Eur. J. Entomol. 107 (2): 157-167, 2010 | DOI: 10.14411/eje.2010.021

Genetic polymorphism in "mixed" colonies of wood ants (Hymenoptera: Formicidae) in southern Finland and its possible origin

Julita KORCZYŃSKA1, Marta GAJEWSKA*,2, Malgorzata PILOT2, Wojciech CZECHOWSKI2, Alexander RADCHENKO2
1 Laboratory of Ethology, Nencki Institute of Experimental Biology, Polish Academy of Sciences, Pasteura 3, 02-093 Warsaw, Poland; e-mail: j.korczynska@nencki.gov.pl
2 Museum and Institute of Zoology, Polish Academy of Sciences, Wilcza 64, 00-679 Warsaw, Poland; e-mails: mpilot@miiz.waw.pl, wcz@miiz.waw.pl, agradchenko@hotmail.com

Wood ant colonies that appear to consist of individuals representing different species are described in several previous papers. The present study is the first to elucidate the genetic basis of the spectacular morphological variability observed within such colonies. Two seemingly mixed colonies (FM-1 and FM-2) from southern Finland were investigated. On the basis of the morphology of their workers these colonies were comprised of individuals with phenotypes typical of Formica rufa L., F. polyctena Först., and F. aquilonia Yarr. The sequence of an mtDNA fragment (5' end of the cytochrome b gene) was used to examine the phylogenetic relationships among haplotypes of workers from homogeneous colonies of different wood ant species and the two supposedly mixed colonies, and to sort the individuals within the colonies into matrilines. Six microsatellite loci were used to analyse the genetic differentiation between colonies and among workers within colonies, and to detect putative hybrids. The results show that, independently of their phenotype, workers from the "mixed" colonies were genetically more similar to other individuals in their colony than to those in the homogeneous F. rufa, F. polyctena or F. aquilonia colonies. However, while colony FM-1 consisted of offspring of the same queen or more likely several maternally related queens, colony FM-2 consisted of the offspring of at least four unrelated queens. The data suggest hybridisation between F. polyctena × F. aquilonia and F. polyctena × F. rufa (and possibly subsequent mating between these hybrids) as the most probable mechanism leading to the existence of these two colonies, which implies that the hybrids are fertile. This study shows that colonies of wood ant hybrids can arise spontaneously and persist under natural conditions. The results also revealed that even some morphologically homogeneous colonies are genetically heterogeneous. In the case of closely related, morphologically similar species that interbreed, morphology can be a bad predictor of genetic differences between individuals.

Keywords: Ants, Formica rufa-group, mixed colonies, hybridisation, genetic polymorphism

Received: February 10, 2009; Accepted: December 9, 2009; Published: April 15, 2010

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References

  1. BERETTA BOERA M., PETRAZZINI S., PAVAN M. & TROCONI A. (eds) 1979: Comptes Rendus de la Reunion des Groupes de Travail "Formica rusa" et "Vertebres Predateurs des Insectes" de l'OILB (Varenna, Italie, 1978). Bulletin SROP, II-3. 514 pp
  2. 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
  3. CLEMENT M., POSADA D. & CRANDALL K.A. 2000: TCS: A computer program to estimate gene genealogies. Mol. Ecol. 9: 1657-1660 Go to original source...
  4. COLLINGWOOD C.A. 1979: The Formicidae (Hymenoptera) of Fennoscandia and Denmark. Fauna Entomol. Scand. 8: 1-174
  5. COLLINGWOOD C.A. & AGOSTI D. 1986: Taxonomy and zoogeography of the Formica rufa species group. Supplement to the Workshop "Taxonomy and Zoogeography of the Formica rufa Species Group" Held at the 10th International Congress of IUSSI, Munich, 1986
  6. COTTI G. 1963: Bibliografia Ragionata 1930-1961 del Gruppo Formica rufa. Collana Verde 8. Ministero dell'Agricoltura e Foreste, Roma, iv + 413 pp. [in Italian, German, English]
  7. CZECHOWSKI W. 1993: Hybrids in red wood ants (Hymenoptera, Formicidae). Ann. Zool. 44: 43-54
  8. CZECHOWSKI W. 1994: Queen recruitment in an orphaned colony of Formica polyctena Foerst. (Hymenoptera, Formicidae). Ann. Zool. 45: 47-49
  9. CZECHOWSKI W. 1996: Colonies of hybrids and mixed colonies; interspecific nest takeover in wood ants (Hymenoptera, Formicidae). Memor. Zool. 50: 1-116
  10. CZECHOWSKI W. & DOUWES P. 1996: Morphometric characterics of Formica polyctena Foerst. and Formica rufa L. (Hymenoptera, Formicidae) from the Gorce Mts; Interspecific variations. Ann. Zool. 46: 125-141
  11. CZECHOWSKI W., RADCHENKO A. & CZECHOWSKA W. 2002: The Ants (Hymenoptera, Formicidae) of Poland. Museum and Institute of Zoology PAS, Warsaw, 200 pp
  12. CZECHOWSKI W. & RADCHENKO A. 2006: Do permanently mixed colonies of wood ants (Hymenoptera: Formicidae) really exist? Ann. Zool. 56: 667-673
  13. DLUSSKY G.M. 1967: The Ants of the Genus Formica. Nauka, Moskva, 236 pp. [in Russian]
  14. DLUSSKY G.M. & PISARSKI B. 1971: Revision of Polish ant species of the genus Formica L. (Hymenoptera, Formicidae) Fragm. Faun. 16: 145-224 [in Polish, English abstr.] Go to original source...
  15. DOUWES P. 1979: Formica rufa-gruppens systematic. Entomol. Tidskr. 100: 187-191
  16. DOUWES P. 1981: Intraspecific and interspecific variation in workers of the Formica rufa group (Hymenoptera: Formicidae) in Sweden. Entomol. Scand. (Suppl.) 15: 213-223
  17. FELSENSTEIN J. 1985: Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39: 783-791 Go to original source...
  18. GOROPASHNAYA A., SEIFERT B. & PAMILO P. 2003: Phylogenetic relationships of Palaearctic species (Hymenoptera, Formicidae) based on mitochondrial cytochrome b sequences. Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology, Paper I . 15 pp
  19. GOROPASHNAYA A., FEDOROV V. & PAMILO P. 2004: Recent speciation in the Formica rufa group ants (Hymenoptera, Formicidae): inference from mitochondrial DNA phylogeny. Mol. Phylogen. Evol. 32: 198-206 Go to original source...
  20. GOUDET J., RAYMOND M., DE MEEUS T. & ROUSSET F. 1996: Testing differentiation in diploid populations. Genetics 144: 1933-1940
  21. GOSSWALD K. 1989: Die Waldameise. Band 1. Biologische Grundlagen, Okologie und Verhalten. Aula, Wiesbaden, xi + 660 pp.
  22. GOSSWALD K., KNEITZ G. & SCHIRMER G. 1965: Die geographische Verbreitung der huegelbauenden Formica-Arten (Hym., Formicidae) in Europa. Zool. Jb. Syst. 92: 369-404
  23. GYLLENSTRAND N., GERTSCH P.J. & PAMILO P. 2002: Polymorphic microsatellite DNA markers in the ant Formica exsecta. Mol. Ecol. Notes 2: 67-69 Go to original source...
  24. GYLLENSTRAND N., SEPPA P. & PAMILO P. 2004: Genetic differentiation in sympatric wood ants, Formica rufa and Formica polyctena. Insectes Soc. 51: 139-145 Go to original source...
  25. KUTTER H. 1977: Hymenoptera, Formicidae. In: Insecta. Helvetica Fauna 6. Schweizerische Entomologische Gesellschaft: Zuerich, 297 pp
  26. NEI M. 1978: Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89: 583-590
  27. PAETKAU D., SLADE R., BURDEN M. & ESTOUP A. 2004: Genetic assignment methods for the direct, real-time estimation of migration rate: a simulation-based exploration of accuracy and power. Mol. Ecol. 13: 55-65 Go to original source...
  28. PAMILO P. & VEPSALAINEN K. 1977: Heretical notes on the taxonomy of Formica s. str. (Hym.). Proceedings of the VIII International Congress of IUSSI. Wageningen, pp. 128-129
  29. PAMILO P., VEPSALAINEN K., ROSENGREN R., VARVIO-AHO S.-L. & PISARSKI B. 1979: Population genetics of Formica ants II. Genic differentiation between species. Ann. Entomol. Fenn. 45: 65-76
  30. PAMILO P., CHAUTEMS D. & CHERIX D. 1992: Genetic differentiation of disjunct populations of the ants Formica aquilonia and Formica lugubris in Europe. Insectes Soc. 39: 15-29 Go to original source...
  31. PEARSON B. 1983: Hybridisation between Lasius niger and Lasius alienus. Insectes Soc. 30: 402-411 Go to original source...
  32. PIRY S., ALAPETITE A., CORNUET J.-M., PAETKAU D., BAUDOUIN L. & ESTOUP A. 2004: GeneClass2: a software for genetic assignment and first generation migrants detection. J. Hered. 95: 536-539 Go to original source...
  33. PISARSKI B. & CZECHOWSKI W. 1994: Ways to reproductive success of wood ant queens. Memor. Zool. 48: 181-186
  34. POSADA D. & CRANDALL K.A. 1998: MODELTEST: testing the model of DNA substitution. Bioinformatics 14: 817-818 Go to original source...
  35. PRITCHARD J. K., STEPHENS M. & DONNELLY P. 2000: Inference of population structure using multilocus genotype data. Genetics 155: 945-959
  36. RANNALA B. & MOUNTAIN J.L. 1997: Detecting immigration by using multilocus genotypes. PNAS 94: 9197-9221 Go to original source...
  37. RAYMOND M. & ROUSSET F. 1995: An exact test for population differentiation. Evolution 49: 1280-1283 Go to original source...
  38. ROSENGREN R. 1977a: Foraging strategy of wood ants (Formica rufa group). I. Age polyethism and topographic traditions. Acta Zool. Fenn. 149: 1-30
  39. ROSENGREN R. 1977b: Foraging strategy of wood ants (Formica rufa group). II. Nocturnal orientation and diel periodicity. Acta Zool. Fenn. 150: 1-30
  40. SEIFERT B. 1984: Nachweis einer im Freiland aufgetretenen Bastardierung von Leptothorax nigriceps Mayr und Leptothorax unifasciatus (Latr.) mittels einer multiplen Diskriminanzanalyse. Abh. Ber. Naturkundemus. GGrlitz 58: 1-8
  41. SEIFERT B. 1991: The phenotypes of the Formica rufa complex in East Germany. Abh. Ber. Naturkundemus. GGrlitz 65: 1-27
  42. SEIFERT B. 1996a: Formica paralugubris nov. spec. - a sympatric sibling species of Formica lugubris from the western Alps (Insecta: Hymenoptera: Formicoidea: Formicidae). Reichenbachia 31: 193-201
  43. SEIFERT B. 1996b: Ameisen: Beobachten, Bestimmen. Nachtbuch, Augsburg, 352 pp
  44. SEIFERT B. 1999: Interspecific hybridizations in natural populations of ants by example of a regional fauna (Hymenoptera, Formicidae). Insectes Soc. 46: 45-52 Go to original source...
  45. SEIFERT B. & GOROPASHNAYA A. 2004: Ideal phenotypes and mismatching haplotypes - errors of mtDNA treeing in ants (Hymenoptera, Formicidae) detected by standardized morphometry. Organ. Diver. Evol. 4: 295-305 Go to original source...
  46. SORVARI J. 2006: Two distinct morphs in the wood ant Formica polyctena in Finland: a result of hybridisation? Entomol. Fenn. 17: 1-7
  47. SWOFFORD D.L. 1998: PAUP Phylogenetic Analysis Using Parsimony and Other Methods. Sinauer Associates, Sunderland, MA
  48. TEMPLETON A.R. & SING C.F.A. 1993: A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping. IV. Nested analysis with cladogram uncertainty and recombination. Genetics 134: 659-669
  49. TEMPLETON A.R., CRANDALL K.A. & SING C.F.A. 1992: A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping and DNA sequence data. III. Cladogram estimation. Genetics 132: 619-633
  50. THOMPSON J.D., HIGGINS D.G. & GIBSON T.J. 1994: CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting position-specific gap penalties and weight matrix choice. Nucl. Acid Res. 22: 4673-4680 Go to original source...
  51. TINAUT A. & MARTINEZ M.D. 1998: Taxonomy and distribution of Formica dusmeti Emery, 1909 and of F. frontalis Santschi, 1919 (Hymenoptera, Formicidae). Graellsia 54: 31-41 Go to original source...
  52. VEPSALAINEN K. & PISARSKI B. 1981: The taxonomy of the Formica rufa group: chaos before order. In Howse P.E. & Clement J.-L. (eds): Biosystematics of Social Insects. Academi Press, New York, pp. 27-36
  53. YARROW I.H.H. 1955: The British ants allied to Formica rufa L. (Hym., Formicidae). Trans. Soc. Br. Entomol. 12: 1-48