Genetic polyethism in the polyandrous desert ant Cataglyphis cursor

Behavioral Ecology

Volumn 24, Issue 1, 2013, Pages 144-151

  Eyer, Pierre André ^a   Freyer, Julien ^a   Aron, Serge ^a  

^a UNIVERSITÉ LIBRE DE BRUXELLES   (Belgium)

Author keywords

division of labor; genetic polyethism; polyandry; polymorphism; social insect

Indexed keywords

ANT; DESERT; GENETIC ANALYSIS; HYPOTHESIS TESTING; LABOR DIVISION; POLYANDRY; POLYETHISM; SOCIAL INSECT; SPECIALIZATION;

CATAGLYPHIS CURSOR; HEXAPODA; HYMENOPTERA;

EID: 84871256208     PISSN: 10452249     EISSN: 14657279     Source Type: Journal    
DOI: 10.1093/beheco/ars146     Document Type: Article

References (98)

1. Acock AC, Stavig GR. 1979. A measure of association for nonparametric statistics. Soc Forces. 57:1381-1386.
2. Alcock J, Barrows EM, Gordh G, Hubbard LJ, Kierkendall L, Pyle DW, Ponder TL, Zalom FG. 1978. The ecology and evolution of male reproductive behaviour in the bees and wasps. Zool J Linnean Soc. 64:293-326.
3. Arnqvist G, Nilsson T. 2000. The evolution of polyandry: multiple mating and female fitness in insects. Anim Behav. 60:145-164.
4. Baer B, Schmid-Hempel P. 1999. Experimental variation in polyandry affects parasite loads and fitness in a bumble-bee. Nature. 397:151-154.
5. Ballari S, Farji-Brener A, Tadey M. 2007. Waste management in the leafcutting ant Acromyrmex lobicornis: division of labour, aggressive behaviour, and location of external refuse dumps. J Insect Behav. 20:87-98.
6. Bargum K, Boomsma JJ, Sundström L. 2004. A genetic component to size in queens of the ant, Formica truncorum. Behav Ecol Sociobiol. 57:9-16.
7. Bertram SM, Gorelick R, Fewell JH. 2003. Colony response to graded resource changes: an analytical model of the influence of genotype, environment, and dominance. Theor Popul Biol. 64:151-162.
8. Beshers S, Fewell JH. 2001. Models of division of labor in social insects. Annu Rev Entomol. 46:413-440.
9. Blatrix R, Durand JL, Jaisson P. 2000. Task allocation depends on matriline in the ponerine ant Gnamptogenys striatula Mayr. J Insect Behav. 13:553-562.
10. Bonabeau E, Theraulaz G, Deneubourg JL. 1996. Quantitative study of the ?xed threshold model for the regulation of division of labour in insect societies. Proc R Soc London B Biol Sci. 263:1565-1569.
11. Bonabeau E, Théraulaz G, Deneubourg JL. 1998. Fixed response thresholds and the regulation of division of labor in insect societies. Bull Math Biol. 60:753-807.
12. Boomsma JJ, Kronauer D, Pedersen JD. 2009. The evolution of social insect mating systems. In: Gadau J, Fewell J, editors. Organization of insect societies-from genome to sociocomplexity. Cambridge (MA): Harvard University Press. p. 3-25.
13. Brian MV. 1957. The growth and development of colonies of the ant Myrmica. Insectes Soc. 4:177-190.
14. Brown MJF, Schmid-Hempel P. 2003. The evolution of female multiple mating in social Hymenoptera. Evolution. 57:2067-2081.
15. Cagniant H. 1983. La parthénogenèse thélytoque et arrhénotoque des ouvrières de la fourmi Cataglyphis cursor Fonscolombe (Hymenoptères Formicidae). Etude biométrique des ouvrières et de leurs potentialités reproductrices. Insectes Soc. 30:241-254.
16. Camargo RS, Forti LC, Lopes JFS, Andrade APP, Ottati ALT. 2007. Age polyethism in the leaf-cutting ant Acromyrmex subterraneus brunneus Forel, 1911 (Hym., Formicidae). J Appl Entomol. 131:139-145.
17. Cerdà X. 2001. Behavioural and physiological traits to thermal stress tolerance in two Spanish desert ants. Etologia. 9:15-27.
18. Cerdà X, Retana J. 2000. Alternative strategies by thermophilic ants to cope with extreme heat: individual versus colony level traits. Oikos. 89:155-163.
19. Cerdà X, Retana J, Cros S. 1998. Critical thermal limits in Mediterranean ant species: trade-off between mortality risk and foraging performance. Funct Ecol. 12:45-55.
20. Chapman NC, Oldroyd BP, Hughes WOH. 2007. Differential responses of honeybee (Apis mellifera) patrilines to changes in stimuli for the generalist tasks of nursing and foraging. Behav Ecol Sociobiol. 61:1185-1194.
21. Choe JC. 1995. Courtship feeding and repeated mating in Zorotypus barberi (Insecta: Zoraptera). Anim Behav. 49:1511-1520.
22. Clémencet J, Cournault L, Odent A, Doums C. 2010. Worker thermal tolerance in the thermophilic ant Cataglyphis cursor (Hymenoptera, Formicidae). Insectes Soc. 57:11-15.
23. Clémencet J, Doums C. 2007. Habitat-related microgeographic variation of worker size and colony size in the ant Cataglyphis cursor. Oecologia. 152:211-218.
24. Clémencet J, Viginier B, Doums C. 2005. Hierarchical analysis of population genetic structure in the monogynous ant Cataglyphis cursor using microsatellite and mitochondrial DNA markers. Mol Ecol. 14:3735-3744.
25. Cole BJ. 1983. Multiple mating and the evolution of social behavior in the Hymenoptera. Behav Ecol Sociobiol. 12:191-201.
26. Cook JM, Crozier R. 1995. Sex determination and population biology in the Hymenoptera. Trends Ecol Evol. 10:281-286.
27. Cornell SJ, Tregenza T. 2007. A new theory for the evolution of polyandry as a means of inbreeding avoidance. Proc R Soc London B Biol Sci. 274:2873-2879.
28. Crozier RH, Fjerdingstad EJ. 2001. Polyandry in social Hymenoptera disunity in diversity? Ann Zool Fenn. 38:267-285.
29. Crozier RH, Page RE. 1985. On being the right size: male contributions and multiple mating in social hymenoptera. Behav Ecol Sociobiol. 18:105-116.
30. Evison SEF, Hughes WOH. 2011. Genetic caste polymorphism and the evolution of polyandry in Atta leaf-cutting ants. Naturwissenschaften. 98:643-649.
31. Fournier D, Battaille G, Timmermans I, Aron S. 2008. Genetic diversity, worker size polymorphism and division of labour in the polyandrous ant Cataglyphis cursor. Anim Behav. 75:151-158.
32. Fraser VS, Kaufmann B, Oldroyd BP, Crozier RH. 2000. Genetic influence on caste in the ant Camponotus consobrinus. Behav Ecol Sociobiol. 47:188-194.
33. Frumhoff PC, Baker J. 1988. A genetic component to division of labour within honey bee colonies. Nature. 333:358-361.
34. Gowaty PA, Kim YK, Rawlings J, Anderson WW. 2010. Polyandry increases offspring viability and mother productivity but does not decrease mother survival in Drosophila pseudoobscura. Proc Natl Acad Sci USA. 107:13771-13776.
35. Hamilton WD. 1987. Kinship, recognition, disease, and intelligence: constraints of social evolution. In: Ito Y, Brown LJ, Kikkawa J, editors. Animal societies: theories and facts. Tokyo: Japan Scienti?c Societies Press. p. 81-100.
36. Hart AG, Ratnieks FLW. 2002. Waste management in the leaf-cutting ant Atta colombica. Behav Ecol. 13:224-231.
37. Hölldobler B, Wilson EO. 1990. The ants. Berlin: Springer-Verlag.
38. Holm S. 1979. A simple sequential rejective multiple test procedure. Scand J Stat. 6:65-70.
39. Holman L, Stürup M, Trontti K, Boomsma JJ. 2011. Random sperm use and genetic effects on worker caste fate in Atta colombica leafcutting ants. Mol Ecol. 50:5092-5102.
40. Hosken D, Stockley P. 2003. Benefits of polyandry: a life history perspective. Evol Biol. 33:173-194.
41. Hughes WOH, Oldroyd BP, Beekman M, Ratnieks FLW. 2008. Ancestral monogamy shows kin selection is key to the evolution of eusociality. Science. 320:1213-1216.
42. Hughes WOH, Sumner S, Van Borm S, Boomsma JJ. 2003. Worker caste polymorphism has a genetic basis in Acromyrmex leaf-cutting ants. Proc Natl Acad Sci USA. 100:9394-9397.
43. Jaffé R, Kronauer DJC, Kraus FB, Boomsma JJ, Moritz RFA. 2007. Worker caste determination in the army ant Eciton burchellii. Biol Lett. 3:513-516.
44. Jandt JM, Dornhaus A. 2009. Spatial organization and division of labour in the bumblebee Bombus impatiens. Anim Behav. 77:641-651.
45. Jennions MD, Petrie M. 2000. Why do females mate multiply? A review of the genetic bene?ts. Biol Rev. 75:21-64.
46. Johnson B. 2010. Spatial effects, sampling errors, and task specialization in the honey bee. Insectes Soc. 57:239-248.
47. Jones JC, Myerscough MR, Graham S, Oldroyd BP. 2004. Honey bee nest thermoregulation: diversity promotes stability. Science. 305:402-404.
48. Julian GE, Fewell JH. 2004. Genetic variation and task specialization in the desert leaf-cutter ant, Acromyrmex versicolor. Anim Behav. 68:1-8.
49. Kaspari M, Byrne MM. 1995. Caste allocation in litter Pheidole: lessons from plant defense theory. Behav Ecol Sociobiol. 37:255-263.
50. Kraus BF, Gerecke E, Moritz RFA. 2011. Shift work has a genetic basis in honeybee pollen foragers (Apis mellifera L.) . Behav Genet. 41:323-328.
51. Kryger P, Kryger U, Moritz RFA. 2000. Genotypical variability for the tasks of water collecting and scenting in a honey bee colony. Ethology. 106:769-779.
52. Lenoir A, Aron S, Cerdà X, Hefetz A. 2009. Cataglyphis desert ants: a good model for evolutionary biology in Darwin's anniversary year-A review. Isr J Entomol. 39:1-32.
53. Lynch M, Walsh B. 1998. Sib analysis. In: Lynch M, Walsh B, editors. Genetics and analysis of quantitative traits. Sunderland (MA): Sinauer. p. 553-579.
54. Mattila HR, Seeley TD. 2007. Genetic diversity in honey bee colonies enhances productivity and fitness. Science. 317:362-364.
55. Michalczyk AU, Millard AL, Martin OY, Lumley AJ, Emerson BC, Chapman T, Gage MJG. 2011. Inbreeding promotes female promiscuity. Science. 333:1739-1742.
56. Muscedere M, Berglund J, Traniello J. 2011. Polymorphism and division of labor during foraging cycles in the leaf-cutting ant Acromyrmex octospinosus; (Formicidae; Attini). J Insect Behav. 24:94-105.
57. Oldroyd BP, Fewell JH. 2007. Genetic diversity promotes homeostasis in insect colonies. Trends Ecol Evol. 22:408-413.
58. Oldroyd BP, Sylvester HA, Wongsiri S, Rinderer TE. 1994. Task specialization in a wild bee, Apis florea (Hymenoptera, Apidae), revealed by RFLP banding. Behav Ecol Sociobiol. 34:25-30.
59. Oxley PR, Spivak M, Oldroyd BP. 2010. Six quantitative trait loci influence task thresholds for hygienic behaviour in honeybees (Apis mellifera). Mol Ecol. 19:1452-1461.
60. Page RE, Robinson GE, Fondrk MK, Nasr ME. 1995. Effects of worker genotypic diversity on honey bee colony development and behavior (Apis mellifera L.) . Behav Ecol Sociobiol. 36:387-396.
61. Parker GA. 1970. Sperm competition and its evolutionary consequences in the insects. Biol Rev. 45:525-567.
62. Pearcy M, Aron S. 2006. Local resource competition and sex ratio in the ant Cataglyphis cursor. Behav Ecol. 17:569-574.
63. Pearcy M, Aron S, Doums C, Keller L. 2004. Conditional use of sex and parthenogenesis for worker and queen production in ants. Science. 306:1780-1783.
64. Pearcy M, Hardy O, Aron S. 2006. Thelytokous parthenogenesis and its consequences on inbreeding in an ant. Heredity. 96(5):377-382.
65. Pearcy M, Timmermans I, Allard D, Aron S. 2009. Multiple mating in the ant Cataglyphis cursor: testing the sperm limitation and the diploid male load hypotheses. Insectes Soc. 56:94-102.
66. Porter SD, Tschinkel WR. 1985. Fire ant polymorphism: factors affecting worker size. Ann Entomol Soc Am. 78:381-386.
67. Ratnieks FLW. 1988. Reproductive harmony via mutual policing by workers in eusocial Hymenoptera. Am Nat. 132:217-236.
68. Ratnieks FLW, Boomsma JJ. 1995. Facultative sex allocation by workers and the evolution of polyandry by queens in social Hymenoptera. Am Nat. 145:969-993.
69. Ravary F, Lecoutey E, Kaminski G, Chaline N, Jaisson P. 2007. Individual experience alone can generate lasting division of labor in ants. Curr Biol. 17:1308-1312.
70. Reynolds JD. 1996. Animal breeding systems. Trends Ecol Evol. 11:68-72.
71. Rheindt FE, Strehl CP, Gadau J. 2005. A genetic component in the determination of worker polymorphism in the Florida harvester ant Pogonomyrmex badius. Insectes Soc. 52:163-168.
72. Robinson GE, Page RE. 1988. Genetic determination of guarding and undertaking in honeybee colonies. Nature. 333:356-358.
73. Robinson GE, Page RE. 1989. Genetic determination of nectar foraging, pollen foraging, and nest-site scouting in honey bee colonies. Behav Ecol Sociobiol. 24:317-323.
74. Rosset H, Keller L, Chapuisat M. 2005. Experimental manipulation of colony genetic diversity had no effect on short-term task efficiency in the Argentine ant Linepithema humile. Behav Ecol Sociobiol. 58:87-98.
75. Schlüns EA, Wegener BJ, Robson SKA. 2011. Genetic polyethism and nest building in the weaver ant Oecophylla smaragdina (Fabricius 1775)(Hymenoptera: Formicidae). Myrmecol News. 15:7-11.
76. Schmid-Hempel P. 1998. Parasites in social insects. Princeton (NJ): Princeton University Press.
77. Schwander T, Rosset H, Chapuisat M. 2005. Division of labour and worker size polymorphism in ant colonies: the impact of social and genetic factors. Behav Ecol Sociobiol. 59:215-221.
78. Seeley T, Tarpy D. 2007. Queen promiscuity lowers disease within honeybee colonies. Proc R Soc B Biol Sci. 274:67-72.
79. Sherman PW, Seeley TD, Reeve HK. 1988. Parasites, pathogens, and polyandry in social Hymenoptera. Am Nat. 131:602-610.
80. Simmons LW. 2001. Sperm competition and its evolutionary consequences in the insects. Princeton (NJ): Princeton University Press.
81. Slayter RA, Mautz BS, Backwell PRY, Jennions MD. 2012. Estimating genetic benefits of polyandry from experimental studies: a metaanalysis. Biol Rev. 87:1-33.
82. Strassmann J. 2001. The rarity of multiple mating by females in the social Hymenoptera. Insectes Soc. 48:1-13.
83. Sundström L, Boomsma JJ. 2000. Reproductive alliances and posthumous fitness enhancement in male ants. Proc R Soc London B Biol Sci. 267:1439-1444.
84. Tarpy DR, Caren JR, Delaney DA, Sammataro D, Finley J, Loper GM, DeGrandi-Hoffman G. 2010. Mating frequencies of Africanized honey bees in the south western USA. J Apic Res. 49:302-310.
85. Tarpy DR, Page RE. 2002. Sex determination and the evolution of polyandry in honey bees (Apis mellifera). Behav Ecol Sociobiol. 52:143-150.
86. Thornill R, Alcock J. 1983. The evolution of insect mating systems. Cambridge (MA): Harvard University Press.
87. Timmermans I, Hefetz A, Fournier D, Aron S. 2008. Population genetic structure, worker reproduction and thelytokous parthenogenesis in the desert ant Cataglyphis sabulosa. Heredity. 101:490-498.
88. Trivers RL, Hare H. 1976. Haplodiploidy and the evolution of the social insects. Sciences. 191:249-263.
89. Waddington SJ, Hughes WOH. 2010. Waste management in the leafcutting ant Acromyrmex echinatior: the role of worker size, age and plasticity. Behav Ecol Sociobiol. 64:1219-1228.
90. Waddington SJ, Santorelli LA, Ryan FR, Hughes WOH. 2010. Genetic polyethism in leaf-cutting ants. Behav Ecol. 21:1165-1169.
91. Wang J. 2004. Sibship reconstruction from genetic data with typing errors. Genetics. 166:1963-1979.
92. Waser NM. 1998. Task-matching and short-term size shifts in foragers of the harvester ant, Messor pergandei (Hymenoptera: Formicidae). J Insect Behav. 11:451-462.
93. Wetterer JK. 1994. Ontogenetic changes in forager polymorphism and foraging ecology in the leaf-cutting ant Atta cevhalotes. Oecologia. 98:235-238.
94. Wetterer JK. 1999. The ecology and evolution of worker size-distribution in leaf-cutting ants (Hymenoptera: Formicidae). Sociobiology. 34:119-144.
95. Wiernasz DC, Cole BJ. 2010. Patriline shifting leads to apparent genetic caste determination in harvester ants. Proc Natl Acad Sci USA. 107(29):12958-12962.
96. Wilson EO. 1980. Caste and division of labor in leaf-cutter ants (Hymenoptera, Formicidae, Atta). 2. The ergonomic optimization of leaf cutting. Behav Ecol Sociobiol. 7:157-165.
97. Wood LA, Tschinkel WR. 1981. Quantification and modification of worker size variation in the fire ant Solenopsis invicta. Insectes Soc. 28:117-128.
98. Woyciechowski M, Lomnicki A. 1987. Multiple mating of queens and sterility of workers among eusocial Hymenoptera. J Theor Biol. 128:317-327.