Abstract
Invasive species are one of the main reasons for the ongoing global loss of biodiversity. Anoplolepis gracilipes is an invasive ant that has recently received significant attention due to its negative effect on the native fauna and flora of Christmas Island, Indian Ocean. This species has contributed to a drastic change in the structure of the Christmas Island rainforest through its negative impact on the island’s endemic red land crab, the dominant consumer on the islands forest floor. In this study, we investigate the population structure of A. gracilipes on Christmas Island in order to determine whether multiple introductions occurred on the island and how they correspond to known infestations. We genotyped 578 individuals collected from 50 nests across the Island. We identify two distinct subgroups in the population that represent two different supercolonies. These supercolonies are interspersed across the island, however both nuclear (microsatellites) and mitochondrial markers strongly suggest that there is no gene flow between the two colonies. Significant heterozygote excess within the entire sampling area, with all but one worker examined being heterozygous for all seven microsatellite loci, suggests an unusual reproductive system in these ants. Our results are consistent with recent sociogenetic findings in a population of A. gracilipes in Northern Borneo.
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References
Abbott KL (2005) Supercolonies of the invasive yellow crazy ant, Anoplolepis gracilipes, on an oceanic island: forager activity patterns, density and biomass. Insectes Soc 52:266–273. doi:10.1007/s00040-005-0800-6
Abbott KL (2006) Spatial dynamics of supercolonies of the invasive yellow crazy ant, Anoplolepis gracilipes, on Christmas Island, Indian Ocean. Divers Distrib 12:101–110. doi:10.1111/j.1366-9516.2006.00193.x
Abbott KL, Green PT (2007) Collapse of an ant-scale mutualism in a rainforest on Christmas Island. Oikos 116:1238–1246. doi:10.1111/j.0030-1299.2007.15629.x
Abbott KL, Greaves SNJ, Ritchie PA, Lester PJ (2007) Behaviourally and genetically distinct populations of an invasive ant provide insight into invasion history and impacts on a tropical ant community. Biol Invasions 9:453–463. doi:10.1007/s10530-006-9052-2
Causton CE, Sevilla CR, Porter SD (2005) Eradication of the little fire ant, Wasmannia auropunctata (Roger) (Hymenoptera: Formicidae), from Marchena Island, Galapàgos: on the edge of success? Fla Entomol 8:159–167. doi:10.1653/0015-4040(2005)088[0159:EOTLFA]2.0.CO;2
Claussen J (2005) Native plants of Christmas Island. Flora Aust Suppl Ser 22:1–146
Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1659. doi:10.1046/j.1365-294x.2000.01020.x
Crawley WC (1915) Ants from north and south-west Australia (G.F. Hill, Rowland Turner) and Christmas Island, Straits Settlements. Part II. Annu Mag Nat Hist 15:232–239
Crozier RH, Crozier YC (1993) The mitochondrial genome of the honeybee Apis mellifera—complete sequence and genome organization. Genetics 133:97–117
Crozier RH, Koulinanos S, Crozier YC (1991) An improved test for Africanized honey bee mitochondrial DNA. Experientia 47:968–969. doi:10.1007/BF01929894
Dejean A, Le Breton J, Suzzoni J, Orivel J, Saux-Moreau C (2005) Influence of interspecific competition on the recruitment behavior and liquid food transport in the tramp ant species Pheidole megacephala. Naturwissenschaften 92:324–327. doi:10.1007/s00114-005-0632-2
Donisthorpe H (1935) The ants of Christmas Island. Annu Mag Nat Hist 10:629–635
Drescher J, Blüthgen N, Feldhaar H (2007) Population structure and intraspecific aggression in the invasive ant species Anoplolepis gracilipes in Malaysian Borneo. Mol Ecol 16:1453–1465. doi:10.1111/j.1365-294X.2007.03260.x
Errard C, Delabie J, Jourdan H, Hefetz A (2005) Intercontinental chemical variation in the invasive ant Wasmannia auropunctata (Roger) (Hymenoptera Formicidae): a key to the invasive success of a tramp species. Naturwissenschaften 92:319–323. doi:10.1007/s00114-005-0628-y
Falush D, Stephens M, Pritchard JK (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164:1567–1587
Feldhaar H, Drescher J, Blüthgen N (2006) Characterization of microsatellite markers for the invasive ant species Anoplolepis gracilipes. Mol Ecol Notes 6:912–914. doi:10.1111/j.1471-8286.2006.01397.x
Framenau VW, Thomas ML (2008) The ants of Christmas Island (Hymenoptera: Formicidae). Rec W Aust Mus 25:45–86
Giraud T, Pedersen JS, Keller L (2002) Evolution of supercolonies: the Argentine ants of southern Europe. Proc Natl Acad Sci USA 99:6075–6079. doi:10.1073/pnas.092694199
Goudet J (1995) FSTAT (version 1.2): a computer program to calculate F-statistics. J Hered 86:485–486
Goudet J (2001) Fstat, a program to estimate and test gene diversities and fixation indices (version 2.9.3). Updated from Goudet (1995). Department of Ecology and Evolution, University of Lausanne, Lausanne
Gutrich JJ, VanGelder E, Loope L (2007) Potential economic impact of introduction and spread of the red imported fire ant, Solenopsis invicta, in Hawaii. Environ Sci Pol 10:685–696
Hall TA (1999) BioEdit: a user-friendly biological sequence alignement editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98
Holway D, Suarez AV (2006) Homogenization of ant communities in mediterranean California: the effects of urbanization and invasion. Biol Conserv 127:319–326. doi:10.1016/j.biocon.2005.05.016
Holway DA, Suarez AV, Case TJ (1998) Loss of intraspecific aggression in the success of a widespread invasive social insect. Science 282:949–951. doi:10.1126/science.282.5390.949
Holway DA, Lach L, Suarez AV, Tsutsui ND, Case TJ (2002) The causes and consequences of ant invasions. Annu Rev Ecol Syst 33:181–233. doi:10.1146/annurev.ecolsys.33.010802.150444
Human KG, Gordon DM (1999) Behavioral interactions of the invasive Argentine ant with native ant species. Insectes Soc 46:159–163. doi:10.1007/s000400050127
Jaquiery J, Vogel V, Keller L (2005) Multilevel genetic analyses of two European supercolonies of the Argentine ant, Linepithema humile. Mol Ecol 14:589–598. doi:10.1111/j.1365-294X.2005.02433.x
Lard C, Willis DB, Salin V, Robinson S (2002) Economic assessments of red imported fire ant on Texas’ urban and agricultural sectors. Southwest Entomol 25(Suppl):123–137
Moller H (1996) Lessons for invasion theory from social insects. Biol Conserv 78:125–142. doi:10.1016/0006-3207(96)00022-5
O’Dowd DJ, Green PT, Lake PS (2003) Invasional ‘meltdown’ on an oceanic island. Ecol Lett 6:812–817. doi:10.1046/j.1461-0248.2003.00512.x
Pedersen JS, Krieger MJB, Vogel V, Giraud T, Keller L (2006) Native supercolonies of unrelated individuals in the invasive argentine ant. Evol Int J Org Evol 60:782–791
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959
Queller DC, Goodnight KF (1989) Estimating relatedness using genetic markers. Evol Int J Org Evol 43:258–275. doi:10.2307/2409206
Raymond M, Rousset F (1995) Genepop (version-1.2)—population genetics software for exact tests and ecumenicism. J Hered 86:248–249
Rice WR (1989) Analyzing tables of statistical tests. Evol Int J Org Evol 43:223–225. doi:10.2307/2409177
Ross KG, Fletcher DJC (1985) Genetic origin of male diploidy in the fire ant, Solenopsis invicta (Hymenoptera, Formicidae), and its evolutionary significance. Evol Int J Org Evol 39:888–903. doi:10.2307/2408688
Sakai AK, Allendorf FW, Holt JS, Lodge DM, Molofsky J, With KA, Baughman S, Cabin RJ, Cohen JE, Ellstrand NC, McCauley DE, O’Neil P, Parker IM, Thompson JN, Weller SG (2001) The population biology of invasive species. Annu Rev Ecol Syst 32:305–332. doi:10.1146/annurev.ecolsys.32.081501.114037
Sanders NJ, Gotelli NJ, Heller NE, Gordon DM (2003) Community disassembly by an invasive species. Proc Natl Acad Sci USA 100:2474–2477. doi:10.1073/pnas.0437913100
Silverman J, Brightwell RJ (2008) The Argentine ant: challenges in managing an invasive unicolonial pest. Annu Rev Entomol 53:231–252. doi:10.1146/annurev.ento.53.103106.093450
Simberloff D, Gibbons L (2004) Now you see them, now you don’t—population crashes of established introduced species. Biol Invasions 6:161–172. doi:10.1023/B:BINV.0000022133.49752.46
Slatkin M (1985) Rare alleles as indicators of gene flow. Evol Int J Org Evol 39:53–65. doi:10.2307/2408516
Thomas ML, Payne-Makrisâ CM, Suarez AV, Tsutsui ND, Holway DA (2006) When supercolonies collide: territorial aggression in an invasive and unicolonial social insect. Mol Ecol 15:4303–4315. doi:10.1111/j.1365-294X.2006.03038.x
Tsutsui ND, Suarez AV (2003) The colony structure and population biology of invasive ants. Conserv Biol 17:48–58. doi:10.1046/j.1523-1739.2003.02018.x
Zayed A, Packer L (2005) Complementary sex determination substantially increases extinction proneness of haplodiploid populations. Proc Natl Acad Sci USA 102:10742–10746. doi:10.1073/pnas.0502271102
Acknowledgments
We thank two anonymous reviewers for helpful comments on the manuscript. Special thanks to the following PANCI staff for help with fieldwork; Haddis Alpisal, Lauren Barrow, Nicolas Chapellon, Claire Davies, Gary Foo, David James, John Jaycock, Mick Jeffreys, Ruth Marr, Imran Pereira and Kent Retallick. Field work was funded by Parks Australia North, Christmas Island. Laboratory work was funded by the German Research Foundation (DFG) Priority program SFB 554 “Arthropod behavior” project E2.
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Thomas, M.L., Becker, K., Abbott, K. et al. Supercolony mosaics: two different invasions by the yellow crazy ant, Anoplolepis gracilipes, on Christmas Island, Indian Ocean. Biol Invasions 12, 677–687 (2010). https://doi.org/10.1007/s10530-009-9473-9
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DOI: https://doi.org/10.1007/s10530-009-9473-9