, A., and Dapporto, L. (2009). Autumnal helpers of Polistes dominulus represent a distinct behavioural phenotype. Ann. Zool. Fenn. 46, 423-430. doi: 10.5735/086.046.0603
28. Cini, A., Nieri, R., Dapporto, L., Monnin, T., and Cervo, R. (2014). Almost royal: incomplete suppression of host worker ovarian development by a social parasite wasp. Behav. Ecol. Sociobiol. 68, 467-475. doi: 10.1007/s00265-013-1661-z
29. Dapporto, L., Cervo, R., Sledge, M. F., and Turillazzi, S. (2004). Rank integration in dominance hierarchies of host colonies by the paper wasp social parasite Polistes sulcifer (Hymenoptera, Vespidae). J. Insect Physiol. 50, 217-223. doi: 10.1016/j.jinsphys.2003.11.012
30. Dapporto, L., and Palagi, E. (2006). Wasps in the shadow: looking at the pre-hibernating clusters of Polistes dominulus. Ann. Zool. Fenn. 43, 583-594.
31. Daugherty, T. H. F., Toth, A. L., and Robinson, G. E. (2011). Nutrition and division of labor: effects on foraging and brain gene expression in the paper wasp Polistes metricus. Mol. Ecol. 20, 5337-5347. doi: 10.1111/j.1365-294X.2011.05344.x
32. Davies, N. B. (2000). Cuckoos, Cowbirds and Other Cheats. London: T. & A. D. Poyser.
33. Dawkins, R. (1982). The Extended Phenotype. Oxford: Oxford University Press.
34. De Visser, J. A. G. M., and Krug, J. (2014). Empirical fitness landscapes and the predictability of evolution. Nat. Rev. Genetics 15, 480-490. doi: 10.1038/nrg3744
35. Dybdahl, M. F., Jenkins, C. E., and Nuismer, S. L. (2014). Identifying the molecular basis of host-parasite coevolution: merging models and mechanisms. Am. Nat. 184, 1-13. doi: 10.1086/676591
36. Evans, J. D., and Wheeler, D. E. (2001). Gene expression and the evolution of insect polyphenisms. Bioessays 23, 62-68. doi: 10.1002/1521-1878(200101)23:1>62::AID-BIES1008<3.3.CO;2-Z
37. Ezkurdia, I., Juan, D., Rodriguez, J. M., Frankish, A., Diekhans, M., Harrow, J., et al. (2014). Multiple evidence strands suggest that there may be as few as 19 000 human protein-coding genes. Hum. Mol. Genet. 23, 5866-5878. doi: 10.1093/hmg/ddu309
38. Feldmeyer, B., Elsner, D., and Foitzik, S. (2014). Gene expression patterns associated with caste and reproductive status in ants: worker-specific genes are more derived than queen-specific ones. Mol. Ecol. 23, 151-161. doi: 10.1111/mec.12490
39. Fernald, R. D. (2004). Evolving eyes. Intern. J. Dev. Biol. 48, 701-705. doi: 10.1387/ijdb.041888rf
40. Ferreira, P. G., Patalano, S., Chauhan, R., Ffrench-Constant, R., Gabaldón, T., Guigó, R., et al. (2013). Transcriptome analyses of primitively eusocial wasps reveal novel insights into. the evolution of sociality and the origin of alternative phenotypes. Genome Biol. 14:R20. doi: 10.1186/gb-2013-14-2-r20
41. Fiedler, K. (2006). Ant-associates of Palaearctic lycaenid butterfly larvae (Hymenoptera: Formicidae; Lepidoptera: Lycaenidae)-a review. Myrmec. Nachrichten 9, 77-87.
42. Fischman, B. J., Woodard, S. H., and Robinson, G. E. (2011). Molecular evolutionary analyses of insect societies. Proc. Natl. Acad. Sci. 108 10847-10854. doi: 10.1073/pnas.1100301108
43. Fusco, G., and Minelli, A. (2010). Phenotypic plasticity in development and evolution: facts and concepts. Introduction. Phil. Trans. R. Soc. London B 365, 547-556. doi: 10.1098/rstb.2009.0267
44. Gibbs, J., Albert, J., and Packer, L. (2012). Dual origins of social parasitism in North American Dialictus (Hymenoptera: Halictidae) confirmed using a phylogenetic approach. Cladistics 28, 195-207. doi: 10.1111/j.1096-0031.2011.00373.x
45. Greenberg, J. K., Xia, J., Zhou, X., Thatcher, S. R., Gu, X., Ament, S. A., et al. (2012). Behavioral plasticity in honey bees is associated with differences in brain microRNA transcriptome. Genes Brain Behav. 11, 660-670. doi: 10.1111/j.1601-183X.2012.00782.x
46. Hamilton, W. D. (1980). Sex versus non-sex versus parasite. Oikos 35, 282-290. doi: 10.2307/3544435
47. Harpur, B. A., Kent, C. F., Molodtsova, D., Lebon, J. M., Alqarni, A. S., Owayss, A. A., et al. (2014). Population genomics of the honey bee reveals strong signatures of positive selection on worker traits. Proc. Natl Acad. Sci. U.S.A. 111, 2614-2619. doi: 10.1073/pnas.1315506111
48. Hines, H. M., and Cameron, S. A. (2010). The phylogenetic position of the bumble bee inquiline Bombus inexspectatus and implications for the evolution of social parasitism. Insectes Soc. 57, 379-383. doi: 10.1007/s00040-010-0094-1
49. Huang, M. H., and Dornhaus, A. (2008). A meta-analysis of ant social parasitism: host characteristics of different parasitism types and a test of Emery's rule. Ecol. Entomol. 33, 589-596. doi: 10.1111/j.1365-2311.2008.01005.x
50. Hughes, A. L. (2012). Evolution of adaptive phenotypic traits without positive Darwinian selection. Heredity 108, 347-353. doi: 10.1038/hdy.2011.97
51. Hunt, B. G., Ometto, L., Wurm, Y., Shoemaker, D., Soojin, V. Y., Keller, L., et al. (2011). Relaxed selection is a precursor to the evolution of phenotypic plasticity. Proc. Natl Acad. Sci. U.S.A. 108, 15936-15941. doi: 10.1073/pnas.1104825108
52. Hunt, G., and Carrano, M. T. (2010). "Models and methods for analyzing phenotypic evolution in lineages and clades, "in Quantitative Methods in Paleobiology, eds J. Alroy and G. Hunt (Boulder, CO: The Paleontological Society), 245-269.
53. Jeanne, R. L. (1977). Behavior of the obligate social parasite Vespula arctica (Hymenoptera: Vespidae). J. Kansas Ent. Soc. 50, 541-557.
54. Johnson, B. R., and Tsutsui, N. D. (2011). Taxonomically restricted genes are associated with the evolution of sociality in the honey bee. BMC Genomics 12:164. doi: 10.1186/1471-2164-12-164
55. Kaessmann, H. (2010). Origins, evolution, and phenotypic impact of new genes. Genome Res. 20, 1313-1326. doi: 10.1101/gr.101386.109
56. Kang, L., Chen, X., Zhou, Y., Liu, B., Zheng, W., Li, R., et al. (2004). The analysis of large-scale gene expression correlated to the phase changes of the migratory locust. Proc. Natl. Acad. Sci. U.S.A. 101, 17611-17615. doi: 10.1073/pnas.0407753101
57. Khalturin, K., Anton-Erxleben, F., Sassmann, S., Wittlieb, J., Hemmrich, G., and Bosch, T. C. (2008). A novel gene family controls species-specific morphological traits in Hydra. PLoS Biol. 6:e278. doi: 10.1371/journal.pbio.0060278
58. Kucharski, R., Maleszka, J., Foret, S., and Maleszka, R. (2008). Nutritional control of reproductive status in honeybees via DNA methylation. Science 319, 1827-1830. doi: 10.1126/science.1153069
59. Lee, P. N., Callaerts, P., and Couet, H. G., De (2003). Cephalopod Hox genes and the origin of morphological novelties. Nature 424, 1061-1065. doi: 10.1038/nature01872
60. Lenoir, A., d'Ettorre, P., Errard, C., and Hefetz, A. (2001). Chemical ecology and social parasitism in ants. Ann. Rev. Entomol. 46, 573-599. doi: 10.1146/annurev.ento.46.1.573
61. Looso, M., Preussner, J., Sousounis, K., Bruckskotten, M., Michel, C. S., Lignelli, E., et al. (2013). A de novo assembly of the newt transcriptome combined with proteomic validation identifies new protein families expressed during tissue regeneration. Genome Biol., 14:R16. doi: 10.1186/gb-2013-14-2-r16
62. Lowe, R. M., Ward, S. A., and Crozier, R. H. (2002). The evolution of parasites from their hosts: intra-and interspecific parasitism and Emery's rule. Proc. R. Soc. Lond. B 269, 1301-1305. doi: 10.1098/rspb.2002.2008
63. Lyko, F., Foret, S., Kucharski, R., Wolf, S., Falckenhayn, C., and Maleszka, R. (2010). The honey bee epigenomes: differential methylation of brain DNA in queens and workers. PLoS Biol. 8:e1000506. doi: 10.1371/journal.pbio.1000506
64. Michener, C. D. (1970). Social parasites among African allodapine bees. Zool. J. Linn. Soc. 49, 199-215. doi: 10.1111/j.1096-3642.1970.tb00736.x
65. Moczek, A. P. (2009). "Developmental plasticity and the origins of diversity: a case study on horned beetles, "in Phenotypic Plasticity in Insects: Mechanisms and Consequences, eds T. N. Ananthakrishnan and D. Whitman (Plymouth: Science Publishers), 81-134.
66. Moczek, A. P. (2010). Phenotypic plasticity and diversity in insects. Phil. Trans. R. Soc. London B 365, 593-603. doi: 10.1098/rstb.2009.0263
67. Nachtomy, O., Shavit, A., and Yakhini, Z. (2007). Gene expression and the concept of the phenotype. Stud. Hist. Phil. Biol. Biomed. Sci. 38, 238-254. doi: 10.1016/j.shpsc.2006.12.014
68. Nijhout, H. F. (2003). Development and evolution of adaptive polyphenisms. Evol. Dev. 5, 9-18. doi: 10.1046/j.1525-142X.2003.03003.x
69. Ortolani, I., Turillazzi, S., and Cervo, R. (2008). Spring usurpation restlessness: a wasp social parasite adapts its seasonal activity to the host cycle. Ethology 114, 782-788. doi: 10.1111/j.1439-0310.2008.01525.x
70. Page, R. E., and Amdam, G. V. (2007). The making of a social insect: developmental architectures of social design. Bioessays 29, 334-343. doi: 10.1002/bies.20549
71. Pardi, L. (1946). La 'Dominazione'e il ciclo ovario annuale in polistes gallicus (L.). Ricerche sui Polistini VII. Boll. Ist. Entom. 25-84.
72. Pardi, L. (1996). "Polistes: analysis of a society, "in Natural History and Evolution of Paper-Wasps, eds S. Turillazzi and M. J. West-Eberhard (New York, NY: Oxford University Press), 98-112.
73. Patalano, S., Hore, T. A., Reik, W., and Sumner, S. (2012). Shifting behaviour: epigenetic reprogramming in eusocial insects. Curr. Opin. Cell Biol. 24, 367-373. doi: 10.1016/j.ceb.2012.02.005
74. Pavey, S. A., Collin, H., Nosil, P., and Rogers, S. M. (2010). The role of gene expression in ecological speciation. Ann. NY Acad. Sci. 1206, 110-129. doi: 10.1111/j.1749-6632.2010.05765.x
75. Pfennig, D. W., Wund, M. A., Snell-Rood, E. C., Cruickshank, T., Schlichting, C. D., and Moczek, A. P. (2010). Phenotypic plasticity's impacts on diversification and speciation. Trends Ecol. Evol. 25, 459-467. doi: 10.1016/j.tree.2010.05.006
76. Riddell, C. E., Sumner, S., Adams, S., and Mallon, E. B. (2011). Pathways to immunity: temporal dynamics of the bumblebee (Bombus terrestris) immune response against a trypanosomal gut parasite. Insect Molec. Biol. 20, 529-540. doi: 10.1111/j.1365-2583.2011.01084.x
77. Savolainen, R., and Vepsäläinen, K. (2003). Sympatric speciation through intraspecific social parasitism. Proc. Natl. Acad. Sci. U.S.A. 100, 7169-7174. doi: 10.1073/pnas.1036825100
78. Schlichting, C. D., and Wund, M. A. (2014). Phenotypic plasticity and epigenetic marking: an assessment of evidence for genetic accommodation. Evolution 68, 656-672. doi: 10.1111/evo.12348
79. Schwander, T., and Leimar, O. (2011). Genes as leaders and followers in evolution. Trends Ecol. Evol. 26, 143-151. doi: 10.1016/j.tree.2010.12.010
80. Shubin, N., Tabin, C., and Carroll, S. (2009). Deep homology and the origins of evolutionary novelty. Nature 457, 818-823. doi: 10.1038/nature07891
81. Simola, D. F., Wissler, L., Donahue, G., Waterhouse, R. M., Helmkampf, M., Roux, J., et al. (2013). Social insect genomes exhibit dramatic evolution in gene composition and regulation while preserving regulatory features linked to sociality. Genome Res. 23, 1235-1247. doi: 10.1101/gr.155408.113
82. Simpson, S. J., Sword, G. A., and Lo, N. (2011). Polyphenism in insects. Curr. Biol. 21, R738-R749. doi: 10.1016/j.cub.2011.06.006
83. Sledge, M. F., Dani, F. R., Cervo, R., Dapporto, L., and Turillazzi, S. (2001). Recognition of social parasites as nest-mates: adoption of colony-specific host cuticular odours by the paper wasp parasite Polistes sulcifer. Proc. R. Soc. Lond. B 268, 2253-2260. doi: 10.1098/rspb.2001.1799
84. Smith, C. R., Toth, A. L., Suarez, A. V., and Robinson, G. E. (2008). Genetic and genomic analyses of the division of labour in insect societies. Nat. Rev. Genet. 9, 735-748. doi: 10.1038/nrg2429
85. Smith, J. A., Chenoweth, L. B., Tierney, S. M., and Schwarz, M. P. (2013). Repeated origins of social parasitism in allodapine bees indicate that the weak form of Emery's rule is widespread, yet sympatric speciation remains highly problematic. Biol. J, Linn. Soc. 109, 320-331. doi: 10.1111/bij.12043
86. Stern, D. L. (2013). The genetic causes of convergent evolution. Nat. Rev. Genet. 14, 751-764. doi: 10.1038/nrg3483
87. Sumner, S. (2006). Determining the molecular basis of sociality in insects: progress, prospects and potential in sociogenomics. Ann. Zool. Fenn. 43, 423-442.
88. Sumner, S. (2014). The importance of genomic novelty in social evolution. Mol. Ecol. 23, 26-28. doi: 10.1111/mec.12580
89. Sumner, S., Aanen, D. K., Delabie, J., and Boomsma, J. J. (2004a). The evolution of social parasitism in Acromyrmex leaf-cutting ants: a test of Emery's rule. Insectes Soc. 51, 37-42. doi: 10.1007/s00040-003-0723-z
90. Sumner, S., Hughes, W. O., Pedersen, J. S., and Boomsma, J. J. (2004b). Ant parasite queens revert to mating singly. Nature 428, 35-36. doi: 10.1038/428035a
91. Sumner, S., Pereboom, J. J., and Jordan, W. C. (2006). Differential gene expression and phenotypic plasticity in behavioural castes of the primitively eusocial wasp, Polistes canadensis. Proc. R. Soc. Lond. B 273, 19-26. doi: 10.1098/rspb.2005.3291
92. Tautz, D., Ellegren, H., and Weigel, D. (2010). Next generation molecular ecology. Mol. Ecol. 19, 1-3. doi: 10.1111/j.1365-294X.2009.04489.x
93. Tierney, S. M., Smith, J. A., Chenoweth, L., and Schwarz, M. P. (2008). Phylogenetics of allodapine bees: a review of social evolution, parasitism and biogeography. Apidologie 39, 3-15. doi: 10.1051/apido:2007045
94. Toth, A. L., Bilof, K. B. J., Henshaw, M. T., Hunt, J. H., and Robinson, G. E. (2009). Lipid stores, ovary development, and brain gene expression in Polistes metricus females. Insectes Soc. 56, 77-84. doi: 10.1007/s00040-008-1041-2
95. Toth, A. L., and Robinson, G. E. (2007). Evo-devo and the evolution of social behavior. Trends Genet. 23, 334-341. doi: 10.1016/j.tig.2007.05.001
96. Toth, A. L., Tooker, J. F., and Radhakrishnan, S. (2014). Shared genes related to aggression, rather than chemical communication, are associated with reproductive dominance in paper wasps (Polistes metricus). BMC Genomics 15:75. doi: 10.1186/1471-2164-15-75
97. Toth, A. L., Varala, K., Henshaw, M. T., Rodriguez-Zas, S. L., Hudson, M. E., and Robinson, G. E. (2010). Brain transcriptomic analysis in paper wasps identifies genes associated with behaviour across social insect lineages. Proc. R. Soc. Lond. B 277, 2139-2148. doi: 10.1098/rspb.2010.0090
98. Toth, A. L., Varala, K., Newman, T. C., Miguez, F. E., Hutchison, S. K., Willoughby, D. A., et al. (2007). Wasp gene expression supports an evolutionary link between maternal behavior and eusociality. Science 318, 441-444. doi: 10.1126/science.1146647
99. Turillazzi, S., Cervo, R., and Cavallari, I. (1990). Invasion of thenest of Polistes dominulus by the social parasite Sulcopolistes sulcifer (Hymenoptera, Vespidae). Ethology 84, 47-59. doi: 10.1111/j.1439-0310.1990.tb00784.x
100. Turillazzi, S., Sledge, M. F., Dani, F. R., Cervo, R., Massolo, A., and Fondelli, L. (2000). Social hackers: integration in the host chemical recognition system by a paper wasp social parasite. Naturwissen 87, 172-176. doi: 10.1007/s001140050697
101. Valcu, C. M., and Kempenaers, B. (2014). Proteomics in behavioral ecology. Behav. Ecol. 26, 1-15. doi: 10.1093/beheco/aru096
102. Van Dyken, J. D., and Wade, M. J. (2010). The genetic signature of conditional expression. Genetics 184, 557-570. doi: 10.1534/genetics.109.110163
103. Vergara, C. H., Schroder, S., Almanza, M. T., and Wittmann, D. (2003). Suppression of ovarian development of Bombus terrestris workers by B. terrestris queens, Psithyrus vestalis and Psithyrus bohemicus females. Apidol 34, 563-568. doi: 10.1051/apido:2003056
104. Waddington, C. H. (1942). Canalization of development and the inheritance of acquired characters. Nature 150, 563-565. doi: 10.1038/150563a0
105. Werren, J. H., Richards, S., Desjardins, C. A., Niehuis, O., Gadau, J., and Colbourne, J. K. (2010). Functional and evolutionary insights from the genomes of three parasitoid Nasonia species. Science 327, 343-348. doi: 10.1126/science.1178028
106. West-Eberhard, M. J. (1989). Phenotypic plasticity and the origins of diversity. Annu. Rev Ecol. Syst. 249-278. doi: 10.1146/annurev.es.20.110189.001341
107. West-Eberhard, M. J. (2003). Developmental Plasticity and Evolution. New York, NY: Oxford University Press.
108. West-Eberhard, M. J. (2005). Developmental plasticity and the origin of species differences. Proc. Natl. Acad. Sci. U.S.A. 102 (Suppl.), 6543-6549. doi: 10.1073/pnas.0501844102
109. Wheeler, D. E. (1986). Developmental and physiological determinants of caste in social Hymenoptera: evolutionary implications. Am. Nat. 128, 13-34. doi: 10.1086/284536
110. Wissler, L., Gadau, J., Simola, D. F., Helmkampf, M., and Bornberg-Bauer, E. (2013). Mechanisms and dynamics of orphan gene emergence in insect genomes. Genome Biol. Evol. 5, 439-455. doi: 10.1093/gbe/evt009
111. Woodard, S. H., Fischman, B. J., Venkat, A., Hudson, M. E., Varala, K., Cameron, S. A., et al. (2011). Genes involved in convergent evolution of eusociality in bees. Proc. Natl. Acad. Sci. U.S.A. 108, 7472-7477. doi: 10.1073/pnas.1103457108
112. Yan, H., Simola, D. F., Bonasio, R., Liebig, J., Berger, S. L., and Reinberg, D. (2014). Eusocial insects as emerging models for behavioural epigenetics. Nat. Rev. Genet. 15, 677-688. doi: 10.1038/nrg3787