Review. Lifelong commitment to the wrong partner: Hybridization in ants

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 363, Issue 1505, 2008, Pages 2891-2899

  Feldhaar, Heike ^a   Foitzik, Susanne ^b   Heinze, Jürgen ^c  

^a UNIVERSITY OF WÜRZBURG   (Germany)

^b UNIVERSITY OF MUNICH   (Germany)

^c UNIVERSITY OF REGENSBURG   (Germany)

Author keywords

Caste determination; Evolutionary arms races; Levels of selection; Mating biology; Sperm theft

Indexed keywords

ALLOPATRY; ANT; ARMS RACE; CONSPECIFIC; FITNESS; HYBRIDIZATION; MATE CHOICE; MORPHOLOGY; QUEEN; REPRODUCTIVE ISOLATION; SEX DETERMINATION; SEXUAL CONFLICT; SOCIAL INSECT; WORKER CASTE;

FORMICIDAE; HEXAPODA;

EID: 48749110024     PISSN: 09628436     EISSN: None     Source Type: Journal    
DOI: 10.1098/rstb.2008.0022     Document Type: Review

References (70)

1. Abell, A. J., Cole, B. J., Reyes, R. & Wiernasz, D. C. 1999 Sexual selection on body size and shape in the western harvester ant, Pogonomyrmex occidentalis Cresson. Evolution 53, 535-545. (doi:10.2307/2640789)
2. Anderson, K. E., Gadau, J., Mott, B. M., Johnson, R. A., Altamirano, A., Strehl, C. & Fewell, J. H. 2006 Distribution and evolution of genetic caste determination in Pogonomyrmex seed-harvester ants. Ecology 87, 2171-2184. (doi:10.1890/0012-9658(2006)87[2171:DAEOGC]2.0.CO;2)
3. Arnqvist, G. & Rowe, L. 2005 Sexual conflict. Princeton, NJ: Princeton University Press.
4. Baldridge, R. S., Rettenmeyer, C. W. & Watkins, J. F. I. 1980 Seasonal, nocturnal and diurnal flight periodicities of Nearctic army ant males (Hymenoptera: Formicidae). J. Kans. Entomol. Soc. 43, 189-204.
5. Boomsma, J. J., Baer, B. & Heinze, J. 2005 The evolution of male traits in social insects. Annu. Rev. Entomol. 50, 395-420. (doi:10.1146/annurev.ento.50.071803.130416)
6. Brandt, M., Foitzik, S., Fischer-Blass, B. & Heinze, J. 2005 The coevolutionary dynamics of obligate ant social parasite system - between prudence and antagonism. Biol. Rev. 80, 251-267. (doi:10.1017/S1464793104006669)
7. Buschinger, A. 1972 Kreuzung zweier sozialparasitischer Ameisenarten, Doronomyrmex pacis Kutter und Leptothorax kutteri Buschinger (Hym., Formicidae). Zool. Anz. 189, 169-179.
8. Buschinger, A. 2001 Multiple Hybridisierung von Arten der Ameisen-Gattung Epimyrma (Hymenoptera: Formicidae), und Beobachtungen zur Ausbeutung der Wirtsarten durch die Parasiten. Myrmecol. Nachr. 4, 25-35.
9. Clark, R. M., Anderson, K. E., Gadau, J. & Fewell, J. H. 2006 Behavioral regulation of genetic caste determination in a Pogonomyrmex population with dependent lineages. Ecology 87, 2201-2206. (doi:10.1890/0012-9658(2006)87[2201:BROGCD]2.0.CO;2)
10. Davidson, D. A. 1982 Sexual selection in harvester ants (Hymenoptera: Formicidae: Pogonomyrmex). Behav. Ecol. Sociobiol. 10, 245-250. (doi:10.1007/BF00302813)
11. Douwes, P. & Stille, B. 1991 Hybridization and variation in the Leptothorax tuberum group (Hymenoptera, Formicidae). Z. Zool. Syst. Evolutionsforsch. 29, 165-175.
12. Dunn, R. R., Parker, C. R., Geraghty, M. & Sanders, N. J. 2007 Reproductive phenologies in a diverse temperate ant fauna. Ecol. Entomol. 32, 135-142.
13. Eidmann, H. 1942 Die Überwinterung der Ameisen. Z. Morphol. Oekol. Tiere 39, 217-275. (doi:10.1007/BF00684467)
14. Feldhaar, H., Fiala, B., Gadau, J., Maryati, M. & Maschwitz, U. 2003 Molecular phylogeny of Crematogaster subgenus Decacrema ants (Hymenoptera: Formicidae) and the colonization of Macaranga (Euphorbiaceae) trees. Mol. Phylogenet. Evol. 27, 441-452. (doi:10.1016/S1055-7903(02)00449-9)
15. Foitzik, S. & Heinze, J. 2000 Intraspecific parasitism and split sex ratios in a monogynous and monandrous ant (Leptothorax nylanderi). Behav. Ecol. Sociobiol. 47, 424-431. (doi:10.1007/s002650050686)
16. Fournier, D., Estoup, A., Orivel, R. M., Foucaud, J., Jourdan, H., Le Breton, J. & Keller, L. 2005 Clonal reproduction by males and females in the little fire ant. Nature 435, 1230-1234. (doi:10.1038/nature03705)
17. Goropashnaya, A. V., Fedorov, V. B. & Pamilo, P. 2004 Recent speciation in the Formica rufa group ants (Hymenoptera, Formicidae): inference from mitochondrial DNA phylogeny. Mol. Phylogenet. Evol. 32, 198-206. (doi:10.1016/j.ympev.2003.11.016)
18. Hammond, R. L. & Keller, L. 2004 Conflict over male parentage in social insects. PLoS Biol. 2, 1472-1482. (doi:10.1371/journal. pbio.0020248)
19. Heinze, J. & Buschinger, A. 1989 Queen polymorphism in Leptothorax spec. A: its genetic and ecological background (Hymenoptera, Formicidae). Insect. Soc. 36, 139-155. (doi:10.1007/BF02225909)
20. Helms Cahan, S. H. & Keller, L. 2003 Complex hybrid origin of genetic caste determination in harvester ants. Nature 424, 306-309. (doi:10.1038/nature01744)
21. Helms Cahan, S. H. & Vinson, S. B. 2003 Reproductive division of labor between hybrid and nonhybrid offspring in a fire ant hybrid zone. Evolution 57, 1562-1570.
22. Helms Cahan, S., Parker, J. D., Rissing, S. W., Johnson, R. A., Polony, T. S., Weiser, M. D. & Smith, D. R. 2002 Extreme genetic differences between queens and workers in hybridizing Pogonomyrmex harvester ants. Proc. R. Soc. B 269, 1871-1877. (doi:10.1098/rspb.2002.2061)
23. Helms Cahan, S. H., Julian, G. E., Rissing, S. W., Schwander, T., Parker, J. D. & Keller, L. 2004 Loss of phenotypic plasticity generates genotype-caste association in harvester ants. Curr. Biol. 14, 2277-2282. (doi:10.1016/j.cub.2004.12.027)
24. Helms Cahan, S. H., Julian, G. E., Schwander, T. & Keller, L. 2006 Reproductive isolation between Pogonomyrmex rugosus and two lineages with genetic caste determination. Ecology 87, 2160-2170. (doi:10.1890/0012-9658(2006)87[2160:RIBPRA]2.0.CO;2)
25. Hölldobler, B. 1966 Futterverteilung durch Männchen in Ameisenstaat. Z. Vgl. Physiol. 52, 430-455. (doi:10.1007/ BF00302295)
26. Hölldobler, B. 1976 The behavioral ecology of mating in harvester ants (Hymenoptera: Formicidae: Pogonomyrmex). Behav. Ecol. Sociobiol. 1, 405-423. (doi:10.1007/BF00299401)
27. Hölldobler, B. & Bartz, S. H. 1985 Sociobiology of reproduction in ants. In Experimental behavioral ecology and sociobiology, vol. 31 (eds B. Hölldobler & M. Lindauer), pp. 237-257. Sunderland, MA: Sinauer Associates.
28. Howard, R. W. & Blomquist, G. J. 2005 Ecological, behavioral, and biochemical aspects of insect hydrocarbons. Annu. Rev. Entomol. 50, 371-393. (doi:10.1146/annurev.ento.50.071803.130359)
29. Hung, A. C. F. & Vinson, S. B. 1977 Interspecific hybridization and caste specificity of protein in fire ant. Science 196, 1458-1460. (doi:10.1126/science.196.4297.1458)
30. James, S. S., Pereira, R. M., Vail, K. M. & Ownley, B. H. 2002 Survival of imported fire ant (Hymenoptera: Formicidae) species subjected to freezing and near-freezing temperatures. Environ. Entomol. 31, 127-133.
31. Jessen, K. & Klinkicht, M. 1990 Hybridization in the social parasitic ant genus Epimyrma (Hymenoptera, Formicidae). Insect. Soc. 37, 273-293. (doi:10.1007/BF02225993)
32. Julian, G. E., Fewell, J. H., Gadau, J., Johnson, R. A. & Larrabee, D. 2002 Genetic determination of the queen caste in an ant hybrid zone. Proc. Natl Acad. Sci. USA 99, 8157-8160. (doi:10.1073/pnas.112222099)
33. Keller, L. 1999 Levels of selection in evolution. Princeton, NJ: Princeton University Press.
34. Lahav, S., Soroker, V., Hefetz, A. & Vander Meer, R. K. 1999 Direct behavioral evidence for hydrocarbons as ant recognition discriminators. Naturwissenschaften 86, 246-249. (doi:10.1007/s001140050609)
35. Linksvayer, T. A., Wade, M. J. & Gordon, D. M. 2006 Genetic caste determination in harvester ants: possible origin and maintenance by cyto-nuclear epistasis. Ecology 87, 2185-2193. (doi:10.1890/0012-9658(2006) 87[2185:GCDIHA]2.0.CO;2)
36. McCluskey, E. S. 1992 Periodicity and diversity in ant mating flights. Comput. Biochem. Physiol. A 103, 241-243. (doi:10.1016/0300- 9629(92)90574-A)
37. Nonacs, P. 2006 The ecology and evolution of hybridization in ants. Ecology 87, 2141-2142. (doi:10.1890/0012-9658(2006)87[2141:TEAEOH] 2.0.CO;2)
38. Oberstadt, B. & Heinze, J. 2003 Mating biology and population structure of the ant, Leptothorax gredleri. Insect. Soc. 50, 340-345. (doi:10.1007/s00040-003-0681-5)
39. Ohkawara, K., Nakayama, M., Satoh, A., Trindl, A. & Heinze, J. 2006 Clonal reproduction and genetic caste differences in a queen-polymorphic ant, Vollenhovia emeryi. Biol. Lett. 2, 359-363. (doi:10.1098/rsbl. 2006.0491)
40. Orr, H. A. 1997 Haldane's rule. Annu. Rev. Ecol. Syst. 28, 195-218. (doi:10.1146/annurev.ecolsys.28.1.195)
41. Orr, H. A. & Presgraves, D. C. 2000 Speciation by postzygotic isolation: forces, genes and molecules. Bioessays 22, 1085-1094. (doi:10.1002/1521-1878(200012)22:12〈1085::AID-BIES6〉3.0.CO;2-G)
42. 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. (doi:10.1126/science.1105453)
43. Pearson, B. 1983a The classification of morphologically intermediate ants in the Lasius alienus/Lasius niger taxon - further observations. Insect. Soc. 30, 100-105. (doi:10.1007/BF02225660)
44. Pearson, B. 1983b Hybridization between the ant species Lasius niger and Lasius alienus - the genetic evidence. Insect. Soc. 30, 402-411. (doi:10.1007/BF02223971)
45. Plateaux, L. 1978 L'essaimage de quelques fourmis Leptothorax: rôles de l'éclairement et de divers autres facteurs. Effet sur l'isolement reproductif et la répartition géographique. 1re partie, I à VI. Ann. Sci. Nat. Zool. Biol. Anim. 20, 129-164.
46. Plateaux, L. 1979 Ovarian polymorphism of queens in Leptothorax ants and interspecific variations: inferiority of interspecific hybrids. Arch. Zool. Exp. Gen. 120, 381-398.
47. Pusch, K., Heinze, J. & Foitzik, S. 2006a The influence of hybridization on colony structure in the ant species Temnothorax nylanderi and T. crassispinus. Insect. Soc. 53, 439-445. (doi:10.1007/s00040-005-0891-8)
48. Pusch, K., Seifert, B., Foitzik, S. & Heinze, J. 2006b Distribution and genetic divergence of two parapatric sibling ant species in Central Europe. Biol. J. Linn. Soc. 88, 223-234. (doi:10.1111/j.1095-8312.2006.00618.x)
49. Ross, K. G. & Robertson, J. L. 1990 Developmental stability, heterozygosity, and fitness in two introduced fire ants (Solenopsis invicta and Solenopsis richteri) and their hybrid. Heredity 64, 93-103. (doi:10.1038/hdy.1990.12)
50. Ross, K. G. & Shoemaker, D. D. 2005 Species delimitation in native South American fire ants. Mol. Ecol. 14, 3419-3438. (doi:10.1111/j.1365-294X.2005.02661.x)
51. Ross, K. G., Vander Meer, R. K., Fletcher, D. J. C. & Vargo, E. L. 1987 Biochemical phenotypic and genetic studies of two introduced fire ants and their hybrid (Hymenoptera: Formicidae). Evolution 41, 280-293. (doi:10.2307/2409138)
52. Schrempf, A., Heinze, J. & Cremer, S. 2005 Sexual cooperation: mating increases longevity in ant queens. Curr. Biol. 15, 267-270. (doi:10.1016/j.cub.2005.01.036)
53. Schwander, T., Keller, L. & Helms Cahan, S. 2006 Genetic caste determination in Pogonomyrmex harvester ants imposes costs during colony founding. J. Evol. Biol. 19, 402-409. (doi:10.1111/j.1420-9101. 2005.01023.x)
54. Schwander, T., Keller, L. & Helms Cahan, S. 2007a Two alternate mechanisms contribute to the persistence of interdependent lineages in Pogonomyrmex harvester ants. Mol. Ecol. 16, 3533-3543. (doi:10.1111/j.1365-294X.2007.03407.x)
55. Schwander, T., Helms Cahan, S. & Keller, L. 2007b Characterization and distribution of Pogonomyrmex harvester ant lineages with genetic caste determination. Mol. Ecol. 16, 367-387. (doi:10.1111/j.1365-294X.2006.03124.x)
56. Seifert, B. 1991 The phenotypes of the Formica rufa complex in East Germany. Abh. Ber. Naturkundemus. Görlitz 65, 1-27.
57. Seifert, B. 1999 Interspecific hybridisations in natural populations of ants by example of a regional fauna (Hymenoptera, Formicidae). Insect. Soc. 46, 45-52. (doi:10.1007/s000400050111)
58. Seifert, B. & Goropashnaya, A. V. 2004 Ideal phenotypes and mismatching haplotypes - errors of mtDNA treeing in ants (Hymenoptera: Formicidae) detected by standardized morphometry. Org. Divers. Evol. 4, 295-305. (doi:10.1016/j.ode.2004.04.005)
59. Shoemaker, D. D., Ahrens, M. E. & Ross, K. G. 2006 Molecular phylogeny of fire ants of the Solenopsis saevissima species-group based on mtDNA sequences. Mol. Phylogenet. Evol. 38, 200-215. (doi:10.1016/j.ympev.2005.07.014)
60. Simmons, L. W. 2001 Sperm competition and its evolutionary consequences in the insects. Princeton, NJ: Princeton University Press.
61. Umphrey, G. J. 2006 Sperm parasitism in ants: Selection for interspecific mating and hybridization. Ecology 87, 2148-2159. (doi:10.1890/0012-9658(2006)87[2148:SPIASF]2.0.CO;2)
62. Umphrey, G. J. & Danzman, R. G. 1998 Electrophoretic evidence for hybridization in the ant genus Acanthomyops (Hymenoptera: Formicidae). Biochem. Syst. Ecol. 26, 431-440. (doi:10.1016/S0305-1978(97) 00124-5)
63. Vander Meer, R. K. & Lofgren, C. S. 1989 Biochemical and behavioral evidence for hybridization between fire ants, Solenopsis invicta and Solenopsis richteri (Hymenoptera, Formicidae). J. Chem. Ecol. 15, 1757-1765. (doi:10.1007/BF01012263)
64. Volny, V. P. & Gordon, D. M. 2002 Genetic basis for queen-worker dimorphism in a social insect. Proc. Natl Acad. Sci. USA 99, 6108-6111. (doi:10.1073/pnas.092066699)
65. Volny, V. P., Greene, M. J. & Gordon, D. M. 2006 Brood production and lineage discrimination in the red harvester ant (Pogonomyrmex barbatus). Ecology 87, 2194-2200. (doi:10.1890/0012-9658(2006)87[2194:BPALDI]2. 0.CO;2)
66. Wheeler, W. M. 1910 Ants: their structure, development and behavior. New York, NY: Columbia University Press.
67. Wiernasz, D. C., Yencharis, J. & Cole, B. J. 1995 Size and mating success in males of the Western Harvester Ant, Pogonomyrmex occidentalis (Hymenoptera, Formicidae). J. Insect Behav. 8, 523-531. (doi:10.1007/BF01995324)
68. Wilson, E. O. 1971 The insect societies. Cambridge, MA: Harvard University Press.
69. Woyciechowski, M. 1987 The phenology of nuptial flights of ants (Hymenoptera: Formicidae). Acta Zool. Cracor. 30, 137-140.
70. Woyciechowski, M. 1990 Mating behaviour in the ant Myrmica rubra (Hymenoptera, Formicidae). Acta Zool. Cracov. 33, 565-574.