Advertisement

CHEMOECOLOGY

, Volume 2, Issue 1, pp 20–28 | Cite as

Sex pheromones and their potential role in the evolution of reproductive isolation in small ermine moths (Yponomeutidae)

  • Christer Löfstedt
  • Wim M. Herrebout
  • Steph B. J. Menken
Research papers

Summary

Sex pheromone communication in the nine European species of small ermine moths (Yponomeuta) is reviewed in regard to the potential role of pheromones in the speciation process. Six of the nine species studied (viz.,Y. evonymellus, Y. cagnagellus, Y. padellus, Y. irrorellus, Y. plumbellus, andY. vigintipunctatus) use a mixture of (E)-11-and (Z)-11-tetradecenyl acetate in different ratios as primary pheromone components, with combinations of tetradecyl acetate, (Z)-9-tetradecenyl acetate, (Z)-11-hexadecenyl acetate and the corresponding alcohols of the acetates as additional pheromone components. Analysis of (Z)- to (E)-11-tetradecenyl acetate ratios produced by individual females of these species demonstrated significant variation among females of all species. However, the ranges of ratios produced byY. cagnagellus, Y. irrorellus, andY. plumbellus, sharing the same host-plant species, spindle tree, did not overlap. Niche separation of all six species mentioned required consideration of at least one additional pheromone component or of temporal aspects. The remaining three species,i.e. Y. malinellus, Y. mahalebellus andY. rorellus, have pheromones that differ qualitatively.

Biosynthetic routes to the pheromone components identified are proposed on the basis of fatty acid pheromone precursors found in the pheromone glands. A phylogenetic tree for the genus is constructed based on allozyme frequency data and changes in pheromone composition are superimposed on this tree. We suggest that the ancestral ermine moth pheromone is a mixture of (Z)-11- and (E)-11-tetradecenyl acetate and the corresponding alcohols, and a scenario of how present-day patterns evolved is outlined. The pheromone differences among the three species using spindle tree as their host-plant might have evolved throughreproductive character displacement upon secondary contact between populations that had already diverged genetically in allopatry. Pheromone differences within the so-calledpadellus-complex (includingY. cagnagellus, Y. mahalebellus, Y. malinellus, Y. padellus, andY. rorellus) in which species might have originated sympatrically, may have evolved byreinforcing selection as these species still hybridise and produce viable offspring when confined in cages. The role of pheromones in reproductive isolation amongYponomeuta species is emphasised by (1) the function of pheromone components of some of the species as behavioural antagonists to other species, (2) the cross-attraction under experimental conditions between allochronic species with similar pheromones, and (3) the formation of hybrids in the laboratory between species that are isolated in nature by pheromone differences.

Key words

speciation reinforcement character displacement biosynthesis phylogeny sex pheromones reproductive isolation (Z)-11-tetradecenyl acetate (E)-11-tetradecenyl acetate Lepidoptera Yponomeutidae Yponomeuta 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Arduino P, Bullini L (1985) Reproductive isolation and genetic divergence between the small ermine mothsYponomeuta padellus andYponomeuta malinellus (Lepidoptera: Yponomeutidae). Atti Acad Naz Lincei 18:33–61Google Scholar
  2. Barton NH, Charlesworth B (1984) Genetic revolutions, founder effects, and speciation. Annu Rev Ecol Syst 15:133–164Google Scholar
  3. Bestmann HJ, Herrig M, Attygalle AB (1987) Terminal acetylation in pheromone biosynthesis byMamestra brassicae L. (Lepidoptera: Noctuidae). Experientia 43:1033–1034Google Scholar
  4. Bjostad LB, Roelofs WL (1983) Sex pheromone biosynthesis inTrichoplusia ni: key steps involve delta-11 desaturation and chain-shortening. Science 220:1387–1389Google Scholar
  5. Bjostad LB, Roelofs WL (1986) Sex pheromone biosynthesis in the redbanded leafroller moth, studies by mass labeling with stable isotopes and analysis with mass spectrometry. J Chem Ecol 12:431–450Google Scholar
  6. Butlin R (1987) Speciation by reinforcement. Trends Ecol Evol 2:8–13Google Scholar
  7. Butlin R (1989) Reinforcement of premating isolation. Pp 158–179in Otte D, Endler JA (eds) Speciation and its Consequences. Sunderland/MA SinauerGoogle Scholar
  8. Dijkerman HJ (1990) Suitability of eightYponomeuta-species as hosts ofDiadegma armillata. Entomol exp appl 54:173–180Google Scholar
  9. Du J-W, Löfstedt C, Löfqvist J (1987) Repeatability of pheromone emissions from individual female ermine mothsYponomeuta padellus andY. rorellus. J Chem Ecol 13:1431–1441Google Scholar
  10. Feder JL, Chilcot A, Bush GL (1990) The geopgraphic pattern of genetic differentiation between host associated populations ofRhagoletis pomonella (Diptera: Tephritidae) in the eastern United States and Canada. Evolution 44:570–94Google Scholar
  11. Friese G (1960) Revision der palaearktischen Yponomeutidae unter besonderer Berücksichtigung der Genitalien (Lepidoptera). Beitr Entomol 10:1–131Google Scholar
  12. Gerrits-Heybroek EM, Herrebout WM, Ulenberg SA, Wiebes JT (1978) Host plant preferences of five species of small ermine moths. Entomol exp appl 24:360–368Google Scholar
  13. Gershenson ZS (1967) Karyotype of the willow ermine mothYponomeuta rorellus HB. (Lepidoptera, Yponomeutidae). Tsitol Genet 1:79–80 (in Russian)Google Scholar
  14. Grant V (1971) Plant Speciation. New York: Columbia University PressGoogle Scholar
  15. Greenfield MD, Karandinos MG (1979) Resource partitioning of the sex communication channel in clearwing moths (Lepidoptera:Sesiidae) of Wisconsin. Ecol Monogr 49:403–426Google Scholar
  16. Hendrikse A (1978) Factors influencing the courtship behaviour ofYponomeuta vigintipunctatus (Retz.). Neth J Zool 28:139–149Google Scholar
  17. Hendrikse A (1979) Activity patterns and sex pheromone specificity as isolating mechanisms in eight species ofYponomeuta (Lepidoptera: Yponomeutidae). Entomol exp appl 25:172–180Google Scholar
  18. Hendrikse A (1986) Intra- and interspecific sex pheromone communication in the genusYponomeuta Latreille. Physiol Entomol 11:159–169Google Scholar
  19. Hendrikse A (1988) Hybridization and sex-pheromone responses among menbers of theYponomeuta padellus-complex. Entomol exp appl 48:213–223Google Scholar
  20. Hendrikse A, Vos-Bünnemeyer E (1987) Role of host-plant stimuli in sexual behaviour of small ermine moths (Yponomeuta). Ecol Entomol 12:363–371Google Scholar
  21. Herrebout WM, Van De Water TPM (1982) The effect of hostplant on pheromone communication in a small ermine moth,Yponomeuta cagnagellus (Lepidoptera: Yponomeutidae). Med Fac Landbouww Rijksuniv Gent 47:503–509Google Scholar
  22. Herrebout WM, Menken SBJ (1990) Preliminary data on the origin of small ermine moths introduced into North America (Lepidoptera, Yponomeutidae). Proc Exper & Appl Entomol 1:146–151Google Scholar
  23. Herrebout WM, Kuijten PJ, Wiebes JT (1976) Small ermine moths of the genusYponomeuta and their host relationships (Lepidoptera: Yponomeutidae). Symp Biol Hung 16:91–94Google Scholar
  24. Jong MCM de (1987) A direct search approach to characterize the sex pheromone composition giving maximal male response. Physiol Entomol 12:11–22Google Scholar
  25. Jong, MCM de (1988) Evolutionary approaches to insect communication systems (Thesis). Leiden, The Netherlands: University of LeidenGoogle Scholar
  26. Jurenka RA, Roelofs WL (1989) Characterization of the acetyltransferase used in pheromone biosynthesis in moths: specificity for the Z isomer in Tortricidae. Insect Biochem 19:639–644Google Scholar
  27. Kaneshiro KY (1980) Sexual isolation, speciation and the direction of evolution. Evolution 34:437–444Google Scholar
  28. Lanier GN, Burkholder WE (1974) Pheromones in Speciation of Coleoptera. Pp 161–189in Birch MC (ed) Pheromones. New York: North-Holland/American ElsevierGoogle Scholar
  29. Littlejohn MJ (1981) Reproductive isolation: a critical review. Pp 298–334in Atchley WR & Woodruff DS (eds) Evolution and Speciation. Cambridge: Cambridge University PressGoogle Scholar
  30. Löfstedt C (1986) Sex pheromones and reproductive isolation in moths. Ent Tidskr 107:125–137Google Scholar
  31. Löfstedt C (1987) Behaviour of small ermine moths in overlapping pheromone plumes. Pp 37–39in Arn H (ed) Mating Disruption — Behaviour of Moths and Molecules. WPRS Bulletin 1987/X/3. Paris: OILB-SROPGoogle Scholar
  32. Löfstedt C (1991) Evolution of moth pheromones. In pressin Proceedings of Conference on Insect Chemical Ecology. Tábor, CzechoslovakiaGoogle Scholar
  33. Löfstedt C, Herrebout WM (1988) Sex pheromones of three small ermine moths found on spindle tree. Entomol exp appl 46:29–38Google Scholar
  34. Löfstedt C, Van Der Pers JNC (1985) Sex pheromones and reproductive isolation in four European small ermine moths. J Chem Ecol 11:649–666Google Scholar
  35. Löfstedt C, Herrebout WM, Du J-W (1986a) Evolution of the ermine moth pheromone tetradecyl acetate. Nature 323:621–623Google Scholar
  36. Löfstedt C, Löfqvist J, Lanne BS, Van Der Pers JNC, Hansson BS (1986b) Pheromone dialects in European turnip mothsAgrotis segetum. Oikos 46:250–257Google Scholar
  37. Löfstedt C, Hansson BS, Roelofs WL, Bengtsson BO (1989) No linkage between genes determining female pheromone production and male olfactory response in the European corn borerOstrinia nubilalis. Genetics 123:553–556Google Scholar
  38. Löfstedt C, Hansson BS, Dijkerman HJ, Herrebout WM (1990) Behavioural and electrophysiological activity of unsaturated analogues to the pheromone tetradecyl acetate in the small ermine mothYponomeuta rorellus. Physiol Entomol 15:47–54Google Scholar
  39. Mayr E (1963) Animal Species and Evolution. Cambridge/MA Harvard University PressGoogle Scholar
  40. McDonough LM, Davis HG, Smithhisler CL, Voerman S, Chapman PS (1990) Apple ermine moth,Yponomeuta malinellus Zeller: two components of female sex pheromone gland highly effective in field trapping tests. J Chem Ecol 16:477–486Google Scholar
  41. Menken SBJ (1980) Inheritance of allozymes inYponomeuta, II. Interspecific crosses within thepadellus-complex and reproductive isolation. Proc Kon Ned Acad Wet (C) 83:425–431Google Scholar
  42. Menken SBJ (1982) Biochemical genetics and systematics of small ermine moths (Lepidoptera: Yponomeutidae). Z Zool Syst Evolforsch 20:131–143Google Scholar
  43. Menken SBJ (1987) Is the extremely low heterozygosity level inYponomeuta rorellus caused by bottlenecks? Evolution 41:630–637Google Scholar
  44. Menken SBJ (1989) Electrophoretic studies on populations, host races, and sibling species in insect pest species. Pp 181–201in Loxdale H, Den Hollander J (eds) Electrophoretic Studies in Insect Pests. Oxford: Clarendon PressGoogle Scholar
  45. Menken SBJ, Herrebout WM, Wiebes JT (1991) Small ermine moths: their host relations and evolution. Annu Rev Entomol (in press)Google Scholar
  46. Nilsson N-O, Löfstedt C, Dävring L (1988) Chromosome number and an unusual inheritance of sex chromosomes in species ofYponomeuta (Yponomeutidae; Lepidoptera). Hereditas 108:259–265Google Scholar
  47. Paterson HEH (1978) More evidence against speciation by reinforcement. Afr J Science 74:369–371Google Scholar
  48. Paterson HEH (1985) The recognition concept of species. Pp 21–29in Vrba ES (ed) Species and Speciation. Pretoria: Transvaal MuseumGoogle Scholar
  49. Peterson SC, Herrebout WM, Kooi RE (1990) Chemosensory basis of host colonization by small ermine moth larvae. Proc Kon Ned Acad Wet (C) 93:282–294Google Scholar
  50. Povel GDE (1984) The identification of the European small ermine moths, with special reference to theYponomeuta padellus-complex (Lepidoptera: Yponomeutidae). Proc Kon Ned Acad Wet (C) 87:149–180Google Scholar
  51. Povel GDE (1986) Pattern detection within theYponomeuta padellus-complex of the European small ermine moths (Lepidoptera, Yponomeutidae). I. Biometric description and recognition of groups by numerical taxonomy. Proc Kon Ned Akad Wet (C) 89:425–41Google Scholar
  52. Roelofs WL, Bjostad LB (1984) Biosynthesis of lepidopteran pheromones. Bioorganic Chemistry 12:279–298Google Scholar
  53. Roelofs WL, Comeau A (1969) Sex pheromone specificity: taxonomic and evolutionary aspects in Lepidoptera. Science 165:398–400Google Scholar
  54. Roelofs WL, Wolf WA (1988) Pheromone biosynthesis in Lepidoptera. J Chem Ecol 14:2019–2031Google Scholar
  55. Roelofs WL, Glover T, Tang X-H, Sreng I, Robbins P, Eckenrode C, Löfstedt C, Hansson B, Bengtsson BO (1987) Sex pheromone production and perception in European corn borer moths is determined by both autosomal and sex-linked genes. Proc Natl Acad Sci USA 84:7585–7589Google Scholar
  56. Rogers JS (1984) Deriving phylogenetic trees from allele frequencies. Syst Zool 33:52–63Google Scholar
  57. Tauber CA, Tauber MJ (1989) Sympatric speciation in insects: perception and perspective. Pp 307–344in Otte D, Endler JA (eds) Speciation and its Consequences. Sunderland/Ma: SinauerGoogle Scholar
  58. Thorpe WH (1929) Biological races inHyponomeuta padella L. J Linn Soc Zool 36:621–634Google Scholar
  59. Van Der Pers JNC (1982) Comparison of single cell responses of antennal sensilla trichodea to sex attractants in nine European small moths (Yponomeuta spp.). Entomol exp appl 31:255–264Google Scholar
  60. Van Drongelen W, van Loon JJA (1980) Inheritance of gustatory sensitivity in F1 progeny of crosses betweenYponomeuta cagnagellus andYponomeuta malinellus. Entomol exp appl 24:199–203Google Scholar
  61. Wiebes JT (1976) The speciation process in the small ermine moths. Neth J Zool 26:440Google Scholar
  62. Wolf WA, Roelofs WL (1987) Reinvestigation confirms action of △11-desaturases in spruce budworm moth sex pheromone biosynthesis. J Chem Ecol 13:1019–1027Google Scholar

Copyright information

© Georg Thieme Verlag Stuttgart 1991

Authors and Affiliations

  • Christer Löfstedt
    • 1
  • Wim M. Herrebout
    • 2
  • Steph B. J. Menken
    • 3
  1. 1.Department of EcologyLund UniversityLundSweden
  2. 2.Division of Systematics and Evolutionary BiologyUniversity of LeidenLeidenThe Netherlands
  3. 3.Institute of Taxonomic ZoologyUniversity of AmsterdamAmsterdamThe Netherlands

Personalised recommendations