Genetic clusters and sex-biased gene flow in a unicolonial Formica ant

BMC Evolutionary Biology

Volumn 9, Issue 1, 2009, Pages

  Holzer, Barbara ^a   Keller, Laurent ^a   Chapuisat, Michel ^a  

^a UNIVERSITY OF LAUSANNE   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

ANT; ARTICLE; COLONIAL SPECIES; GENDER BIAS; GENE CLUSTER; GENE FLOW; GENE STRUCTURE; GENETIC ANALYSIS; GENETIC HETEROGENEITY; GENETIC VARIABILITY; GENOTYPE; HAPLOTYPE; MITOCHONDRION; NONHUMAN; SEX DIFFERENCE; SRY GENE; ANIMAL; ANIMAL BEHAVIOR; BIOLOGY; DNA SEQUENCE; GENE; GENETIC MARKER; GENETIC POLYMORPHISM; GENETICS; MALE; POPULATION GENETICS; SOCIAL BEHAVIOR;

ANIMALIA; FORMICA; FORMICA PARALUGUBRIS; FORMICIDAE;

MICROSATELLITE DNA; MITOCHONDRIAL DNA;

ANIMALS; ANTS; BEHAVIOR, ANIMAL; COMPUTATIONAL BIOLOGY; DNA, MITOCHONDRIAL; GENE FLOW; GENES, INSECT; GENETIC MARKERS; GENETICS, POPULATION; HAPLOTYPES; MALE; MICROSATELLITE REPEATS; POLYMORPHISM, GENETIC; SEQUENCE ANALYSIS, DNA; SOCIAL BEHAVIOR;

EID: 65249177812     PISSN: None     EISSN: 14712148     Source Type: Journal    
DOI: 10.1186/1471-2148-9-69     Document Type: Article

References (84)

1. The genetical evolution of social behaviour. II. WD Hamilton, J Theor Biol 1964 7 17 52 10.1016/0022-5193(64)90039-6 5875340
2. Kin selection is the key to altruism. KR Foster T Wenseleers FLW Ratnieks, Trends Ecol Evol 2006 21 57 60 10.1016/j.tree.2005.11.020 16701471 (Pubitemid 43144374)
3. Ancestral monogamy shows kin selection is key to the evolution of eusociality. WOH Hughes BP Oldroyd M Beekman FLW Ratnieks, Science 2008 320 1213 1216 10.1126/science.1156108 18511689
4. Advanced eusociality, kin selection and male haploidy. RH Crozier, Aust J Entomol 2008 47 2 8 10.1111/j.1440-6055.2007.00621.x
5. The number of queens: an important trait in ant evolution. B Hölldobler EO Wilson, Naturwissenschaften 1977 64 8 15 10.1007/BF00439886
6. Kin selection and social insects. DC Queller JE Strassmann, Bioscience 1998 48 165 175 10.2307/1313262
7. Abandoning aggression but maintaining self-nonself discrimination as a first stage in ant supercolony formation. FM Steiner BC Schlick-Steiner K Moder C Stauffer W Arthofer A Buschinger X Espadaler E Christian K Einfinger E Lorbeer, Curr Biol 2007 17 1903 1907 10.1016/j.cub.2007.09.061 17964165 (Pubitemid 350019573)
8. Evolution of social insect colonies: sex allocation and kin selection. RH Crozier P Pamilo, Oxford: Oxford University Press 1996
9. Native supercolonies of unrelated individuals in the invasive Argentine ant. JS Pedersen MJB Krieger V Vogel T Giraud L Keller, Evolution 2006 60 782 791 16739459
10. Social life: the paradox of multiple-queen colonies. L Keller, Trends Ecol Evol 1995 10 355 360 10.1016/S0169-5347(00)89133-8
11. AFG Bourke NR Franks, Social evolution in ants Princeton: Princeton University Press 1995
12. Molecular ecology of social behaviour: analyses of breeding systems and genetic structure. KG Ross, Mol Ecol 2001 10 265 284 10.1046/j.1365-294x.2001. 01191.x 11298944 (Pubitemid 32232336)
13. Genetic relatedness in viscous populations. DC Queller, Evol Ecol 1994 8 70 73 10.1007/BF01237667 (Pubitemid 2036743)
14. Evolutionary explanations for cooperation. SA West AS Griffin A Gardner, Curr Biol 2007 17 R661 R672 10.1016/j.cub.2007.06.004 17714660 (Pubitemid 47259365)
15. Evolution of supercolonies: the Argentine ants of southern Europe. T Giraud JS Pedersen L Keller, Proc Natl Acad Sci USA 2002 99 6075 6079 11959924 10.1073/pnas.092694199 (Pubitemid 34493267)
16. Loss of intraspecific aggression in the success of a widespread invasive social insect. DA Holway AV Suarez TJ Case, Science 1998 282 949 952 10.1126/science.282.5390.949 9794767 (Pubitemid 28507529)
17. Reduced genetic variation and the success of an invasive species. ND Tsutsui AV Suarez DA Holway TJ Case, Proc Natl Acad Sci USA 2000 97 5948 5953 10811892 10.1073/pnas.100110397 (Pubitemid 30367504)
18. Assessing genetic structure with multiple classes of molecular markers: A case study involving the introduced fire ant Solenopsis invicta. KG Ross DD Shoemaker MJB Krieger CJ DeHeer L Keller, Mol Biol Evol 1999 16 525 543 10331278 (Pubitemid 29190959)
19. Experimental evidence of large-scale unicoloniality in the tramp ant Wasmannia auropunctata (Roger). J Le Breton JHC Delabie J Chazeau A Dejean H Jourdan, J Insect Behav 2004 17 263 271 10.1023/B:JOIR.0000028575.28700.71 (Pubitemid 39001192)
20. Intercontinental chemical variation in the invasive ant Wasmannia auropunctata (Roger) (Hymenoptera Formicidae): a key to the invasive success of a tramp species. C Errard J Delabie H Jourdan A Hefetz, Naturwissenschaften 2005 92 319 323 10.1007/s00114-005-0628-y 15973547 (Pubitemid 41187668)
21. Seasonal polydomy and unicoloniality in a polygynous population of the red wood ant Formica truncorum. M Elias R Rosengren L Sundström, Behav Ecol Sociobiol 2005 57 339 349 10.1007/s00265-004-0864-8 (Pubitemid 40564283)
22. Microsatellites reveal high population viscosity and limited dispersal in the ant Formica paralugubris. M Chapuisat J Goudet L Keller, Evolution 1997 51 475 482 10.2307/2411120 (Pubitemid 27205144)
23. Influence of a supercolonial ant Formica (Formica) yessensis Forel on the distribution of other ants in Ishikari Coast. S Higashi K Yamauchi, Jap J Ecol 1979 29 257 264
24. The evolution of polygyny and polydomy in mound-building Formica ants. R Rosengren P Pamilo, Acta Entomol Fennica 1983 42 65 77
25. Contrasting population genetic structure for workers and queens in the putatively unicolonial ant Formica exsecta. R Kümmerli L Keller, Mol Ecol 2007 16 4493 4503 10.1111/j.1365-294X.2007.03514.x 17868291 (Pubitemid 47620522)
26. Sociobiological studies of the polygynic ant Lasius sakagami. 1 General features of its polydomous system. K Yamauchi K Kinomura S Miyake, Ins Soc 1981 28 279 296 10.1007/BF02223629
27. Gene flow and population viscosity in Myrmica ants. P Seppä P Pamilo, Heredity 1995 74 200 209 10.1038/hdy.1995.28 (Pubitemid 26447078)
28. Sociogenetic organization of the red ant Myrmica rubra. P Seppä L Walin, Behav Ecol Sociobiol 1996 38 207 217 10.1007/s002650050234 (Pubitemid 3043887)
29. Convergent development of low-relatedness supercolonies in Myrmica ants. T van der Hammen JS Pedersen JJ Boomsma, Heredity 2002 89 83 89 10.1038/sj.hdy.6800098 12136409
30. Genetic analysis of colony structure in polydomous and polygynous ant populations. JS Pedersen JJ Boomsma, Biol J Linn Soc 1999 66 115 144 10.1111/j.1095-8312.1999.tb01919.x (Pubitemid 29096729)
31. First record of unicolonial polygyny in Tetramorium cf. caespitum (Hymenoptera, Formicidae). FM Steiner BC Schlick-Steiner A Buschinger, Ins Soc 2003 50 98 99 10.1007/s000400300015 (Pubitemid 36333375)
32. Social and genetic structure of a supercolonial weaver ant, Polyrhachis robsoni, with dimorphic queens. JS van Zweden ME Carew MT Henshaw SKA Robson RH Crozier, Ins Soc 2007 54 34 41 10.1007/s00040-007-0909-x
33. Unicoloniality, recognition and genetic differentiation in a native Formica ant. B Holzer M Chapuisat N Kremer C Finet L Keller, J Evol Biol 2006 19 2031 2039 10.1111/j.1420-9101.2006.01133.x 17040400 (Pubitemid 44571641)
34. Population viscosity can promote the evolution of altruistic sterile helpers and eusociality. L Lehmann V Ravigné L Keller, Proc R Soc B 2008 275 1887 1895 10.1098/rspb.2008.0276 18460428
35. F Rousset, Genetic structure and selection in subdivided populations Princeton: Princeton University Press 2004
36. Altruism in viscous populations - an inclusive fitness model. PD Taylor, Evol Ecol 1992 6 352 356 10.1007/BF02270971
37. Kin selection: fact and fiction. AS Griffin SA West, Trends Ecol Evol 2002 17 15 21 10.1016/S0169-5347(01)02355-2 (Pubitemid 34076722)
38. Note préliminaire sur la structure, la phénologie et le régime alimentaire d'une super-colonie de Formica lugubris Zett. D Cherix, Ins Soc 1980 27 226 236 10.1007/BF02223666
39. Pseudogynes (= sécrétergates) et répartition des individus l'intérieur d'une fourmilière de Formica lugubris Zett. (Hymenoptera: Formicidae). D Cherix, Ins Soc 1983 30 184 192 10.1007/BF02223868
40. Worker reproduction in Formica ants. H Helanterä L Sundström, Am Nat 2007 170 E14 E25 10.1086/518185 17853986
41. Alternative reproductive strategies in Formica lugubris Zett. (Hymenoptera Formicidae). D Cherix D Chautems DJC Fletcher W Fortelius G Gris L Keller L Passera R Rosengren EL Vargo F Walter, Ethol Ecol Evol 1991 Special Issue 1 61 66
42. Extended family structure in the ant Formica paralugubris : the role of the breeding system. M Chapuisat L Keller, Behav Ecol Sociobiol 1999 46 405 412 10.1007/s002650050636
43. A test of queen recruitment models using nuclear and mitochondrial markers in the fire ant Solenopsis invicta. MAD Goodisman KG Ross, Evolution 1998 52 1416 1422 10.2307/2411311 (Pubitemid 28537251)
44. Coexistence of the social types: Genetic population structure in the ant Formica exsecta. P Seppä M Gyllenstrand J Corander P Pamilo, Evolution 2004 58 2462 2471 15612289 (Pubitemid 39548063)
45. Inferring sex-biased dispersal from population genetic tools: a review. F Prugnolle T de Meeus, Heredity 2002 88 161 165 10.1038/sj.hdy.6800060 11920116 (Pubitemid 34287134)
46. Perspective: Highly variable loci and their interpretation in evolution and conservation. PW Hedrick, Evolution 1999 53 313 318 10.2307/2640768 (Pubitemid 29239704)
47. A standardized genetic differentiation measure. PW Hedrick, Evolution 2005 59 1633 1638 16329237 (Pubitemid 41266769)
48. Indirect measures of gene flow and migration: F ST 1/(4Nm+1). MC Whitlock DE McCauley, Heredity 1999 82 117 125 10.1038/sj.hdy.6884960 10098262
49. Nestmate recognition in the unicolonial ant Formica paralugubris. M Chapuisat C Bernasconi S Hoehn M Reuter, Behav Ecol 2005 16 15 19 10.1093/beheco/arh128 (Pubitemid 40112936)
50. Computer programs for population genetics data analysis: a survival guide. L Excoffier G Heckel, Nature Reviews Genetics 2006 7 745 758 10.1038/nrg1904 16924258 (Pubitemid 44413219)
51. The Bayesian revolution in genetics. MA Beaumont B Rannala, Nature Reviews Genetics 2004 5 251 261 10.1038/nrg1318 15131649 (Pubitemid 38435621)
52. A spatial statistical model for landscape genetics. G Guillot A Estoup F Mortier JF Cosson, Genetics 2005 170 1261 1280 15520263 10.1534/genetics.104. 033803 (Pubitemid 41105481)
53. Colony fission affects kinship in a social insect. P Seppä I Fernandez-Escudero N Gyllenstrand P Pamilo, Behav Ecol Sociobiol 2008 62 589 597 10.1007/s00265-007-0483-2
54. Nestmate recognition and the genetic relatedness of nests in the ant Formica pratensis. M Beye P Neumann M Chapuisat P Pamilo RFA Moritz, Behav Ecol Sociobiol 1998 43 67 72 10.1007/s002650050467 (Pubitemid 28320582)
55. Does population viscosity promote kin selection? DC Queller, Trends Ecol Evol 1992 7 322 324 10.1016/0169-5347(92)90120-Z
56. Cooperation and competition in pathogenic bacteria. AS Griffin SA West A Buckling, Nature 2004 430 1024 1027 10.1038/nature02744 15329720 (Pubitemid 39128386)
57. Stay or drift? Queen acceptance in the ant Formica paralugubris. B Holzer J Meunier L Keller M Chapuisat, Ins Soc 2008 55 392 396 10.1007/s00040-008- 1017-2
58. Mating frequency of ant queens with alternative dispersal strategies, as revealed by microsatellite analysis of sperm. M Chapuisat, Mol Ecol 1998 7 1097 1105 10.1046/j.1365-294x.1998.00422.x (Pubitemid 28428488)
59. Attraction of the sexes in Formica lugubris Zett. (Hymenoptera: Formicidae). D Cherix DJC Fletcher D Chautems W Fortelius G Gris L Keller R Rosengren E Vargo F Walter, Ins Soc 1993 40 319 324 10.1007/BF01242368
60. Genetic differentiation of disjunct populations of the ants Formica aquilonia and Formica lugubris in Europe. P Pamilo D Chautems D Cherix, Ins Soc 1992 39 15 29 10.1007/BF01240528 (Pubitemid 23149228)
61. Genetic population structure and dispersal patterns in Formica ants - a review. L Sundström P Seppä P Pamilo, Ann Zool Fenn 2005 42 163 177 (Pubitemid 40982716)
62. Mitochondrial markers in the ant Leptothorax rugatulus reveal the population genetic consequences of female philopatry at different hierarchical levels. O Rüppell M Stratz B Baier J Heinze, Mol Ecol 2003 12 795 801 10.1046/j.1365-294X.2003.01769.x 12675834 (Pubitemid 36380437)
63. Obligatory female philopatry affects genetic population structure in the ant Proformica longiseta. P Seppä I Fernandez-Escudero N Gyllenstrand P Pamilo, Ins Soc 2006 53 362 368 10.1007/s00040-006-0882-9 (Pubitemid 44141166)
64. Queen number in colonies of social Hymenoptera as a kin-selected adaptation. P Nonacs, Evolution 1988 42 566 580 10.2307/2409040 (Pubitemid 19322067)
65. Alternative reproductive strategies: a queen perspective in ants. J Heinze L Keller, Trends Ecol Evol 2000 15 508 512 10.1016/S0169-5347(00)01995-9 11114438
66. Restricted effective queen dispersal at a microgeographic scale in polygynous populations of the ant Formica exsecta. C Liautard L Keller, Evolution 2001 55 2484 2492 11831664 (Pubitemid 34115681)
67. The influence of sociality on the conservation biology of social insects. RE Chapman AFG Bourke, Ecol Lett 2001 4 650 662 10.1046/j.1461-0248.2001.00253. x (Pubitemid 33105379)
68. Social evolution: pathways to ant unicoloniality. DE Jackson, Curr Biol 2007 17 R1063 R1064 10.1016/j.cub.2007.10.031 18088593 (Pubitemid 350236853)
69. Ecology and evolution of social organization: insights from fire ants and other highly eusocial insects. KG Ross L Keller, Annu Rev Ecol Syst 1995 26 631 656 10.1146/annurev.es.26.110195.003215 (Pubitemid 3019642)
70. Polydomy in ants: what we know, what we think we know, and what remains to be done. G Debout B Schatz M Elias D McKey, Biol J Linn Soc 2007 90 319 348 10.1111/j.1095-8312.2007.00728.x (Pubitemid 46192771)
71. Colony-structure variation and interspecific competitive ability in the invasive Argentine ant. DA Holway AV Suarez, Oecologia 2004 138 216 222 10.1007/s00442-003-1414-1 14566557 (Pubitemid 38162229)
72. Characterization of microsatellite loci in Formica lugubris B and their variability in other ant species. M Chapuisat, Mol Ecol 1996 5 599 601 10.1111/j.1365-294X.1996.tb00354.x 8794567 (Pubitemid 27108423)
73. Polymorphic microsatellite DNA markers in the ant Formica exsecta. N Gyllenstrand PJ Gertsch P Pamilo, Mol Ecol Notes 2002 2 67 69 10.1046/j.1471-8286.2002.00152.x (Pubitemid 34287116)
74. Long sections of mitochondrial DNA amplified from fourteen orders of insects using conserved polymerase chain reaction primers. RL Roehrdanz ME Degrugillier, Ann Entomol Soc Am 1998 91 771 778 (Pubitemid 128652263)
75. The mitochondrial genome of the honeybee Apis mellifera : complete sequence and genome organization. RH Crozier YC Crozier, Genetics 1993 133 97 117 8417993 (Pubitemid 23011400)
76. GENELAND: a computer package for landscape genetics. G Guillot F Mortier A Estoup, Mol Ecol Notes 2005 5 712 715 10.1111/j.1471-8286.2005.01031.x (Pubitemid 41716893)
77. Inference of population structure using multilocus genotype data. JK Pritchard M Stephens P Donnelly, Genetics 2000 155 945 959 10835412 (Pubitemid 30397141)
78. Estimating relatedness using genetic markers. DC Queller KF Goodnight, Evolution 1989 242 258 275 10.2307/2409206
79. A step-by-step tutorial to use HierFstat to analyse populations hierarchically structured at multiple levels. T de Meeus J Goudet, Infection Genetics and Evolution 2007 7 731 735 10.1016/j.meegid.2007.07.005 (Pubitemid 350010603)
80. HIERFSTAT, a package for R to compute and test hierarchical F -statistics. J Goudet, Mol Ecol Notes 2005 5 184 186 10.1111/j.1471-8286.2004. 00828.x (Pubitemid 40350918)
81. Arlequin: a software for population genetics data analysis, version 2.000. S Schneider D Roessli L Excoffier, Genetics and Biometry Lab, Dept. of Anthropology, University of Geneva 2.000 2000
82. Estimating the relative rates of pollen and seed migration among plant populations. RA Ennos, Heredity 1994 72 250 259 10.1038/hdy.1994.35 (Pubitemid 2057321)
83. The genetical structure of populations. S Wright, Ann Eug 1951 15 323 354
84. The infinite island model with sex-differentiated gene flow. LM Berg M Lascoux P Pamilo, Heredity 1998 81 63 68 10.1046/j.1365-2540.1998.00358.x (Pubitemid 28351537)