Biological Invasions

, Volume 9, Issue 5, pp 571–584

Genetic and morphological variation over space and time in the invasive fire ant Solenopsis invicta

  • Michael A. D. Goodisman
  • Karen A. Sankovich
  • Jennifer L. Kovacs
Original Paper

Abstract

Social insects are among the most successful and damaging of invasive taxa. We studied spatial and temporal variation in two traits, colony genetic structure and worker mass, associated with social insect success in the introduced fire ant Solenopsisinvicta. Our aim was to determine if changes in social structure occurred over time and if variation in worker size was related to worker genotype. We sampled 1139 workers from five multiple-queen S. invicta nests on six dates over a one-year period. The genotypes of workers were determined at ten microsatellite loci and at the selected locus general protein-9 (Gp-9). We found little evidence for genetic differentiation of workers sampled from distinct nests or from different dates at the microsatellite loci. However, worker Gp-9 genotype frequencies varied among nests and over time. In addition, worker mass was affected by nest-of-origin, sampling date, ploidy level, and Gp-9 genotype. Our results suggest that large numbers of queens contribute to the production of workers in introduced S. invicta nests throughout the year. Colony boundaries are semi-permeable, although the among-nest variation in Gp-9 genotype frequencies and worker mass does suggest that boundaries are present. In addition, selection operating on Gp-9 genotype depends on nest environment. Finally, worker mass is affected by both endogenous and exogenous factors in S. invicta. Overall, our data suggests that the key traits of colony social structure and worker size reflect the effects of variable selection in invasive social insects.

Keywords

Insect pest Formicidae Genetic structure Invasive ant Microsatellites Polygyny Relatedness Social insects 

References

  1. Adams ES, Tschinkel WR (2001) Mechanisms of population regulation in the fire ant Solenopsis invicta: an experimental study. J Anim Ecol 70:355–369CrossRefGoogle Scholar
  2. Bourke AFG, Franks NR (1995) Social evolution in ants. Princeton University Press, PrincetonGoogle Scholar
  3. Cahan SH, Vinson SB (2003) Reproductive division of labor between hybrid and nonhybrid offspring in a fire ant hybrid zone. Evolution 57:1562–1570Google Scholar
  4. Calabi P, Porter SD (1989) Worker longevity in the fire ant Solenopsis invicta: ergonomic considerations of correlations between temperature, size and metabolic rates. J Ins Phys 35:643–649CrossRefGoogle Scholar
  5. Callcott AMA, Collins HL (1996) Invasion and range expansion of imported fire ants (Hymenoptera: Formicidae) in North America from 1918–1995. Florida Entomol 79:240–251CrossRefGoogle Scholar
  6. Callcott AMA, Oi DH, Collins HL, Williams DF, Lockley TC (2000) Seasonal studies of an isolated red imported fire ant (Hymenoptera : Formicidae) population in eastern Tennessee. Env Entomol 29:788–794CrossRefGoogle Scholar
  7. Chapman RE, Bourke AFG (2001) The influence of sociality on the conservation biology of social insects. Ecol Lett 4:650–662CrossRefGoogle Scholar
  8. Chapuisat M, Bocherens S, Rosset H (2004) Variable queen number in ant colonies: no impact on queen turnover, inbreeding, and population genetic differentiation in the ant Formica selysi. Evolution 58:5CrossRefGoogle Scholar
  9. Chen YP, Lu LY, Skow LC, Vinson SB (2003) Relatedness among co-existing queens within polygyne colonies of a Texas population of the fire ant, Solenopsis invicta. Southwestern Entomol 28:27–36Google Scholar
  10. Clapperton BK, Tilley JAV, Beggs JR, Moller H (1994) Changes in the distribution and proportions of Vespula vulgaris (L.) and Vespula germanica (Fab.) (Hymenoptera: Vespidae) between 1987 and 1990 in New Zealand. NZ J Zool 21:295–303Google Scholar
  11. Crozier RH, Kaufmann B, Carew ME, Crozier YC (1999) Mutability of microsatellites developed for the ant Camponotus consobrinus. Mol Ecol 8:271–276PubMedCrossRefGoogle Scholar
  12. Crozier RH, Pamilo P (1996) Evolution of social insect colonies: sex allocation and kin selection. Oxford University Press, OxfordGoogle Scholar
  13. Davis LR, Vander Meer R, Porter SD (2001) Red imported fire ants expand their range across the West Indies. Florida Entomol 84:735–736CrossRefGoogle Scholar
  14. DeHeer CJ (2002) A comparison of the colony-founding potential of queens from single- and multiple-queen colonies of the fire ant Solenopsis invicta. Anim Behav 64:655–661CrossRefGoogle Scholar
  15. DeHeer CJ, Goodisman MAD, Ross KG (1999) Queen dispersal strategies in the multiple-queen form of the fire ant Solenopsis invicta. Am Nat 153:660–675CrossRefGoogle Scholar
  16. DeHeer CJ, Vargo EL (2004) Colony genetic organization and colony fusion in the termite Reticulitermes flavipes as revealed by foraging patterns over time and space. Mol Ecol 13:431–441PubMedCrossRefGoogle Scholar
  17. Goodisman MAD, DeHeer CJ, Ross KG (2000a) Unusual behavior of polygyne fire ant queens on nuptial flights. J Ins Behav 13:455–468CrossRefGoogle Scholar
  18. Goodisman MAD, Mack PD, Pearse DE, Ross KG (1999) Effects of a single gene on worker and male body mass in the fire ant Solenopsis invicta (Hymenoptera: Formicidae). Ann Entomol Soc Am 92:563–570Google Scholar
  19. Goodisman MAD, Ross KG (1996) Relationship of queen number and worker size in polygyne colonies of the fire ant Solenopsis invicta. Ins Soc 43:303–307CrossRefGoogle Scholar
  20. Goodisman MAD, Ross KG (1997) Relationship of queen number and queen relatedness in multiple-queen colonies of the fire ant Solenopsis invicta. Ecol Entomol 22:150–157CrossRefGoogle Scholar
  21. Goodisman MAD, Ross KG (1998) A test of queen recruitment models using nuclear and mitochondrial markers in the fire ant Solenopsis invicta. Evolution 52:1416–1422CrossRefGoogle Scholar
  22. Goodisman MAD, Ross KG (1999) Queen recruitment in a multiple-queen population of the introduced fire ant Solenopsis invicta. Behav Ecol 10:428–435CrossRefGoogle Scholar
  23. Goodisman MAD, Ross KG, Asmussen MA (2000b) A formal assessment of the effects of gene flow and selection in the fire ant Solenopsis invicta. Evolution 54:606–616Google Scholar
  24. Greenberg L, Vinson SB, Ellison S (1992) Nine-year study of a field containing both monogyne and polygyne red imported fire ants (Hymenoptera: Formicidae). Ann Entomol Soc Am 85:686–695Google Scholar
  25. Henshaw MT, Kunzmann N, Vanderwoude C, Sanetra M, Crozier RH (2005) Population genetics and history of the introduced fire ant, Solenopsis invicta Buren (Hymenoptera: Formicidae), in Australia. Aust J Entomol 44:37–44CrossRefGoogle Scholar
  26. Hölldobler B, Wilson EO (1990) The ants. The Belknap Press of Harvard University Press, CambridgeGoogle Scholar
  27. Holway DA, Lach L, Suarez AV, Tsutsui ND, Case TJ (2002) The causes and consequences of ant invasions. Annu Rev Ecol Syst 33:181–233CrossRefGoogle Scholar
  28. Ingram KK (2002) Plasticity in queen number and social structure in the invasive argentine ant (Linepithema humile). Evolution 56:2008–2016PubMedGoogle Scholar
  29. Ingram KK, Gordon DM (2003) Genetic analysis of dispersal dynamics in an invading population of Argentine ants. Ecology 84:2832–2842CrossRefGoogle Scholar
  30. Keller L, Ross KG (1998) Selfish genes: a green beard in the red fire ant. Nature 394:573–575CrossRefGoogle Scholar
  31. Keller L, Ross KG (1999) Major gene effects on phenotype and fitness: the relative roles of Pgm-3 and Gp-9 in introduced populations of the fire ant Solenopsis invicta. J Evol Biol 12:672–680CrossRefGoogle Scholar
  32. Krieger MJB, Keller L (1997) Polymorphism at dinucleotide microsatellite loci in fire ant (Solenopsis invicta) populations. Mol Ecol 6:997–999CrossRefGoogle Scholar
  33. Krieger MJB, Ross KG (2002) Identification of a major gene regulating complex social behavior. Science 295:328–332PubMedCrossRefGoogle Scholar
  34. Krieger MJB, Ross KG, Chang CWY, Keller L (1999) Frequency and origin of triploidy in the fire ant Solenopsis invicta. Heredity 82:142–150CrossRefGoogle Scholar
  35. Lewis PO, Zaykin D (2000) Genetic data analysis: computer program for the analysis of allelic data. Version 1.0 (d15). Google Scholar
  36. Lowe S, Browne M, Boudjelas S, De Poorter M (2000) 100 of the world’s worst invasive alien species: a selection from the global invasive species database. Invasive species specialist groupGoogle Scholar
  37. Macom TE, Porter SD (1996) Comparison of polygyne and monogyne red imported fire ant (Hymenoptera: Formicidae) population densities. Ann Entomol Soc Am 89:535–543Google Scholar
  38. McGlynn TP (1999) Non-native ants are smaller than related native ants. Am Nat 154:690–699CrossRefPubMedGoogle Scholar
  39. Mirenda JT, Vinson SB (1981) Division of labor and specification of castes in the red imported fire ant Solenopsis invicta Buren. Anim Behav 29:410–420CrossRefGoogle Scholar
  40. Moller H (1996) Lessons for invasion theory from social insects. Biol Conserv 78:125–142CrossRefGoogle Scholar
  41. Oster GF, Wilson EO (1978) Caste and ecology in the social insects. Princeton University Press, PrincetonGoogle Scholar
  42. Pimentel D, Lach L, Zuniga R, Morrison D (2000) Environmental and economic costs of nonindigenous species in the United States. Bioscience 50:53–65CrossRefGoogle Scholar
  43. Pinto MA, Rubink WL, Patton JC, Coulson RN, Johnston JS (2005) Africanization in the United States: replacement of feral European honeybees (Apis mellifera L.) by an African hybrid swarm. Genetics 170:1653–1665PubMedCrossRefGoogle Scholar
  44. Porter SD, Tschinkel WR (1986) Adaptive value of nanitic workers in newly founded red imported fire ant colonies (Hymenoptera: Formicidae). Ann Entomol Soc Am 79:723–726Google Scholar
  45. Queller DC, Goodnight KF (1989) Estimating relatedness using genetic markers. Evolution 43:258–275CrossRefGoogle Scholar
  46. Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249Google Scholar
  47. Ross KG (1986) Kin selection and the problem of sperm utilization in social insects. Nature 323:798–800CrossRefGoogle Scholar
  48. Ross KG (1988) Differential reproduction in multiple-queen colonies of the fire ant Solenopsis invicta (Hymenoptera: Formicidae). Behav Ecol Sociobiol 23:341–355CrossRefGoogle Scholar
  49. Ross KG (1993) The breeding system of the fire ant Solenopsis invicta: effects on colony genetic structure. Am Nat 141:554–576CrossRefPubMedGoogle Scholar
  50. Ross KG (1997) Multilocus evolution in fire ants: effects of selection, gene flow and recombination. Genetics 145:961–974PubMedGoogle Scholar
  51. Ross KG (2001) Molecular ecol of social behaviour: analyses of breeding systems and genetic structure. Mol Ecol 10:265–284PubMedCrossRefGoogle Scholar
  52. Ross KG, Fletcher DJC (1985) Genetic origin of male diploidy in the fire ant, Solenopsis invicta (Hymenoptera: Formicidae), and its evolutionary significance. Evolution 39:888–903CrossRefGoogle Scholar
  53. Ross KG, Keller L (1995) Ecology and evolution of social organization: insights from fire ants and other highly eusocial insects. Annu Rev Ecol Syst 26:631–656CrossRefGoogle Scholar
  54. Ross KG, Keller L (1998) Genetic control of social organization in an ant. Proc Natl Acad Sci USA 95:14232–14237PubMedCrossRefGoogle Scholar
  55. Ross KG, Vargo EL, Keller L (1996) Social evolution in a new environment: the case of introduced fire ants. Proc Natl Acad Sci USA 93:3021–3025PubMedCrossRefGoogle Scholar
  56. Rousset F, Raymond M (1995) Testing heterozygote excess and deficiency. Genetics 140:1413–1419PubMedGoogle Scholar
  57. Schluns H, Koeniger G, Koeniger N, Moritz RFA (2004) Sperm utilization pattern in the honeybee (Apis mellifera). Behav Ecol Sociobiol 56:458–463CrossRefGoogle Scholar
  58. Sokal RR, Rohlf FJ (1995) Biometry. W. H. Freeman and company, New YorkGoogle Scholar
  59. Tschinkel WR (1993) Sociometry and sociogenesis of colonies of the fire ant Solenopsis invicta during one annual cycle. Ecol Monogr 63:425–457CrossRefGoogle Scholar
  60. Tschinkel WR (1998) The reproductive biology of fire ant societies. Bioscience 48:593–605CrossRefGoogle Scholar
  61. Tsutsui ND, Suarez AV (2003) The colony structure and population biology of invasive ants. Conserv Biol 17:48–58CrossRefGoogle Scholar
  62. Valles SM, Porter SD (2003) Identification of polygyne and monogyne fire ant colonies (Solenopsis invicta) by multiplex PCR of Gp-9 alleles. Ins Soc 50:199–200CrossRefGoogle Scholar
  63. Vargo EL, Porter SD (1989) Colony reproduction by budding in the polygyne form of Solenopsis invicta (Hymenoptera: Formicidae). Ann Entomol Soc Am 82:307–313Google Scholar
  64. Vinson SB (1986) Economic impact and control of social insects. Praeger, New YorkGoogle Scholar
  65. Vinson SB (1997) Invasion of the red imported fire ant (Hymenoptera: Formicidae). Am Entomol 43:23–39Google Scholar
  66. Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370CrossRefGoogle Scholar
  67. Williams DF (1994) Exotic ants: biology, impact, and control of introduced species. Westview Press, BoulderGoogle Scholar
  68. Williamson M (1996) Biological invasions. Chapman and Hall, New YorkGoogle Scholar

Copyright information

© Springer Science+Business Media, Inc. 2006

Authors and Affiliations

  • Michael A. D. Goodisman
    • 1
  • Karen A. Sankovich
    • 1
  • Jennifer L. Kovacs
    • 1
  1. 1.School of BiologyGeorgia Institute of TechnologyAtlantaUSA

Personalised recommendations