Insectes Sociaux

, Volume 63, Issue 4, pp 531–541 | Cite as

Distribution and origin of intraspecific social variation in the California harvester ant Pogonomyrmex californicus

  • R. OversonEmail author
  • J. Fewell
  • J. Gadau
Research Article


The California seed harvester ant Pogonomyrmex californicus exhibits striking differences in queen behavior and colony organization throughout its range. Most populations show the likely ancestral condition of single-queen colonies (monogyny). However, in one known population, cooperation between queens during colony founding (pleometrosis) occurs, and is suspected to persist to the mature colony stage (primary polygyny). To better understand this variation in social phenotype, we estimate relatedness among co-foundresses, measure the frequency of polygyny in adult colonies across three focal populations, and assess population genetic structure between populations. We additionally measure queen mating frequency (polyandry) across focal populations. With few possible exceptions, queens within pleometrotic associations are unrelated. We demonstrate a correlation between pleometrosis in incipient colonies and polygyny in adult colonies at the population level. Nuclear microsatellites and mtDNA barcoding indicate significant structure between focal populations. Queens from all three focal populations engage in relatively high levels of polyandry. These findings, when examined with previous data demonstrating that pleometrosis leads to polygynous colonies in the laboratory, strongly suggest that the same occurs in nature. However, the possibility of additional queen adoption in adult colonies (secondary polygyny) is not excluded. Thus, polygynous P. californicus colonies potentially represent long-term associations of unrelated family groups, containing multiple unrelated queens and their mixed-paternity offspring. Due to its pronounced variation in social behavior, P. californicus provides a unique opportunity to examine the evolutionary history and genetic underpinnings of cooperation among non-relatives, a strategy of intense interest in behavioral ecology.


Pogonomyrmex Primary polygyny Pleometrosis Cooperation Population genetics Biogeography 



We would like to thank Tresa Marchi and Danielle Sensenig, who worked tirelessly and efficiently at genotyping samples. Robert A. Johnson, C. Tate Holbrook, Joshua D. Gibson, and Brendon Mott provided samples. Bert Hölldobler provided valuable contributions to the development of ideas leading to this study. We would also like to thank two anonymous reviewers for their thorough feedback which strongly improved this manuscript.

Supplementary material

40_2016_497_MOESM1_ESM.docx (71 kb)
Supplementary material 1 (DOCX 71 kb)


  1. Alonso WJ, Schuck-Paim C (2002) Sex-ratio conflicts, kin selection, and the evolution of altruism. Proc Natl Acad Sci USA 99:6843. doi: 10.1073/pnas.092584299 CrossRefPubMedPubMedCentralGoogle Scholar
  2. Aviles L (2002) Solving the freeloaders paradox: genetic associations and frequency-dependent selection in the evolution of cooperation among nonrelatives. Proc Natl Acad Sci USA 99:14268–14273. doi: 10.1073/pnas.212408299 CrossRefPubMedPubMedCentralGoogle Scholar
  3. Baglione V, Canestrari D, Marcos JM, Ekman J (2003) Kin selection in cooperative alliances of carrion crows. Science 300:1947. doi: 10.1126/science.1082429 CrossRefPubMedGoogle Scholar
  4. Balshine-Earn S, Neat FC, Reid H, Taborsky M (1998) Paying to stay or paying to breed? Field evidence for direct benefits of helping behavior in a cooperatively breeding fish. Behav Ecol 9:432–438. doi: 10.1093/beheco/9.5.432 CrossRefGoogle Scholar
  5. Bartz SH, Hölldobler B (1982) Colony founding in Myrmecocystus mimicus Wheeler (Hymenoptera, Formicidae) and the evolution of foundress-associations. Behav Ecol Sociobiol 10:137–147. doi: 10.1007/BF00300174 CrossRefGoogle Scholar
  6. Bekkevold D, Frydenberg J, Boomsma JJ (1999) Multiple mating and facultative polygyny in the Panamanian leafcutter ant Acromyrmex echinatior. Behav Ecol Sociobiol 46:103–109. doi: 10.1007/s002650050598 CrossRefGoogle Scholar
  7. Bernasconi G, Keller L (1996) Reproductive conflicts in cooperative associations of fire ant queens (Solenopsis invicta). Proc R Soc Lond B Biol Sci 263:509–513. doi: 10.1098/rspb.1996.0077 CrossRefGoogle Scholar
  8. Bernasconi G, Strassmann JE (1999) Cooperation among unrelated individuals: the ant foundress case. Trends Ecol Evol 14:477–482. doi: 10.1016/S0169-5347(99)01722-X CrossRefPubMedGoogle Scholar
  9. Bourke AFG (1988) Dominance orders, worker reproduction, and queen-worker conflict in the slave-making ant Harpagoxenus sublaevis. Behav Ecol Sociobiol 23:323–333. doi: 10.1007/bf00300579 CrossRefGoogle Scholar
  10. Bourke AFG, Franks NR (1995) Social evolution in ants. Princeton University Press, PrincetonGoogle Scholar
  11. Bourke AFG, Green HA, Bruford MW (1997) Parentage, reproductive skew and queen turnover in a multiple-queen ant analysed with microsatellites. Proc R Soc Lond B Biol Sci 264:277. doi: 10.1098/rspb.1997.0039 CrossRefGoogle Scholar
  12. Bshary R (2010) Cooperation between unrelated individuals—a game theoretic approach. Animal behaviour: evolution and mechanisms. Springer, Berlin, pp 213–240CrossRefGoogle Scholar
  13. Buckley SB (1867) Descriptions of new species of North American Formicidae. Entomol Soc Phila 6:335–350Google Scholar
  14. Cahan S (1999) Causes and consequences of an abrupt transition in colony founding behavior in the ant Messor pergandei - Ph.D. dissertation, Arizona State University, TempeGoogle Scholar
  15. Cahan SH (2001) Ecological variation across a transition in colony-founding behavior in the ant Messor pergandei. Oecologia 129:629–635. doi: 10.1007/s004420100761 CrossRefPubMedGoogle Scholar
  16. Cahan SH, Fewell JH (2004) Division of labor and the evolution of task sharing in queen associations of the harvester ant Pogonomyrmex californicus. Behav Ecol Sociobiol 56:9–17. doi: 10.1007/s00265-003-0746-5 CrossRefGoogle Scholar
  17. Cahan S, Helms KR, Rissing SW (1998) An abrupt transition in colony founding behaviour in the ant Messor pergandei. Anim Behav 55:1583–1594. doi: 10.1006/anbe.1997.0699 CrossRefPubMedGoogle Scholar
  18. Chapuisat M (1998) Mating frequency of ant queens with alternative dispersal strategies, as revealed by microsatellite analysis of sperm. Mol Ecol 7:1097–1105. doi: 10.1046/j.1365-294x.1998.00422.x CrossRefGoogle Scholar
  19. Cheney DL, Moscovice LR, Heesen M et al (2010) Contingent cooperation between wild female baboons. Proc Natl Acad Sci USA 107:9562–9566. doi: 10.1073/pnas.1001862107 CrossRefPubMedPubMedCentralGoogle Scholar
  20. Clark RM, Fewell JH (2014) Social dynamics drive selection in cooperative associations of ant queens. Behav Ecol 25:117–123. doi: 10.1093/beheco/art093 CrossRefGoogle Scholar
  21. Clutton-Brock T (2002) Breeding together: kin selection and mutualism in cooperative vertebrates. Science 296:69. doi: 10.1126/science.296.5565.69 CrossRefPubMedGoogle Scholar
  22. Clutton-Brock T (2009) Cooperation between non-kin in animal societies. Nature 462:51–57. doi: 10.1038/nature08366 CrossRefPubMedGoogle Scholar
  23. Cole BJ (2009) The ecological setting of social evolution: the demography of ant populations. In: Gadau J, Fewell J (eds) Organization of insect societies: from genome to sociocomplexity. Harvard University Press, Cambridge, p 74–104 Google Scholar
  24. Cole BJ, Wiernasz DC (2000) The nature of ant colony success—response. Science 287:1363. doi: 10.1126/science.287.5457.1363b CrossRefGoogle Scholar
  25. Core Team R (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  26. Creel SR, Rabenold KN (1994) Inclusive fitness and reproductive strategies in dwarf mongooses. Behav Ecol 5:339–348. doi: 10.1093/beheco/5.3.339 CrossRefGoogle Scholar
  27. Diehl E, de Araújo AM, Cavalli-Molina S (2001) Genetic variability and social structure of colonies in Acromyrmex heyeri and A. striatus (Hymenoptera: Formicidae). Braz J Biol 61:667–678. doi: 10.1590/S1519-69842001000400017 PubMedGoogle Scholar
  28. Dolezal AG, Brent CS, Gadau J et al (2009) Endocrine physiology of the division of labour in Pogonomyrmex californicus founding queens. Anim Behav 77:1005–1010. doi: 10.1016/j.anbehav.2009.01.010 CrossRefGoogle Scholar
  29. Dugatkin LA (2002) Animal cooperation among unrelated individuals. Naturwissenschaften 89:533–541. doi: 10.1007/s00114-002-0379-y PubMedGoogle Scholar
  30. Dugatkin LA, Mesterton-Gibbons M (1996) Cooperation among unrelated individuals: reciprocal altruism, by-product mutualism and group selection in fishes. Biosystems 37:19–30. doi: 10.1016/0303-2647(95)01542-6 CrossRefPubMedGoogle Scholar
  31. Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620. doi: 10.1111/j.1365-294X.2005.02553.x CrossRefPubMedGoogle Scholar
  32. Fomer O, Black M, Hoeh W et al (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol 3:294–299Google Scholar
  33. Foster RL, Brunskill A, Verdirame D, O’Donnell S (2004) Reproductive physiology, dominance interactions, and division of labour among bumble bee workers. Physiol Entomol 29:327–334. doi: 10.1111/j.0307-6962.2004.00388.x CrossRefGoogle Scholar
  34. Gadau J (2009) DNA isolation from ants. Cold Spring Harb Protoc 2009(7). doi: 10.1101/pdb.prot5245
  35. Gadau J, Strehl CP, Oettler J, Hölldobler B (2003) Determinants of intracolonial relatedness in Pogonomyrmex rugosus (Hymenoptera; Formicidae): mating frequency and brood raids. Mol Ecol 12:1931–1938. doi: 10.1046/j.1365-294X.2003.01853.x CrossRefPubMedGoogle Scholar
  36. Goudet J (1995) FSTAT (version 1.2): a computer program to calculate F-statistics. J Hered 86:485Google Scholar
  37. Griffin AS, West SA (2003) Kin discrimination and the benefit of helping in cooperatively breeding vertebrates. Science 302:634. doi: 10.1126/science.1089402 CrossRefPubMedGoogle Scholar
  38. Hacker M, Kaib M, Bagine RKN et al (2005) Unrelated queens coexist in colonies of the termite Macrotermes michaelseni. Mol Ecol 14:1527–1532. doi: 10.1111/j.1365-294X.2005.02507.x CrossRefPubMedGoogle Scholar
  39. Hamilton WD (1964) The genetical evolution of social behaviour. I. J Theor Biol 7:1–16. doi: 10.1016/0022-5193(64)90038-4 CrossRefPubMedGoogle Scholar
  40. Hamilton WD (1971) Selection of selfish and altruistic behaviour in some extreme models. Man and beast: comparative social behavior. Smithsonian Press, Washington, D.C., pp 57–91Google Scholar
  41. Hammond R, Bourke A, Bruford M (2001) Mating frequency and mating system of the polygynous ant, Leptothorax acervorum. Mol Ecol 10:2719–2728. doi: 10.1046/j.0962-1083.2001.01394.x CrossRefPubMedGoogle Scholar
  42. Heinze J (1993) Queen-queen interactions in polygynous ants. Queen number and sociality in insects. Oxford University Press, Oxford, pp 334–361Google Scholar
  43. Helms KR, Helms Cahan S (2012) Large-scale regional variation in cooperation and conflict among queens of the desert ant Messor pergandei. Anim Behav 84:499–507. doi: 10.1016/j.anbehav.2012.05.019 CrossRefGoogle Scholar
  44. Holbrook CT, Eriksson TH, Overson RP et al (2013) Colony-size effects on task organization in the harvester ant Pogonomyrmex californicus. Insectes Soc 60:191–201. doi: 10.1007/s00040-013-0282-x CrossRefGoogle Scholar
  45. Hölldobler B, Carlin NF (1985) Colony founding, queen dominance and oligogyny in the Australian meat ant Iridomyrmex purpureus. Behav Ecol Sociobiol 18:45–58. doi: 10.1007/BF00299237 Google Scholar
  46. Hölldobler B, Wilson E (2009) The superorganism: the beauty, elegance, and strangeness of insect societies. WW Norton & Company Inc, New YorkGoogle Scholar
  47. Hölldobler B, Grillenberger B, Gadau J (2011) Queen number and raiding behavior in the ant genus Myrmecocystus (Hymenoptera: Formicidae). Myrmecol News 15:53–61Google Scholar
  48. Hughes AR, Inouye BD, Johnson MTJ et al (2008) Ecological consequences of genetic diversity. Ecol Lett 11:609–623. doi: 10.1111/j.1461-0248.2008.01179.x CrossRefPubMedGoogle Scholar
  49. Hunt J (2007) The evolution of social wasps. Oxford University Press, New YorkCrossRefGoogle Scholar
  50. Ito F (1993) Social organization in a primitive ponerine ant: queenless reproduction, dominance hierarchy and functional polygyny in Amblyopone sp. (reclinata group) (Hymenoptera: Formicidae: Ponerinae). J Nat Hist 27:1315–1324. doi: 10.1080/00222939300770751 CrossRefGoogle Scholar
  51. Jeanson R, Fewell J (2008) Influence of the social context on division of labor in ant foundress associations. Behav Ecol 19:567. doi: 10.1093/beheco/arn018 CrossRefGoogle Scholar
  52. Johnson RA (2004) Colony founding by pleometrosis in the semiclaustral seed-harvester ant Pogonomyrmex californicus (Hymenoptera: Formicidae). Anim Behav 68:1189–1200CrossRefGoogle Scholar
  53. Johnson RA, Overson RP (2009) A new North American species of Pogonomyrmex (Hymenoptera: Formicidae) from the Mohave Desert of eastern California and western Nevada. J Hymenopt Res 18:305–314Google Scholar
  54. Johnson RA, Overson RP, Moreau CS (2013) A new species of seed-harvester ant, Pogonomyrmex hoelldobleri (Hymenoptera: Formicidae), from the Mohave and Sonoran Deserts of North America. Zootaxa 3646:201–227. doi: 10.11646/zootaxa.3646.3.1 CrossRefPubMedGoogle Scholar
  55. Keller L (1995) Social life: the paradox of multiple-queen colonies. Trends Ecol Evol 10:355–360. doi: 10.1016/S0169-5347(00)89133-8 CrossRefPubMedGoogle Scholar
  56. Keller L, Reeve HK (1994) Genetic variability, queen number, and polyandry in social Hymenoptera. Evolution 48:694–704. doi: 10.2307/2410479 CrossRefGoogle Scholar
  57. Kellner K, Trindl A, Heinze J, D’Ettorre P (2007) Polygyny and polyandry in small ant societies. Mol Ecol 16:2363–2369. doi: 10.1111/j.1365-294X.2007.03297.x CrossRefPubMedGoogle Scholar
  58. Kolmer K, Heinze J (2000) Rank orders and division of labour among unrelated cofounding ant queens. Proc R Soc Lond B Biol Sci 267:1729–1734. doi: 10.1098/rspb.2000.1202 CrossRefGoogle Scholar
  59. Kolmer K, Hölldobler B, Heinze J (2002) Colony and population structure in Pachycondyla cf. inversa, a ponerine ant with primary polygyny. Ethol Ecol Evol 14:157–164. doi: 10.1080/08927014.2002.9522754 CrossRefGoogle Scholar
  60. Kronauer DJ, Boomsma JJ (2007) Multiple queens means fewer mates. Curr Biol 17:R753–R755. doi: 10.1016/j.cub.2007.06.057 CrossRefPubMedGoogle Scholar
  61. Kronauer DJC, Johnson RA, Boomsma JJ (2007) The evolution of multiple mating in army ants. Evolution 61:413–422. doi: 10.1111/j.1558-5646.2007.00040.x CrossRefPubMedGoogle Scholar
  62. Mintzer AC (1987) Primary polygyny in the ant Atta texana: number and weight of females and colony foundation success in the laboratory. Insectes Soc 34:108–117. doi: 10.1007/BF02223829 CrossRefGoogle Scholar
  63. Monnin T, Peeters C (1999) Dominance hierarchy and reproductive conflicts among subordinates in a monogynous queenless ant. Behav Ecol 10:323–332. doi: 10.1093/beheco/10.3.323 CrossRefGoogle Scholar
  64. Nielsen R, Tarpy DR, Reeve HK (2003) Estimating effective paternity number in social insects and the effective number of alleles in a population. Mol Ecol 12:3157–3164. doi: 10.1046/j.1365-294X.2003.01994.x CrossRefPubMedGoogle Scholar
  65. Overson R, Gadau J, Clark RM et al (2013) Behavioral transitions with the evolution of cooperative nest founding by harvester ant queens. Behav Ecol Sociobiol. doi: 10.1007/s00265-013-1618-2 Google Scholar
  66. Pamilo P (1993) Polyandry and allele frequency differences between the sexes in the ant Formica aquilonia. Heredity 70:472–480. doi: 10.1038/hdy.1993.69 CrossRefGoogle Scholar
  67. Pedersen JS, Boomsma JJ (1999a) Positive association of queen number and queen-mating frequency in Myrmica ants: a challenge to the genetic-variability hypotheses. Behav Ecol Sociobiol 45:185–193. doi: 10.1007/s002650050552 CrossRefGoogle Scholar
  68. Pedersen JS, Boomsma JJ (1999b) Multiple paternity in social Hymenoptera: estimating the effective mate number in single–double mating populations. Mol Ecol 8:577–587. doi: 10.1046/j.1365-294x.1999.00573.x CrossRefGoogle Scholar
  69. Penick CA, Liebig J, Brent CS (2011) Reproduction, dominance, and caste: endocrine profiles of queens and workers of the ant Harpegnathos saltator. J Comp Physiol A 197:1063–1071. doi: 10.1007/s00359-011-0667-0 CrossRefGoogle Scholar
  70. Pew J, Wang J, Muir P, Frasier T (2015) related: related: an R package for analyzing pairwise relatedness data based on codominant molecular markers. R package version 1.0Google Scholar
  71. Pol R, de Casenave J, Feldhaar H et al (2008) Polyandry in two South American harvester ants. Insectes Soc 55:91–97. doi: 10.1007/s00040-007-0975-0 CrossRefGoogle Scholar
  72. Pritchard J, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945PubMedPubMedCentralGoogle Scholar
  73. Qian ZQ, Schlüns H, Schlick-Steiner BC et al (2011) Intraspecific support for the polygyny-vs.-polyandry hypothesis in the bulldog ant Myrmecia brevinoda. Mol Ecol 20:3681–3691. doi: 10.1111/j.1365-294X.2011.05195.x PubMedGoogle Scholar
  74. Queller D, Goodnight K (1989) Estimating relatedness using genetic markers. Evolution 43:258–275. doi: 10.2307/2409206 CrossRefGoogle Scholar
  75. Queller DC, Strassmann JE (1998) Kin selection and social insects. Bioscience 48:165–175. doi: 10.2307/1313262 Google Scholar
  76. Queller DC, Zacchi F, Cervo R et al (2000) Unrelated helpers in a social insect. Nature 405:784–787. doi: 10.1038/35015552 CrossRefPubMedGoogle Scholar
  77. Rheindt FE, Gadau J, Strehl CP, Hölldobler B (2004) Extremely high mating frequency in the Florida harvester ant (Pogonomyrmex badius). Behav Ecol Sociobiol 56:472–481. doi: 10.1007/s00265-004-0808-3 CrossRefGoogle Scholar
  78. Rissing SW, Pollock GB (1987) Queen aggression, pleometrotic advantage and brood raiding in the ant Veromessor pergandei (Hymenoptera, Formicidae). Anim Behav 35:975–981. doi: 10.1016/S0003-3472(87)80154-9 CrossRefGoogle Scholar
  79. Rissing SW, Pollock GB, Higgins MR et al (1989) Foraging specialization without relatedness or dominance among co-founding ant queens. Nature 338:420–422. doi: 10.1038/338420a0 CrossRefGoogle Scholar
  80. Rissing SW, Johnson RA, Martin JW (2000) Colony founding behavior of some desert ants: geographic variation in metrosis. Psyche (Stuttg) 103:95CrossRefGoogle Scholar
  81. Röseler P-F, Röseler I, Strambi A, Augier R (1984) Influence of insect hormones on the establishment of dominance hierarchies among foundresses of the paper wasp, Polistes gallicus. Behav Ecol Sociobiol 15:133–142. doi: 10.1007/BF00299381 CrossRefGoogle Scholar
  82. Schlüns E, Wegener B, Schlüns H et al (2009) Breeding system, colony and population structure in the weaver ant Oecophylla smaragdina. Mol Ecol 18:156–167. doi: 10.1111/j.1365-294X.2008.04020.x CrossRefPubMedGoogle Scholar
  83. Sefc KM, Koblmüller S (2009) Assessing parent numbers from offspring genotypes: the importance of marker polymorphism. J Hered 100:197–205. doi: 10.1093/jhered/esn095 CrossRefPubMedGoogle Scholar
  84. Sommer K, Hölldobler B (1995) Colony founding by queen association and determinants of reduction in queen number in the ant Lasius niger. Anim Behav 50:287–294. doi: 10.1006/anbe.1995.0244 CrossRefGoogle Scholar
  85. Starr CK (1984) Sperm competition, kinship, and sociality in the aculeate Hymenoptera. In: Smith RL (ed) Sperm competition and the evolution of animal mating systems. Academic Press, Inc., Orlando, pp 427–464Google Scholar
  86. Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596. doi: 10.1093/molbev/msm092 CrossRefPubMedGoogle Scholar
  87. Toquenaga Y (2005) Special feature: cooperation among unrelated individuals—Preface. Popul Ecol 47:1–2. doi: 10.1007/s10144-005-0206-3 CrossRefGoogle Scholar
  88. Trontti K, Thurin N, Sundström L, Aron S (2007) Mating for convenience or genetic diversity? Mating patterns in the polygynous ant Plagiolepis pygmaea. Behav Ecol 18:298–303. doi: 10.1093/beheco/arl083 CrossRefGoogle Scholar
  89. Trunzer B, Heinze J, Hölldobler B (1998) Cooperative colony founding and experimental primary polygyny in the ponerine ant Pachycondyla villosa. Insectes Soc 45:267–276. doi: 10.1007/s000400050087 CrossRefGoogle Scholar
  90. Tschinkel WR, Howard DF (1983) Colony founding by pleometrosis in the fire ant, Solenopsis invicta. Behav Ecol Sociobiol 12:103–113. doi: 10.1007/BF00343200 CrossRefGoogle Scholar
  91. Volny VP, Gordon DM (2002) Characterization of polymorphic microsatellite loci in the red harvester ant, Pogonomyrmex barbatus. Mol Ecol Notes 2:302–303. doi: 10.1046/j.1471-8286.2002.00243.x CrossRefGoogle Scholar
  92. West-Eberhard MJ (1975) The evolution of social behavior by kin selection. Q Rev Biol 50:1–33. doi: 10.1086/408298 Google Scholar
  93. Wiernasz D, Perroni C, Cole B (2004) Polyandry and fitness in the western harvester ant, Pogonomyrmex occidentalis. Mol Ecol 13:1601–1606. doi: 10.1111/j.1365-294X.2004.02153.x CrossRefPubMedGoogle Scholar
  94. Wright S (1950) Genetical structure of populations. Nature 166:247–249. doi: 10.1038/166247a0 CrossRefPubMedGoogle Scholar

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© International Union for the Study of Social Insects (IUSSI) 2016

Authors and Affiliations

  1. 1.Chicago Botanic GardenGlencoeUSA
  2. 2.School of Life Sciences and Center for Social Dynamics and ComplexityArizona State UniversityTempeUSA

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