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2019 | 69 | 2 |

Tytuł artykułu

Microsatellite polymorphism suggests high genetic diversity but disrupted gene flow in the two-spot ladybird Adalia bipunctata (Linnaeus, 1758) (Coleoptera: Coccinellidae) populations from diverse environments

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Języki publikacji

EN

Abstrakty

EN
The two-spot ladybird Adalia bipunctata (Linnaeus, 1758) (Coleoptera: Coccinellidae) is a widely distributed generalist, feeding preferably on aphids. The species inhabits various environments, including anthropogenic landscape, where pollution and microclimate enables to attain very high numbers of favorite prey. Recently, the abundance of the two-spot ladybird has declined, mainly as an after-effect of invasion of the competing species — the harlequin ladybird Harmonia axyridis (Pallas, 1773). High phenotypic polymorphisms made the two-spot ladybird classic model for population genetic studies of Coccinellidea. However, studies investigating diversity of the species at DNA level have Coccinellidae been scarce. In our investigation we used microsatellite markers to characterize genetic diversity in the two-spot ladybird populations from different environments. We made an attempt to amplify 13 loci, identified previously in the genome of the species, however due to lack of amplification, monomorphisms and presence of the null alleles, the final set of six markers useful for analysis on a population level was obtained. Analyzing genotypes of 124 individuals, we confirmed high genetic diversity of the species, suggested previously by studies, applying allozymes and mitochondrial DNA. Also, microsatellites revealed weakly pronounced genetic structure in a large scale (localities separated by a distance of 500 kilometers). However, we found some indications (signs of the Wahlund effect) that gene flow could be disturbed among sites in diverse environments (rural, suburban and urban). Our data suggested that invasion of the harlequin ladybird has not yet affected populations of the two-spot in such extent to alter genetic diversity or genetic structure.

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-

Czasopismo

Rocznik

Tom

69

Numer

2

Opis fizyczny

p.477-486,fig.,ref.

Twórcy

autor
  • Museum and Institute of Zoology, Polish Academy of Sciences, Warsaw 00-679, Wilcza 64, Poland
  • Museum and Institute of Zoology, Polish Academy of Sciences, Warsaw 00-679, Wilcza 64, Poland
autor
  • Faculty of Biology and Environmental Sciences, Cardinal Stefan Wyszynski University in Warsaw, 01-938 Warsaw, K.Woycickiego 1/3, Poland
autor
  • Department of Entomology, Phytopathology and Molecular Diagnostic, University of Warmia and Mazury in Olsztyn, Olsztyn 10-720, R.Prawochenskiego 17, Poland
  • Museum and Institute of Zoology, Polish Academy of Sciences, Warsaw 00-679, Wilcza 64, Poland
  • Department of Plant Protection, Wroclaw University of Environmental and Life Sciences, Wroclaw 50-363, Grunwaldzki Square 24a, Poland
  • Department of Plant Protection, Wroclaw University of Environmental and Life Sciences, Wroclaw 50-363, Grunwaldzki Square 24a, Poland

Bibliografia

  • 1. Balayeva, N. M., Eremeeva, M. E., Tissot-Dupont, H., Zakharov, I. A., and D. Raoult. 1995. Genotype characterization of the bacterium expressing the male-killing trait in the ladybird beetle Adalia bipunctata with specific rickettsial molecular tools. Applied and Environmental Microbiology, 61: 1431–1437.
  • 2. Bjørklund, M., Ruiz, I., and J. C. Senar. 2010. Genetic differentiation in the urban habitat: the great tits (Parus major) of the parks of Barcelona city. Biological Journal of the Linnean Society, 99: 9–19.
  • 3. Brakefield, P. M. 1984. Ecological studies on the polymorphic ladybird Adalia bipunctata in the Netherlands. I. Population biology and geographical variation in melanism. Journal of Animal Ecology, 53: 761–774.
  • 4. Brakefield, P. M., and P. G. Willmer. 1985. The basis of thermal melanism in the ladybird Adalia bipunctata: differences in reflectance and thermal properties between the morphs. Heredity, 54: 9–14.
  • 5. Brookfield, J. F. Y. 1996. A simple new method for estimating null allele frequency from heterozygote deficiency. Molecular Ecology, 5: 453–455.
  • 6. Brown, P. M. J., Thomas, C. E., Lombaert, E., Jeffries, D. L., Estoup, A., and L.-J. L. Handley. 2011. The global spread of Harmonia axyridis (Coleoptera: Coccinellidae): distribution, dispersal and routes of invasion. BioControl, 56: 623–641
  • 7. Burakowski, B., Mroczkowski, M., and J. Stefańska. 1986. Katalog Fauny Polski, Część XXIII, Tom 13. Chrząszcze Coleoptera, Cucujoidea, cz. 2. PWN, Warszawa, 278 pp.
  • 8. Ceryngier, P., Romanowski, J., and M. Romanowski. 2016. Biedronkowate (Coleoptera: Coccinellidae) Parku Skaryszewskiego w Warszawie. In: J. Romanowski (eds) Park Skaryszewski w Warszawie – przyroda i użytkowanie. Wydawnictwo UKSW, Warszawa, 177–186 pp.
  • 9. Chapin, J. B., and V. A. Brou. 1991. Harmonia axyridis (Pallas), the third species of the genus to be found in the United States (Coleoptera: Coccinellidae). Proceedings of the Entomological Society of Washington, 93: 630–635.
  • 10. Chapuis, M.-P., and A. Estoup. 2007. Microsatellite null alleles and estimation of population differentiation. Molecular Biology and Evolution, 24: 621–631.
  • 11. Czechowska, W., and R. Bielawski. 1981. Coccinellids (Coleoptera, Coccinellidae) of Warsaw and Mazovia. Memorabilia Zoologica, 34: 181–197.
  • 12. Dąbrowski, M. J., Bornelöv, S., Kruczyk, M., Baltzer, N., and J. Komorowski. 2015. ‘True’ null allele detection in microsatellite loci: a comparison of methods, assessment of difficulties and survey of possible improvements. Molecular Ecology Resources, 15: 477–488.
  • 13. De Meeûs, T. 2018. Revisiting FIS, FST, Wahlund effects and null alleles. The Journal of Heredity, 109: 446–456.
  • 14. Desender, K., Small, E., Gaublomme, E., and P. Verdyck. 2005. Rural-urban gradients and the population genetic structure of woodland ground beetles. Conservation Genetics, 6: 51–62.
  • 15. Dimetry, N. Z. 1976. The role of predator and prey densities as factors affecting behavioural and biological aspects of Adalia bipunctata (L.) larvae. Zeitschrift fur Angewandte Entomologie, 81: 386–392.
  • 16. Dudek, K., Sienkiewicz, P., Gwiazdowicz, D. J., and P. Tryjanowski. 2017. A “clean” alien species? Parasites of the invasive ladybird Harmonia axyridis (Coleoptera: Coccinellidae). European Journal of Entomology, 114: 350–354.
  • 17. Engelstädter, J., and G. D. D. Hurst. 2007. The impact of male-killing bacteria on host evolutionary processes. Genetics, 175: 245–254.
  • 18. Gillespie, J. H. 2004. Nonrandom mating. In: Population Genetics: a concise guide. The Johns Hopkins University-Press, Baltimore, Maryland, pp. 119–138.
  • 19. Gordon, R. D. 1985. The Coccinellidae (Coleoptera) of America North of Mexico. Journal of the New York Entomological Society, 93: 1–912.
  • 20. Gortat, T., Rutkowski, R., Gryczyńska, A., Kozakiewicz, A., and M. Kozakiewicz. 2017. The spatial genetic structure of the yellow-necked mouse in an urban environment — a recent invader vs. a closely related permanent inhabitant. Urban Ecosystems, 20: 581–594.
  • 21. Gortat, T., Rutkowski, R., Gryczyńska, A., Pieniążek, A., Kozakiewicz, A., and M. Kozakiewicz. 2015. Anthropopressure gradients and the population genetic structure of Apodemus agrarius. Conservation Genetics, 16: 649–659.
  • 22. Gortat, T., Rutkowski, R., Gryczyńska-Siemiątkowska, A., Kozakiewicz, A., and M. Kozakiewicz. 2013. Genetic structure in urban and rural populations of Apodemus agrarius in Poland. Mammalian Biology, 78: 171–177.
  • 23. Goryacheva, I. I. and A. V. Blekhman. 2017. Genetic structure of native and invasive populations of Harmonia axyridis Pall. in the light of global invasion. Russian Journal of Genetics, 53: 9–20
  • 24. Goudet, J. 2001. FSTAT V2.9.3, a program to estimate and test gene diversities and fixation indices. Available: http://www.unil.ch/izea/softwares/fstat.htlm
  • 25. Haddrill, P. R., Majerus, M. E. N., and S. Mayes. 2002. Isolation and characterization of highly polymorphic microsatellite loci in the 2-Spot Ladybird, Adalia bipunctata. Molecular Ecology Notes, 2: 316–319.
  • 26. Haddrill, P. R., Shuker, D. M., Amos, W., Majerus, M. E. N., and S. Mayes. 2008. Female multiple mating in wild and laboratory populations of the two-spot ladybird, Adalia bipunctata. Molecular Ecology, 17: 3189–3197.
  • 27. Harmon, J. P., Stephens, E., and J. Losey. 2007. The decline of native coccinellids (Coleoptera: Coccinellidae) in the United States and Canada. Journal of Insect Conservation, 11: 85–94.
  • 28. Hodek, I., and A. Honék. 1996. Ecology of Coccinellidae. Kluwer Acad. Publ., Dordrecht, Boston, pp. 480.
  • 29. Hodek, I., and P. Ceryngier. 2000. Sexual activity in Coccinellidae (Coleoptera): a review. European Journal of Entomology, 97: 449–456.
  • 30. Hodek, I., Iperti, G., and M. Hodková. 1993. Long-distance flights in Coccinellidae (Coleoptera). European Journal of Entomology, 90: 403–414.
  • 31. Hurst, G. D. D., and F. M. Jiggins. 2000. Male-killing bacteria in insects: mechanisms, incidence, and implications. Emerging Infectious Diseases, 6: 329–336.
  • 32. Kalinowski, S. T. 2005. HP-RARE 1.0: a computer program for performing rarefaction on measures of allelic richness. Molecular Ecology Notes, 5: 187–189.
  • 33. Kovář, I. 2007. Family Coccinellidae Latreille, 1807. In: I. Löbl and A. Smetana (eds) Catalogue of Palaearctic Coleoptera, Vol. 4. Apollo Books, Stenstrup, pp. 568–631.
  • 34. Krafsur, E. S., Nariboli, P., and J. J. Obrycki. 1996. Gene flow and diversity at allozyme loci in the two-spotted lady beetle (Coleoptera: Coccinellidae). Annals of the Entomological Society of America, 89: 410–419.
  • 35. Krafsur, E. S., Obrycki, J. J. and J. D. Harwood. 2005. Comparative genetic studies of native and introduced Coccinellidae in North America. European Journal of Entomology, 102: 469–474.
  • 36. Lee, C. E. 2002. Evolutionary genetics of invasive species. Trends in Ecology and Evolution, 17: 386–391.
  • 37. Lombaert, E., Guillemaud, T., Thomas, C. E., Lawson Handley, L. J., Li, J., Wang, S., Pang, H., Goryacheva, I., Zakharov, I. A., Jousselin, E., Poland, R. L., Migeon, A., Van Lenteren, J., Clercq, D. E. P., Berkvens, N., Jones, W., and A. Estoup. 2011. Inferring the origin of populations introduced from a genetically structured native range by approximate Bayesian computation: case study of the invasive ladybird Harmonia axyridis. Molecular Ecology, 20: 4654–4670.
  • 38. Majerus, M. N. E. 1994. Ladybirds. Harper Collins, London, pp. 367.
  • 39. Mikkola, K., and A. Albrecht. 1988. The melanism of Adalia bipunctata around the Gulf of Finland as an industrial phenomenon. Annales Zoologici Fennici, 25: 177–185.
  • 40. Nei, M., and A. K. Roychoudhury. 1974. Sampling variances of heterozygosity and genetic distance. Genetics, 76: 379–390.
  • 41. Omkar, and A. Pervez. 2005. Ecology of two-spotted ladybird, Adalia bipunctata: a review. Journal of Applied Entomology, 129: 465–474.
  • 42. O'Donald, P., and J. Muggleton. 1979. Melanie polymorphism in ladybirds maintained by sexual selection. Heredity, 43: 143–148.
  • 43. Paekall, R., and P. E. Smouse. 2001. GenAlEx V5: Genetic Analysis in Excel. Population genetic software for teaching and research. Available: http://www.anu.ed.au/BoZo/GenAlEx/
  • 44. Palenko, M. V., Andrianov, B. V., Romanov, D. A., and I. A. Zakharov. 2018. Geographical ecocline polymorphism of the pistribution of mitochondrial haplotypes of Adalia bipunctata Linnaeus, 1758 (Coleoptera: Coccinellidae) of Norway. Russian Journal of Genetics, 54: 451–456.
  • 45. Petit, R. J., El Mousadik, A., and O. Pons. 1998. Identifying populations for conservation on the basis of genetic markers. Conservation Biology, 12: 844–855.
  • 46. Pritchard, J. K., Stephens, M., and P. Donnelly. 2000. Inference of population structure using multilocus genotype data. Genetics, 155: 945–959.
  • 47. Puillandre, N., Dupas, S., Dangles, O., Zeddam, J.-L., Capdevielle-Dulac, C., Barbin, K., Torres-Leguizamon, M., and J.F. Silvain. 2008. Genetic bottleneck in invasive species: the potato tuber moth adds to the list. Biological Invasions, 10: 319–333.
  • 48. R Core Team. 2017. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available: https://www.R-project.org/
  • 49. Raymond, M., and F. Rousset. 1995. GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. Journal of Heredity, 86: 248–249.
  • 50. Reiner, G., Lang, M., and H. Willems. 2019. Impact of different panels of microsatellite loci, different numbers of loci, sample sizes, and gender ratios on population genetic results in red deer. European Journal of Wildlife Research, 65: 25.
  • 51. Romanowski, J., Ceryngier, P., Piotrowska, M., Romanowski, M., and D. Sitarska. 2017. Biedronkowate (Coleoptera: Coccinellidae) Miejskiego Ogrodu Zoologicznego w Warszawie. Wiadomości Entomologiczne, 36: 212–220.
  • 52. Rousset, F. 2008. Genepop'007: a complete re-implementation of the Genepop software for Windows and Linux. Molecular Ecology Resources, 8: 103–106.
  • 53. Roy, H. E., Adriaens, T., Isaac, N. J. B., Kenis, M., Onkelinx, T., Martin, G. S., Brown, P. M. J., Hautier, L., Poland, R., Roy D. B., Comont R., Eschen, R., Frost, R., Zindel, R., Van Vlaenderen J., Nedvěd, O., Ravn, H. P., Grégoire, J.-C., Biseau J.-C., and D. Maes. 2012. Invasive alien predator causes rapid declines of native European ladybirds. Diversity and Distributions, 18: 717–725.
  • 54. Roy, H. E., Brown, P. M. J., Adriaens, T., Berkvens, N., Borges, I., Clusella-Trullas, S., Comont, R. F., De Clercq, P., Eschen, R., Estoup, A. et al. 2016. The harlequin ladybird, Harmonia axyridis: global perspectives on invasion history and ecology. Biological Invasions, 18: 997–1044.
  • 55. Rubin, C. S., Warner, R. E., Bouzat, J. L.; and K. N. Paige. 2001. Population genetic structure of Blanding's turtles (Emydoidea blandingii) in an urban landscape. Biological Conservation, 99: 323–330.
  • 56. Rutkowski R., Kosewska A., Ceryngier P., Szczepański S., Wawer W., Twardowska K., and J. Twardowski. 2017. Genetic diversity of an invasive invertebrate in an urban environment, as exemplified by the Harlequin ladybird Harmonia axyridis (Pallas, 1773). Annales Zoologici, 67: 759–772.
  • 57. Sakuratani, Y., Matsumoto, Y., Oka, M., Kubo, T., Fujii, A., Uotani, M., and T. Teraguchi. 2000. Life history of Adalia bipunctata (Coleoptera: Coccinellidae) in Japan. European Journal of Entomology, 97: 555–558.
  • 58. Saxena, S., Mishra, G., and Omkar. 2018. Familiarity dominates relatedness in mate selection in ladybirds. Journal of Zoology, 304: 55–64.
  • 59. Schulenburg, J. H. G. V. D., Hurst, G. D. D., Tetzlaff, D., Booth, G. E., Zakharov, I. A., and M. E. N. Majerus. 2002. History of infection with different male-killing bacteria in the two-spot ladybird beetle Adalia bipunctata revealed through mitochondrial DNA sequence analysis. Genetics, 160: 1075–1086.
  • 60. Selkoe, K. A., and R. J. Toonen. 2006. Microsatellites for ecologists: a practical guide to using and evaluating microsatellite markers. Ecology Letters, 9: 615–629.
  • 61. Sloggett, J. J., and A. Honěk. 2012. Genetic studies. In: I. Hodek, H. F. van Emden, and A. Honěk (eds) Ecology and behaviour of the ladybird beetles. Wiley-Blackwell, Chichester, pp. 13–53.
  • 62. Sloggett, J. J. 2017. Harmonia axyridis (Coleoptera: Coccinellidae): Smelling the rat in native ladybird declines. European Journal of Entomology, 114: 455–461.
  • 63. Susset, E. C., Hemptinne, J. L., Danchin, E., and A. Magro. 2018. Overwintering aggregations are part of Hippodamia undecimnotata's (Coleoptera: Coccinellidae) mating system. PLoS ONE, 13: e0197108.
  • 64. Takami, Y., Koshio, C., Ishii, M., Fujii, H., Hidaka, T., and I. Shimizu. 2004. Genetic diversity and structure of Urban populations of Pieris butterflies assessed using amplified fragment length polymorphism. Molecular Ecology, 13: 245–258.
  • 65. Thomas, A. P., Trotman, J., Wheatley, A., Aebi, A., Zindel, R., and P. M. J. Brown. 2013. Predation of native coccinellids by the invasive alien Harmonia axyridis (Coleoptera: Coccinellidae): detection in Britain by PCR-based gut analysis. Insect Conservation and Diversity, 6: 20–27.
  • 66. Van Oosterhout, C., Hutchinson, W. F., Wills, D. P. M., and P. Shipley. 2004. MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Molecular Ecology Notes, 4: 535–538.
  • 67. Waples, R. S. 2015. Testing for Hardy-Weinberg proportions: have we lost the plot? Journal of Heredity, 106: 1–19.
  • 68. Waples, R. S. 2018. Null alleles and FIS × FST correlations. Journal of Heredity, 109.
  • 69. Wood, B. C., and A. S. Pullin. 2002. Persistence of species in a fragmented urban landscape: the importance of dispersal ability and habitat availability for grassland butterflies. Biodiversity and Conservation, 11: 1451–1468.
  • 70. Zakharov, I. A. 1995. Two-spot ladybird Adalia bipunctata as a genetic model. Genetitka (Moscow), 31: 149–161.

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Bibliografia

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