Eur. J. Entomol. 119: 58-68, 2022 | DOI: 10.14411/eje.2022.006

Variation in the colour pattern of the narrow-headed ant Formica exsecta (Hymenoptera: Formicidae) in European RussiaOriginal article

Tatyana S. PUTYATINA ORCID...1, Alexey V. GILEV ORCID...2, Vladimir G. GRINKOV ORCID...1, Alexander V. MARKOV ORCID...1
1 Department of Biological Evolution, Faculty of Biology, Lomonosov Moscow State University, 119234 Moscow, Russia; e-mails: tsergput@gmail.com, v.grinkov@gmail.com, markov_a@inbox.ru
2 Institute of Plant and Animal Ecology, Ural Branch, Russian Academy of Sciences, Yekaterinburg, Russia; e-mail: gilev@ipae.uran.ru

We determined whether body colour patterns of the narrow-headed Formica exsecta ant can serve as a marker of adaptative strategies in heterogenous environments. The variations in colour were studied in two populations of F. exsecta in central and north western areas in European Russia. A generalised colour scheme of the head and three thorax segments is developed based on a comparative analysis of the colouration of F. exsecta and red wood ants (Formica s. str.). The scheme consists of 23 variants. We found that the colouration of different parts of the body varies independently to a large extent, although a pale (less melanized) head and three thoracic segments often co-occur with paler other parts of the body. We also show that the relationship between colour pattern and body size vary significantly in different complexes. We suggest that these colour variants can be used to study the spatial-temporal phenotypic differentiation of populations and adaptation of ants to microhabitats. The proposed scheme can be used as a convenient tool in future studies to quantify the variation in colour patterns. This scheme should be further tested for its applicability for other species of the subgenus Coptoformica.

Keywords: Polymorphism, polyphenism, colour variants, adaptation, Ryazan Region, White Sea Coast

Received: February 22, 2021; Revised: November 30, 2021; Accepted: November 30, 2021; Published online: January 18, 2022  Show citation

ACS AIP APA ASA Harvard Chicago Chicago Notes IEEE ISO690 MLA NLM Turabian Vancouver
PUTYATINA, T.S., GILEV, A.V., GRINKOV, V.G., & MARKOV, A.V. (2022). Variation in the colour pattern of the narrow-headed ant Formica exsecta (Hymenoptera: Formicidae) in European Russia. EJE119, Article 58-68. https://doi.org/10.14411/eje.2022.006
Download citation

References

  1. Alpatov V.V. 1924: Variation and the lower systematic categories. - Russ. Zool. Zh. 4: 227-244 [in Russian].
  2. Badejo O., Skaldina O., Gilev A. & Sorvari J. 2020: Benefits of insect colours: a review from social insect studies. - Oecologia 194: 27-40. Go to original source...
  3. Belskii E.A. & Gilev A.V. 2007: Accumulation of heavy metals in ants in the vicinity of the Middle Ural copper plant. - Problems Biogeochem. Geochem. Ecol. 2: 92-97 [in Russian].
  4. Benkovskaya G.V. & Udalov M.B. 2011: Colorado Potato Beetles Investigations in the South Urals. Nova Science, New York, 60 рр.
  5. Benkovskaya G.V., Leont'eva T.L. & Udalov M.B. 2008: Colo­rado potato beetle resistance to insecticides in the Southern Urals. - Agrokhimiya 8: 55-59 [in Russian].
  6. Berman D.I., Alfimov A.V., Zhigulskaya Z.A. & Leirikh A.N. 2007: Overwintering and Cold Hardiness of Ants in North-East of Asia. KMK Scientific Press, Moscow, 261 pp.
  7. Bernstein R.A. 1976: The adaptive value of polymorphism in an alpine ant, Formica neorufibarbis gelida Wheeler. - Psyche 83: 180-184. Go to original source...
  8. Boiteau G. 1994: Genetics of the Colorado potato beetle, Leptinotarsa decemlineata (Say). In Jolivet P.H., Cox M.L. & Petitpierre E. (eds): Novel Aspects of the Biology of Chrysomelidae. Series Entomologica, Vol. 50. Springer, Dordrecht, pp. 231-236. Go to original source...
  9. Brakefield P.M. & Frankino W.A. 2009: Polyphenisms in Lepidoptera: Multidisciplinary approaches to studies of evolution. In Whitman D.W. & Ananthakrishnan T.N. (eds): Phenotypic Plasticity of Insects, Mechanisms and Consequences. Science Publishers, Enfield, pp. 337-368. Go to original source...
  10. Cain A.J. & Sheppard P.M. 1954: The theory of adaptive polymorphism. - Am. Nat. 88: 321-326. Go to original source...
  11. Cuthill I.C., Allen W.L., Arbuckle K. & Caspers B. 2017: The biology of color. - Science 357(6350): eaan0221, 7 pp. Go to original source...
  12. Chetverikov S.S. 1926: On certain aspects of the evolutionary process from the standpoint of modern genetics. - J. Exp. Biol. 2: 3-54 [in Russian]. Englich translation (1961) Proc. Am. Phil. Soc. 105: 167-195.
  13. Czechowski W. 1996: Colonies of hybrids and mixed colonies: interspecific nest takeover in wood ants (Hymenoptera, Formicidae). - Memorab. Zool. 50: 1-116.
  14. Dlussky G.M. 1967: Ants of the Genus Formica (Hymenoptera, Formicidae). Nauka, Moscow, 236 pp. [in Russian].
  15. Dlussky G.M., Fedoseeva E.B. & Thompson L.C. 1998: Variability of the ants Solenopsis richteri and S. wagneri (Hymeno­ptera, Formicidae): Statistical analyses of morphometric characters. - Uspekhi Sovrem. Biol. 118: 283-298 [in Russian, English abstract].
  16. Dobzhansky T. 1937: Genetics and the Origin of Species. Columbia University Press, New York, 364 pp.
  17. Filippov N.N. 1961: Regularities of abberative variability of elytra pattern in Coleoptera. - Russ. J. Zool. 40: 372-385 [in Rusian with English abstr.].
  18. Ford E.B. 1965: Genetic Polymorphism. Faber & Faber, London, 101 pp.
  19. Fuzeau-Braesch S. 1972: Pigments and сolor сhanges. - Annu. Rev. Entomol. 17: 403-424. Go to original source...
  20. Gilev A.V. 2002: Discrete variations of coloration and some patterns of pigmentation variability in workers of wood ants of the subgenus Formica (Hymenoptera, Formicidae). - Entomol. Rev. 82: 481-486.
  21. Gilev A.V. 2003: The population pattern of the ant Formica aquilonia (Hymenoptera, Formicidae) in the Middle Urals. - Biol. Bull. Rev. 123: 223-228 [in Russian, English abstract].
  22. Gilev A.V., Mershchiev A.V. & Malyshev D.S. 2015: Interpretation of postglacial recolonization of Formica aquilonia (Hymenoptera, Formicidae) in Fennoscandia according to workers' color variation. - Entomol. Rev. 95: 941-946. Go to original source...
  23. Grinkov V.G., Palko I.V. & Helmut S. 2019: Character displacement within the breeding area questions reinforcement in Ficedula flycatchers. - Bio Rxiv 515916; doi: https://doi.org/10.1101/515916. Go to original source...
  24. Grizenko V.V., Glotov N.V. & Orlinsky D.B. 1998: Ecological and genetic analysis of central elements variation in Leptinotarsa decemlineata (Coleoptera) foreback pattern. - Russ. J. Zool. 77: 278-284 [in Russian, English abstract].
  25. Goryunov D.N. 2007: Forms of settlement organization in Formica exsecta ants. - Uspekhi Sovrem. Biol. 127: 203-208 [in Russian, English abstract].
  26. Goryunov D.N. 2010: Territorial strategies in ants. - Entomol. Rev. 91: 212-220 . Go to original source...
  27. Goryunov D.N. 2015: Nest-building in ants Formica exsecta (Hymenoptera, Formicidae). - Entomol. Rev. 95: 953-958. Go to original source...
  28. Holloway G.J., Brakefield P.M., De Jong P.W., Ottenheim M.M., De Vos H., Kesbeke F. & Peynenburg L. 1995: A quantitative genetic analysis of an aposematic colour pattern and its ecological implications. - Phil. Trans. R. Soc. Lon. (B) 348: 373-379. Go to original source...
  29. Ilyina T.A. & Ivankina E.V. 2001: Seasonal variation of vinging activity and relative effect of the advertising behaviour of males with different plumage colour in the Pied Flycatcher Ficedula hypoleuca. - Acta Ornithol. 36: 85-89. Go to original source...
  30. Kerimov A.B., Grinkov V.G., Ivankina E.V., Ilyina T.A. & Bushuev A.V. 2014: The influence of spring temperature on the intensity of advertising behavior and basal metabolic rate in bright and pale pied flycatcher (Ficedula hypoleuca) males. - Russ. J. Zool. 93:1288-1302 [in Russian, English abstract].
  31. Kingsolver J.K., Diamond S.E., Seiter S.A. & Higgins J.K. 2012: Direct and indirect phenotypic selection on developmental trajectories in Manduca sexta. - Funct. Ecol. 26: 598-607. Go to original source...
  32. Klingenberg C.P. 2008: Morphological integration and developmental modularity. - Annu. Rev. Ecol. Evol. Syst. 39: 115-132. Go to original source...
  33. Korochkina N.I., Konopleva E.E. & Zryanina T.A. 2014: Population structure of Formica aquilonia (Hymenoptera, Formicidae) at the boundary of boreal and subboreal landscapes in the Volga river region. - Entomol. Rev. 94: 664-674. Go to original source...
  34. Korsun O. 1994: Variability and population structure of Hoplia aureola Pall. (Coleoptera, Scarabaeidae). - Ecology 25: 372-379.
  35. Korsun O. 2000: Phenotypic appearance of the natural populations of Adalia bipunctata L. (Coleoptera, Coccinellidae). - Siber. J. Ecol. 6: 723-726.
  36. Majerus M.E.N. 1994: Ladybirds. London, Harper Collins, 367 pp.
  37. Markov A.V. & Ivnitsky S.B. 2016: Evolutionary role of phenotypic plasticity. - Vestn. Mosk. Univ. 16: 3-11 [in Russian, English abstract]. Go to original source...
  38. Markov A., Gilev A. & Putyatina T. 2017: Structure of moundbuilding ant settlements (genus Formica) in Kuzokotsky Peninsula (northern Karelia). - Biol. Commun. 62: 93-102. Go to original source...
  39. Miyazaki S., Okada Y., Miyakawa H., Tokuda G., Cornette R., Kishikawa S., Maekawa K. & Miura T. 2014: Sexually dimorphic body colour is regulated by sex-specific expression of yellow gene in ponerine ant, Diacamma sp. - PLoS ONE 9(3): e92875, 8 pp. Go to original source...
  40. Moczek A.P. 2008: On the origins of novelty in development and evolution. - BioEssays 30: 432-447. Go to original source...
  41. Moczek A.P. 2012: The nature of nurture and the future of Evodevo: toward a theory of developmental evolution. - Integr. Comp. Biol. 52: 108-119. Go to original source...
  42. Nishikawa H., Iijima T., Kajitani R., Yamaguchi J., Ando T., Suzuki Y., Sugano S., Fujiyama A., Kosugi S., Hirakawa H. et al. 2015: A genetic mechanism for female-limited Batesian mimicry in Papilio butterfly. - Nature Genet. 47: 405-409. Go to original source...
  43. Oms C.S., Cerdá X. & Boulay R. 2017: Is phenotypic plasticity a key mechanism for responding to thermal stress in ants? - Sci. Nat. 104: 42, 7 pp. Go to original source...
  44. Pisarski B. & Banert T. 1982: Influence de la structure sociale sur la morphologie de Formica (Coptoformica) exsecta Nyl. - Mem. Zool. 38: 137-162.
  45. Plavilshchikov N.N. 1936: Woodcutter beetles (Cerambycidae). In: Fauna of the USSR. Coleoptera. V. XXI. Part 1. Academy of Sciences of the USSR, Moscow, Leningrad, 612 pp.
  46. Qvarnstrom A.A., Rice M. & Ellegren H. 2010: Speciation in Ficedula flycatchers. - Philos. Trans. R. Soc. Lond. (B) 365: 1841-1852. Go to original source...
  47. Roulin A. 2014: Melanin-based colour polymorphism responding to climate change. - Glob. Change Biol. 20: 3344-3350. Go to original source...
  48. Roulin A. 2016: Condition-dependence, pleiotropy and the handicap principle of sexual selection in melanin-based colouration. - Biol. Rev. 91: 328-348. Go to original source...
  49. Rusina L.Y., Gilev A.V., Skorokhod O.V., Filimonova N.B. & Firman L.A. 2007: Relationship between coloration of the wasp (Polistes dominulus) and spatial and ethological structure of its population in the Lower Dnieper Basin. - Biol. Bull. Rev. 127: 157-165.
  50. Rusina L.Y., Gilyov A.V., Firman L.A., Pekanova I.A. & Orlova E.S. 2011: Dynamic stability of phenotypic variation in Polistes wasps (Hymenoptera: Vespidae). - Russ. Entomol. J. 20: 321-326. Go to original source...
  51. Ruzsky M.D. 1905: The Ants of Russia. Part 1. Kazan, 798 pp.
  52. Saccheri I.J., François R., Phillip C.W., Paul M.B. & Laurence M.C. 2008: Selection and gene flow on a diminishing cline of melanic peppered moths. - Proc. Natn. Acad. Sci. USA 105: 16212-16217. Go to original source...
  53. Seifert B. 2004: The "Black Bog Ant" Formica picea Nylander, 1846 - a species different from Formica candida Smith, 1878 (Hymenoptera: Formicidae). - Myrmecol. Nachr. 6: 29-38.
  54. Seifert B. 2007: Die Ameisen Mittel- und Nordeuropas. Lutra Verlags und Vertriebsgesellschaft, Tauer, 368 pp.
  55. Shvanvich B.N. 1949: The Course of General Entomology. - Sov. Science, Moskow, 900 pp. [in Russian].
  56. Simpson S.J., Sword G.A. & Lo N. 2011: Polyphenism in insects. - Curr. Biol. 21: 738-749. Go to original source...
  57. Skaldina O. & Sorvari J. 2017: Not simply red: Colouration of red wood ant Formica rufa (Hymenoptera: Formicidae) is poly­morphic, modular and size-dependent. - Eur. J. Entomol. 114: 317-324. Go to original source...
  58. Skaldina O. & Sorvari J. 2020: Phenotypic diversity in red wood ants (Hymenoptera: Formicidae): Is kinship involved? - Eur. J. Entomol. 117: 27-33. Go to original source...
  59. Skaldina O., Piraniemi S. & Sorvari J. 2018: Ants and their nests as indicators for industrial heavy metal contamination. - Environ. Pollut. 240: 574-581. Go to original source...
  60. Stoehr A.M. 2016: Costly melanin ornaments: the importance of taxon? - Funct. Ecol. 20: 276-281. Go to original source...
  61. Tibbetts E.A. 2010: The condition dependence and heritability of signaling and nonsignal color traits in a paper wasp. - Am. Nat. 175: 495-503. Go to original source...
  62. Tibbets E.A. 2013: The function, development, and evolution stability of conventional signals of fighting ability. - Adv. Study Behav. 45: 49-80. Go to original source...
  63. Timofeev-Resovskiy N.W., Timofeev-Resovskaya Е.А. & Zimmer K.G. 1965: Experimental and systematic analysis of geographic variability and morphogenesis in Epilachna chrysomelina. In: Proceedings of the Institute of Biology of the Ural Branch of the Academy of Sciences of the USSR. Ekaterinburg, pp. 27-63.
  64. Timofeev-Resovsky N.V., Yablokov A.V. & Glotov N.V. 1973: Essay of the Theory on Population. Nauka, Moscow, 278 pp. [in Russian].
  65. Van't Hof A.E., Campagne P., Rigden D.J., Yung C.J., Lingley J., Quail M.A., Hall N., Darby A.C. & Saccheri I.J. 2016: The industrial melanism mutation in British peppered moths is a transposable element. - Nature 534: 102-105. Go to original source...
  66. Vasilyev A.G. 2005: Epigenetic Patterns of Phenetics: On the Way to Population Meronomy. Akademkniga, Yekaterinburg, 640 pp. [in Russian].
  67. Vilcinskas A. & Vogel H. 2016: Seasonal phenotype-specific transcriptional reprogramming during metamorphosis in the European map butterfly Araschnia levana. - Ecol. Evol. 6: 3476-3485. Go to original source...
  68. West-Eberhard M.J. 2003: Developmental Plasticity and Evolution. Oxford University Press, New York, 816 pp. Go to original source...
  69. Whitman D.W. & Agrawal A.A. 2009: What is phenotypic plasticity and why is it important? In Whitman D.W. & Ananthakrishnan T.N. (eds): Phenotypic Plasticity of Insects, Mechanisms and Consequences. Science Publishers, Enfield, pp. 1-63. Go to original source...
  70. Yablokov A.V. & Larina N.I. 1985: Introduction in Population Phenetics: The New Method to Investigation of Natural Populations. Vyshaya Shkola, Moscow, 159 pp.
  71. Zakharov A.A. 2015: Ants of Forest Communities, their Life and their Role in Forest. KMK Scientific Press, Moscow, 404 pp. [in Russian].
  72. Zhan S., Zhang W., Niitepõld K., Hsu J., Haeger J.F., Zalucki M.P., Altizer S., de Roode J.C., Reppert S.M. & Kronforst M.R. 2014: The genetics of monarch butterfly migration and warning colouration. - Nature 514: 317-321. Go to original source...

This is an open access article distributed under the terms of the Creative Commons Attribution 4.0 International License (CC BY 4.0), which permits use, distribution, and reproduction in any medium, provided the original publication is properly cited. No use, distribution or reproduction is permitted which does not comply with these terms.