Evolution of novel mosaic castes in ants: Modularity, phenotypic plasticity, and colonial buffering

American Naturalist

Volumn 180, Issue 3, 2012, Pages 328-341

  Molet, Mathieu ^a   Wheeler, Diana E ^b   Peeters, Christian ^a  

^a CNRS   (France)

^b UNIVERSITY OF ARIZONA   (United States)

Author keywords

Caste; Development; Ergatoid queen; Intercaste; Polyphenism; Soldier

Indexed keywords

ANT; BIOLOGICAL DEVELOPMENT; CASTE; CONCEPTUAL FRAMEWORK; EVOLUTIONARY BIOLOGY; MORPHOLOGY; PHENOTYPIC PLASTICITY;

ANIMAL; ANT; ARTICLE; BIOLOGICAL MODEL; EVOLUTION; FEMALE; GENETIC SELECTION; GENETICS; HISTOLOGY; MOSAICISM; PHENOTYPE; SOCIAL BEHAVIOR;

ANIMALS; ANTS; BIOLOGICAL EVOLUTION; FEMALE; MODELS, GENETIC; MOSAICISM; PHENOTYPE; SELECTION, GENETIC; SOCIAL BEHAVIOR;

FORMICIDAE;

EID: 84864654520     PISSN: 00030147     EISSN: None     Source Type: Journal    
DOI: 10.1086/667368     Document Type: Article

References (101)

1. Abouheif, E., and G. A. Wray. 2002. Evolution of the gene network underlying wing polyphenism in ants. Science 297:249-252.
2. Anderson, K. E., T. A. Linksvayer, and C. R. Smith. 2008. The causes and consequences of genetic caste determination in ants (Hymenoptera: Formicidae). Myrmecological News 11:119-132.
3. Baroni Urbani, C., and L. Passera. 1996. Origin of ant soldiers. Nature 383:223.
4. Beldade, P., A. R. A. Mateus, and R. A. Keller. 2011. Evolution and molecular mechanisms of adaptive developmental plasticity. Molecular Ecology 20:1347-1363.
5. Berger, D., S. S. Bauerfeind, W. U. Blanckenhorn, and M. A. Schaefer. 2011. High temperatures reveal cryptic genetic variation in a polymorphic female sperm storage organ. Evolution 65:2830-2842.
6. Berndt, K.-P., and G. Kremer. 1982. Heat shock-induced gynandromorphism in the pharaoh's ant, Monomorium pharaonis (L.). Cellular and Molecular Life Sciences 38:798-799.
7. Billick, I., and C. Carter. 2007. Testing the importance of the distribution of worker sizes to colony performance in the ant species Formica obscuripes Forel. Insectes Sociaux 54:113-117.
8. Bolton, B. 1986. Apterous females and shift of dispersal strategy in the Monomorium salomonis-group (Hymenoptera: Formicidae). Journal of Natural History 20:267-272.
9. Bolton, B. 1994. Identification guide to the ant genera of the world. Harvard University Press, Cambridge, MA.
10. Bolton, B., and A. C. Marsh. 1989. The Afrotropical thermophilic ant genus Ocymyrmex (Hymenoptera: Formicidae). Journal of Natural History 23:1267-1308.
11. Bourke, A. F. G. 1988. Dominance orders, worker reproduction, and queen-worker conflict in the slave-making ant Harpagoxenus sublaevis. Behavioral Ecology and Sociobiology 23:323-333.
12. Brian, M. V. 1955. Studies of caste differentiation in "Myrmica rubra" L. 2. The growth of workers and intercastes. Insectes Sociaux 2: 1-23.
13. Buschinger, A., and T. M. Alloway. 1978. Caste polymorphism in Harpagoxenus canadensis M. R. Smith (Hym., Formicidae). Insectes Sociaux 25:339-350.
14. Buschinger, A., and M. Schreiber. 2002. Queen polymorphism and queen-morph related facultative polygyny in the ant, Myrmecina graminicola (Hymenoptera, Formicidae). Insectes Sociaux 49:344-353.
15. Buschinger, A., and U. Winter. 1975. Der Polymorphismus der sklavenhaltenden Ameise Harpagoxenus sublaevis (Nyl.). Insectes Sociaux 22:333-362.
16. Carroll, S. B., J. K. Grenier, and S. D. Weatherbee. 2001. From DNA to diversity: molecular genetics and the evolution of animal design. Blackwell, Oxford.
17. Csõsz, S., and G. Majoros. 2009. Ontogenetic origin of mermithogenic Myrmica phenotypes (Hymenoptera, Formicidae). Insectes Sociaux 56:70-76.
18. Dietrich, M. R. 2003. Richard Goldschmidt: hopeful monsters and other "heresies. " Nature Reviews Genetics 4:68-74.
19. Dornhaus, A., and S. Powell. 2010. Foraging and defence strategies. Pages 210-230 in L. Lach, C. Parr, and K. Abbott, eds. Ant ecology. Oxford University Press, New York.
20. DuBois, M. B. 1986. A revision of the native New World species of the ant genus Monomorium (minimum group) (Hymenoptera: Formicidae). University of Kansas Science Bulletin 53:65-119.
21. Düssmann, O., C. Peeters, and B. Hölldobler. 1996. Morphology and reproductive behaviour of intercastes in the ponerine ant Pachycondyla obscuricornis. Insectes Sociaux 43:421-425.
22. Epper, F. 1983. The evagination of the genital imaginal discs of Drosophila melanogaster. Roux's Archives of Developmental Biology 192:275-279.
23. Fersch, R., A. Buschinger, and J. Heinze. 2000. Queen polymorphism in the Australian ant Monomorium sp. 10. Insectes Sociaux 47: 280-284.
24. Gerhart, J., and M. Kirschner. 1997. Cells, embryos, and evolution: toward a cellular and developmental understanding of phenotypic variation and evolutionary adaptability. Wiley, Malden, MA.
25. Gobin, B., and F. Ito. 2000. Queens and major workers of Acanthomyrmex ferox redistribute nutrients with trophic eggs. Naturwissenschaften 87:323-326.
26. Gobin, B., F. Ito, C. Peeters, and J. Billen. 2006. Queen-worker differences in sperm reservoir of phylogenetically basal ants. Cell and Tissue Research 326:169-178.
27. Gotwald, W. H., Jr. 1995. Army ants: the biology of social predation. Cornell series in arthropod biology. Cornell University Press, Ithaca, NY.
28. Hall, D. W., and I. C. Smith. 1953. Atypical forms of the wingless worker and the winged female in Monomorium pharaonis (L.) (Hymenoptera: Formicidae). Evolution 7:127-135.
29. Hasegawa, E. 1993a. Caste specialization in food storage in the dimorphic ant Colobopsis nipponicus (Wheeler). Insectes Sociaux 40: 261-271.
30. Hasegawa, E. 1993b. Nest defense and early production of the major workers in the dimorphic ant Colobopsis nipponicus (Wheeler) (Hymenoptera: Formicidae). Behavioral Ecology and Sociobiology 33: 73-77.
31. Heinze, J., and A. Buschinger. 1987. Queen polymorphism in a nonparasitic Leptothorax species (Hymenoptera, Formicidae). Insectes Sociaux 34:28-43.
32. Heinze, J., S. P. Cover, and B. Hölldobler. 1995. Neither worker, nor queen: an ant caste specialized in the production of unfertilized eggs. Psyche (Cambridge) 102:173-185.
33. Heinze, J., S. Foitzik, B. Oberstadt, O. Rüppell, and B. Hölldobler. 1999a. A female caste specialized for the production of unfertilized eggs in the ant Crematogaster smithi. Naturwissenschaften 86:93-95.
34. Heinze, J., B. Hölldobler, and G. Alpert. 1999b. Reproductive conflict and division of labor in Eutetramorium mocquerysi, a myrmicine ant without morphologically distinct female reproductives. Ethology 105:701-717.
35. Heinze, J., A. Schrempf, B. Seifert, and A. Tinaut. 2002. Queen morphology and dispersal tactics in the ant, Cardiocondyla batesii. Insectes Sociaux 49:129-132.
36. Hölldobler, B., and E. O. Wilson. 1990. The ants. Harvard University Press, Cambridge, MA.
37. Huang, M. H., and D. E. Wheeler. 2011. Colony demographics of rare soldier-polymorphic worker caste systems in Pheidole ants. Insectes Sociaux 58:539-549.
38. Hurley, I., A. Pomiankowski, K. Fowler, and H. Smith. 2002. Fate map of the eye-antennal imaginal disc in the stalk-eyed fly Cyrtodiopsis dalmanni. Development Genes and Evolution 212:38-42.
39. Johnson, B. R., and T. A. Linksvayer. 2010. Deconstructing the superorganism: social physiology, ground plans, and sociogenomics. Quarterly Review of Biology 85:57-79.
40. Johnson, R. A. 2010. Independent colony founding by ergatoid queens in the ant genus Pogonomyrmex: queen foraging provides an alternative to dependent colony founding. Insectes Sociaux 57: 169-176.
41. Jones, S. R., and S. A. Phillips Jr. 1985. Gynandromorphism in the ant Pheidole dentata Mayr (Hymenoptera: Formicidae). Proceedings of the Entomological Society of Washington 87:583-586.
42. Klingenberg, C. P. 2008. Morphological integration and developmental modularity. Annual Review of Ecology, Evolution, and Systematics 39:115-132.
43. Koshikawa, S., T. Matsumoto, and T. Miura. 2004. Soldier-like intercastes in the rotten-wood termite Hodotermopsis sjostedti (Isoptera: Termopsidae). Zoological Science 21:583-588.
44. Krapp, H. G. 2009. Ocelli. Current Biology 19:R435-R437.
45. Kronauer, D. J. C. 2008. Recent advances in army ant biology (Hymenoptera: Formicidae). Myrmecological News 12:51-65.
46. Masel, J., and S. Siegal. 2009. Robustness: mechanisms and consequences. Trends in Genetics 25:395-403.
47. Mirth, C. K., and L. M. Riddiford. 2007. Size assessment and growth control: how adult size is determined in insects. Bioessays 29:344-355.
48. Miyazaki, S., T. Murakami, T. Kubo, N. Azuma, S. Higashi, and T. Miura. 2010. Ergatoid queen development in the ant Myrmecina nipponica: modular and heterochronic regulation of caste differentiation. Proceedings of the Royal Society B: Biological Sciences 277:1953-1961.
49. Moczek, A. P. 2003. The behavioral ecology of threshold evolution in a polyphenic beetle. Behavioral Ecology 14:841-854.
50. Moczek, A. P. 2007. Developmental capacitance, genetic accommodation, and adaptive evolution. Evolution and Development 9:299-305.
51. Moczek, A. P. 2008. On the origins of novelty in development and evolution. Bioessays 30:432-447.
52. Molet, M., B. L. Fisher, F. Ito, and C. Peeters. 2009. Shift from independent to dependent colony foundation and evolution of "multi-purpose" ergatoid queens in Mystrium ants (subfamilyAmblyoponinae). Biological Journal of the Linnean Society 98:198-207.
53. Molet, M., C. Peeters, and B. L. Fisher. 2007. Permanent loss of wings in queens of the ant Odontomachus coquereli from Madagascar. Insectes Sociaux 54:174-182.
54. Monnin, T., and C. Peeters. 2008. How many gamergates is an ant queen worth? Naturwissenschaften 95:109-116.
55. Morata, G. 2001. How Drosophila appendages develop. Nature Reviews Molecular Cell Biology 2:89-97.
56. Nijhout, H. F., and G. Davidowitz. 2003. Developmental perspectives on phenotypic plasticity, canalization, and fluctuating asymmetry. Pages 3-13 in M. Polak, ed. Developmental instability: causes and consequences. MIT Press, Cambridge, MA.
57. Nijhout, H. F., and Y. Suzuki. 2008. Environment and genetic accommodation. Biological Theory 3:204-212.
58. Ohkawara, K., F. Ito, and S. Higashi. 1993. Production and reproductive function of intercastes in Myrmecina graminicola nipponica colonies (Hymenoptera: Formicidae). Insectes Sociaux 40:1-10.
59. Ohkawara, K., M. Nakayama, A. Satoh, A. Trindl, and J. Heinze. 2006. Clonal reproduction and genetic caste differences in a queenpolymorphic ant, Vollenhovia emeryi. Biology Letters 2:359-363.
60. Passera, L. 1976. Origine des intercastes dans les sociétés de Pheidole pallidula (Nyl.) (Hymenoptera Formicidae) parasitées par Mermis sp. (Nematoda Mermithidae). Insectes Sociaux 23:559-575.
61. Peeters, C. 1991. Ergatoid queens and intercastes in ants: two distinct adult forms which look morphologically intermediate between workers and winged queens. Insectes Sociaux 38:1-15.
62. Peeters, C. 2012. Convergent evolution of wingless reproductives across all subfamilies of ants, and sporadic loss of winged queens (Hymenoptera: Formicidae). Myrmecological News 16:75-91.
63. Peeters, C., and R. H. Crozier. 1988. Caste and reproduction in ants: not all mated egg-layers are "queens. " Psyche (Cambridge) 95: 283-288.
64. Peeters, C., and M. Molet. 2010. Colonial reproduction and life histories. Pages 159-176 in L. Lach, C. Parr, and K. Abbott, eds. Ant ecology. Oxford University Press, New York.
65. Pfennig, D. W., M. A. Wund, E. C. Snell-Rood, T. Cruickshank, C. D. Schlichting, and A. P. Moczek. 2010. Phenotypic plasticity's impacts on diversification and speciation. Trends in Ecology & Evolution 25:459-467.
66. Pie, M. R., and J. F. A. Traniello. 2006. Morphological evolution in a hyperdiverse clade: the ant genus Pheidole. Journal of Zoology (London) 271:99-109.
67. Plateaux, L. 1970. Sur le polymorphisme social de la fourmi Leptothorax nylanderi (Förster). I. Morphologie et biologie comparées des castes. Annales des Sciences Naturelles, Zoologie et Biologie Animale 12:373-478.
68. Powell, S. 2008. Ecological specialization and the evolution of a specialized caste in Cephalotes ants. Functional Ecology 22:902-911.
69. Powell, S., and N. Franks. 2006. Ecology and the evolution of worker morphological diversity: a comparative analysis with Eciton army ants. Functional Ecology 20:1105-1114.
70. Prud'homme, B., C. Minervino, M. Hocine, J. D. Cande, A. Aouane, H. D. Dufour, V. A. Kassner, et al. 2011. Body plan innovation in treehoppers through the evolution of an extra wing-like appendage. Nature 473:83-86.
71. Raghavan, K. V., N. Gendre, and R. F. Stocker. 1996. Transplanted wing and leg imaginal discs in Drosophila melanogaster demonstrate interactions between epidermis and myoblasts in muscle formation. Development Genes and Evolution 206:46-53.
72. Rajakumar, R., D. San Mauro, M. B. Dijkstra, M. H. Huang, D. E. Wheeler, F. Hiou-Tim, A. Khila, et al. 2012. Ancestral developmental potential facilitates parallel evolution in ants. Science 335: 79-82.
73. Rieppel, O. 2005. Modules, kinds and homology. Journal of Experimental Zoology Molecular and Developmental Evolution 304:18-27.
74. Rissing, S. W. 1984. Replete caste production and allometry of workers in the honey ant, Myrmecocystus mexicanus Wesmael (Hymenoptera: Formicidae). Journal of the Kansas Entomological Society 57:347-350.
75. Rutherford, S. L. 2000. From genotype to phenotype: buffering mechanisms and the storage of genetic information. Bioessays 22:1095-1105.
76. Sameshima, S., T. Miura, and T. Matsumoto. 2004. Wing disc development during caste differentiation in the ant Pheidole megacephala (Hymenoptera: Formicidae). Evolution and Development 4:336-341.
77. Schlichting, C. D. 2008. Hidden reaction norms, cryptic genetic variation, and evolvability. Annals of the New York Academy of Sciences 1133:187-203.
78. Schlosser, G., and G. P. Wagner. 2004. Modularity in development and evolution. University of Chicago Press, Chicago.
79. Scriber, J. M., R. J. Mercader, H. Romack, and M. D. Deering. 2009. Not all bilateral gynandromorph butterflies are interspecific hybrids: new Papilio specimens from field populations. Journal of the Lepidopterists' Society 63:37-47.
80. Siegal, M. L., and A. Bergman. 2002. Waddington's canalization revisited: developmental stability and evolution. Proceedings of the National Academy of Sciences of the USA 99:10528-10532.
81. Suzuki, Y., and H. F. Nijhout. 2008. Constraint and developmental dissociation of phenotypic integration in a genetically accommodated trait. Evolution and Development 10:690-699.
82. Thorne, B. L., and J. F. Traniello. 2003. Comparative social biology of basal taxa of ants and termites. Annual Review of Entomology 48:283-306.
83. Tinaut, A., and F. Ruano. 1992. Braquipterismo y apterismo en formícidos. Morfología y biometría en las hembras de especies ibéricas de vida libre (Hymenoptera: Formicidae). Graellsia 48:121-131.
84. Tschinkel, W.R. 2006. The fire ants. Harvard University Press, Cambridge, MA.
85. Tsuji, K. 1990. Nutrient storage in the major workers of Pheidole ryukyuensis (Hymenoptera: Formicidae). Applied Entomology and Zoology 25:283-287.
86. Tsuji, K., T. Furukawa, K. Kinomura, H. Takamine, and K. Yamauchi. 1991. The caste system of the dolichoderine ant Technomyrmex albipes (Hymenoptera: Formicidae): morphological description of queens, workers and reproductively active intercastes. Insectes Sociaux 38:413-422.
87. Villet, M. 1990. Division of labor in the Matabele ant Megaponera foetens (Fabr.) (Hymenoptera Formicidae). Ethology, Ecology, and Evolution 2:397-417.
88. Von Dassow, G., and E. Munro. 1999. Modularity in animal development and evolution: elements of a conceptual framework for EvoDevo. Journal of Experimental Zoology 285:307-325.
89. Wagner, G. P. 1996. Homologues, natural kinds and the evolution of modularity. American Zoologist 36:36-43.
90. Ward, P. S. 1997. Ant soldiers are not modified queens. Nature 385: 494-495.
91. Ward, P. S. 2007. Phylogeny, classification, and species-level taxonomy of ants (Hymenoptera: Formicidae). Zootaxa 1668:549-563.
92. West-Eberhard, M. J. 2003. Developmental plasticity and evolution. Oxford University Press, New York.
93. Wheeler, D. E. 1991. The developmental basis of worker caste polymorphism in ants. American Naturalist 138:1218-1238.
94. Wheeler, D. E., and H. F. Nijhout. 1981. Imaginal wing discs in larvae of the soldier caste of Pheidole bicarinata vinelandica Forel (Hymenoptera: Formicidae). International Journal of Insect Morphology and Embryology 10:131-139.
95. Wheeler, W. M. 1905. Worker ants with vestiges of wings. Bulletin of the American Museum of Natural History 21:405-408.
96. Wheeler, W. M. 1910. Ants: their structure, development and behavior. Columbia University Press, New York.
97. Wheeler, W. M. 1928. Mermis parasitism and intercastes among ants. Journal of Experimental Zoology 50:165-237.
98. Wheeler, W. M. 1937. Mosaics and other anomalies among ants. Harvard University Press, Cambridge, MA.
99. Wilson, E. O. 2003. Pheidole in the New World: a dominant, hyperdiverse ant genus. Harvard University Press, Cambridge, MA.
100. Yang, A. S. 2001. Modularity, evolvability, and adaptive radiations: a comparison of the hemi-and holometabolous insects. Evolution and Development 3:59-72.
101. Yang, A. S., and E. Abouheif. 2011. Gynandromorphs as indicators of modularity and evolvability in ants. Journal of Experimental Zoology Molecular and Developmental Evolution 316:313-318.