Eur. J. Entomol. 113: 446-455, 2016 | 10.14411/eje.2016.058

Genetic identification of a non-native species introgression into wild population of the field cricket Gryllus campestris (Orthoptera: Gryllidae) in Central Europe

Hanna PANAGIOTOPOULOU1,2, Mateusz BACA3, Katarzyna BACA4, Paweł SIENKIEWICZ5, Piotr ŚLIPIŃSKI1, Michał ŻMIHORSKI6,7,*
1 Museum and Institute of Zoology, Polish Academy of Sciences, Wilcza 64, 00-679 Warsaw, Poland; e-mails: hpana@miiz.waw.pl, piotrs@miiz.waw.pl
2 Institute of Biochemistry and Biophysics, Polish Academy of Sciences, Pawińskiego 5a, 02-106 Warsaw, Poland
3 Center for Precolumbian Studies, University of Warsaw, Krakowskie Przedmieście 26/28, 00-927 Warsaw, Poland; e-mail: bacamat@gmail.com
4 Institute of Genetics and Biotechnology, Department of Biology, University of Warsaw, Pawińskiego 5a, 02-106 Warsaw, Poland; e-mail: katarzyna.ewa.pajak@gmail.com
5 Department of Entomology and Environmental Protection, Poznań University of Life Sciences, Dąbrowskiego 159, 60-594 Poznań, Poland; e-mail: ophonus@gmail.com
6 Institute of Nature Conservation, Polish Academy of Sciences, Mickiewicza 33, 31-120 Kraków, Poland; e-mail: michal.zmihorski@gmail.com
7 Department of Ecology, Swedish University of Agricultural Sciences, Box 7044, SE 750 07 Uppsala, Sweden

Two species of the genus Gryllus occur in Europe: G. campestris and G. bimaculatus. The first is widely distributed in the north-western Palaearctic, while the second, G. bimaculatus, occurs predominantly in the Mediterranean area. There is a visible pattern in the distribution of G. campestris, the insect being rare and threatened in the western part of its range, whereas it is still abundant in the east. Despite the fact that this species is commonly used in laboratory experiments, its natural populations are poorly characterised. In the present study, we analysed cricket populations from the lower Oder and Vistula River valleys in Poland. Based on the phylogeny of the mtDNA cytochrome b fragment, we found that 17% of the individuals studied had a G. bimaculatus-like mtDNA haplotype. Analyses of 11 autosomal microsatellite loci failed to reveal any clear genetic differentiation between individuals assigned to these two clades. This suggests, along with the spatial distribution of G. bimaculatus-like haplotypes, successful interbreeding of G. bimaculatus with native populations of G. campestris. However, both the nuclear data and additional analyses of two X-chromosome-linked microsatellite loci revealed incomplete introgression. Human-mediated introgression seems to be the most plausible explanation of the observed genotypic pattern such that caution needs to be taken in conservation efforts carried out in the western part of the species' range.

Keywords: Orthoptera, Gryllidae, Gryllus campestris, Gryllus bimaculatus, conservation, mtDNA, microsatellite loci, X-chromosome-linked markers

Received: November 9, 2015; Accepted: May 25, 2016; Published online: August 29, 2016

Download citation

References

  1. Andrés J.A., Larson E.L., Bogdanowicz S.M. & Harrison R.G. 2013: Patterns of transcriptome divergence in the male accessory gland of two closely related species of field crickets. - Genetics 193: 501-513. Go to original source...
  2. Bazyluk W. 1956: Klucze do oznaczania owadów Polski, XI Prostoskrzydłe - Orthoptera (Saltatoria). [A Key for the Identification of Insects of Poland XI, Orthoptera (Saltatoria).] PWN, Warsaw, 166 pp.
  3. Bazyluk W. & Liana A. 1990: Orthoptera (Saltatoria) - Prostoskrzydłe. In Razowski J. (eds): Wykaz zwierząt Polski, Tom I. [List of Animals of Poland, Vol. 1.] Wydawnictwo Polskiej Akademii Nauk, Ossolineum, Wrocław, Warszawa, Kraków, 4751 pp.
  4. Bazyluk W. & Liana A. 2000: Katalog Fauny Polski, Prostoskrzydłe - Orthoptera, XVII, 2. Muzeum i Instytut Zoologii PAN, Warsaw, 156 pp.
  5. Bellman H. 2006: Der Kosmos Heuschreckenführer. Die Arten Mitteleuropas sicher bestimmen. Franckh-Kosmos, Stuttgart, 355 pp.
  6. Bolnick D.I., Turelli M., López-Fernández H., Wainwright P.C. & Near T.J. 2008: Accelerated mitochondrial evolution and "Darwin's corollary": asymmetric viability of reciprocal F1 hybrids in Centrarchid fishes. - Genetics 178: 1037-1048. Go to original source...
  7. Bretman A., Dawson D.A., Horsburgh G.J. & Tregenza T. 2008: New microsatellite loci isolated from the field cricket Gryllus bimaculatus characterized in two cricket species, Gryllus bimaculatus and Gryllus campestris. - Mol. Ecol. Resour. 8: 1015-1019. Go to original source...
  8. Bretman A., Rodríguez-Muñoz R., Walling C., Slate J. & Tregenza T. 2011: Fine-scale population structure, inbreeding risk and avoidance in a wild insect population. - Mol. Ecol. 20: 3045-3055. Go to original source...
  9. Crispo E., Moore J.S., Lee Yaw J.A., Gray S.M. & Haller B.C. 2011: Broken barriers: Human-induced changes to gene flow and introgression in animals. - BioEssays 33: 508-518. Go to original source...
  10. Dawson D.A., Bretman A.J. & Tregenza T. 2003: Microsatellite loci for the field cricket, Gryllus bimaculatus and their cross-utility in other species of Orthoptera. - Mol. Ecol. Notes 3: 191-195. Go to original source...
  11. Dieringer D. & Schlötterer C. 2003: Microsatellite analyser (MSA): a platform independent analysis tool for large microsatellite data sets. - Mol. Ecol. Notes 3: 167-169. Go to original source...
  12. Earl D.A. & von Holdt B.M. 2012: Structure Harvester: a website and program for visualizing STRUCTURE output and implementing the Evanno method. - Conserv. Genet. Resour. 4: 359-361. Go to original source...
  13. Evanno G., Regnaut S. & Goudet J. 2005: Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. - Mol. Ecol. 14: 2611-2620. Go to original source...
  14. Excoffier L. & Lischer H.E.L. 2010: Arlequin suite ver 3.5: A new series of programs to perform population genetics analyses under Linux and Windows. - Mol. Ecol. Resour. 10: 564-567. Go to original source...
  15. Ferreira M. & Ferguason J.W.H. 2010: Do Mediterranean crickets Gryllus bimaculatus De Geer (Orthoptera: Gryllidae) come from the Mediterranean? Largescale phylogeography and regional gene flow. - Bull. Entomol. Res. 100: 49-58. Go to original source...
  16. Good J.M., Dean M.D. & Nachman M.W. 2008: A complex genetic basis to X-linked hybrid male sterility between two species of house mice. - Genetics 179: 2213-2228. Go to original source...
  17. Good J.M., Vanderpool D. & Keeble S. & Bi K. 2015: Negligible nuclear introgression despite complete mitochondrial capture between two species of chipmunks. - Evolution 69: 1961-7192. Go to original source...
  18. Goudet J. 2002: Fstat, Ver. 2.9.3.2. Institute of Ecology, Lausanne. http://www2.unil.ch/izea/softwares/fstat.html
  19. Grein G. 2000: Zur Verbreitung der Heuschrecken (Saltatoria) in Niedersachsen und Bremen. - Informationsdienst Natursch. Niedersachs. 20: 74-112.
  20. Grein G. 2005: Rote Liste der in Niedersachsen und Bremen gefahrdeten Heuschrecken mit Gesamtartenverzeichnis 3. Fassung. - Informationsdienst Natursch. Niedersachs. 25: 1-20.
  21. Hall T.A. 1999: BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. - Nucl. Acids Symp. Ser. 41: 95-98.
  22. Harrison R.G. 1983: Barriers to gene exchange between closely related cricket species. I. Laboratory hybridization studies. - Evolution 37: 245-251. Go to original source...
  23. Harrison R.G. 1986: Pattern and process in a narrow hybrid zone. - Heredity 56: 337-349. Go to original source...
  24. Harrison R.G., Rand D.M. & Wheeler W.C. 1987: Mitochondrial DNA variation in field crickets across a narrow hybrid zone. - Mol. Biol. Evol. 4: 144-158.
  25. Heller K.G., Korsunovskaya O., Ragge D.R., Vedenina V., Willemse F., Zhantiev R.D. & Frantsevich L. 1998: Check-list of European Orthoptera. - Articulata 7: 1-61.
  26. Hochkirch A. & Lemke I. 2011: Asymmetric mate choice, hybridization, and hybrid fitness in two sympatric grasshopper species. - Behav. Ecol. Sociobiol. 65: 1637-1645. Go to original source...
  27. Hochkirch A., Witzenberger K.A., Teerling A. & Niemeyer F. 2007: Translocation of an endangered insect species, the field cricket (Gryllus campestris Linnaeus, 1758) in northern Germany. - Biodivers. Conserv. 16: 3597-3607. Go to original source...
  28. Holusa J. 2012: Grasshoppers and bushcrickets regionally extinct in the Czech Republic: consequence of the disappearance of habitats scattered on the edge of their ranges. - J. Insect Conserv. 16: 949-960. Go to original source...
  29. Holusa J., Kocarek P., Marhoul P. & Skokanova H. 2012: Platycleis vittata (Orthoptera: Tettigoniidae) in the northwestern part of its range is close to extinction: is this the result of landscape changes? - J. Insect Conserv. 16: 295-303. Go to original source...
  30. Huang Y., Ortí G., Sutherlin M., Duhachek A. & Zera A. 2000: Phylogenetic relationships of north American field crickets inferred from mitochondrial DNA data. - Mol. Phylogenet. Evol. 17: 48-57. Go to original source...
  31. Jakobsson M. & Rosenberg N.A. 2007: CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. - Bioinformatics 23: 1801-1806. Go to original source...
  32. Jang Y. & Gerhardt H.C. 2006: Divergence in the calling songs between sympatric and allopatric populations of the southern wood cricket Gryllus fultoni (Orthoptera: Gryllidae). - J. Evol. Biol. 19: 459-472. Go to original source...
  33. Larson E.L., Hume G.L., Andrés J.A. & Harrison R.G. 2012: Post-mating prezygotic barriers to gene exchange between hybridizing field crickets. - J. Evol. Biol. 25: 174-186. Go to original source...
  34. Maroja L.S., Andrés J.A., Walters J.R. & Harrison R.G. 2009: Multiple barriers to gene exchange in a field cricket hybrid zone. - Biol. J. Linn. Soc. 97: 390-402. Go to original source...
  35. Maroja L., McKenzie Z.M., Hart E., Jing J., Larson E.L. & Richardson D.P. 2014: Barriers to gene exchange in hybridizing field crickets: the role of male courtship effort and cuticular hydrocarbons. - BMC Evol. Biol. 14: 65. Go to original source...
  36. Nei M., Tajima F. & Tateno Y. 1983: Accuracy of estimated phylogenetic trees from molecular data. - J. Mol. Evol. 19: 153-170. Go to original source...
  37. Paekal R. & Smouse P.E. 2006: GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. - Mol. Ecol. Notes 6: 288-295. Go to original source...
  38. Panagiotopoulou H., Baca M., Baca K., Stanoković A. & Żmihorski M. 2015: Optimization and validation of a multiplex assay for microsatellite loci analysis in the field cricket, Gryllus campestris (Orthoptera: Gryllidae). - J. Asia Pac. Entomol. 18: 421-424. Go to original source...
  39. Pritchard J.K., Stephens M. & Donnelly P. 2000: Inference of population structure using multilocus genotype data. - Genetics 155: 945-959.
  40. R Core Team 2015: R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, http://www.R-project.org/
  41. Raymond M. & Rousset F. 1995: Genepop (version 1.2): population genetics software for exact tests and ecumenicism. - J. Hered. 86: 248-249.
  42. Ritz M.S. & Kӧhler G. 2007: Male behaviour over the season in a wild population of the field cricket Gryllus campestris L. - Ecol. Entomol. 32: 384-392. Go to original source...
  43. Rodríguez-Muñoz R., Bretman A., Slate J., Walling C.A. & Tregenza T. 2010: Natural and sexual selection in a wild insect population. - Science 328: 1269-1272. Go to original source...
  44. Ronquist F. & Huelsenbeck J.P. 2003: MRBAYES 3: Bayesian phylogenetic inference under mixed models. - Bioinformatics 19: 1572-1574. Go to original source...
  45. Rosenberg N.A. 2004: DISTRUCT: a program for the graphical display of population structure. - Mol. Ecol. Notes 4: 137-138. Go to original source...
  46. Simmons L.W. 1986: Female choice in the field cricket, Gryllus bimaculatus (de Geer). - Anim. Behav. 34: 1463-1470. Go to original source...
  47. Simmons L.W. 1991: Female choice and the relatedness of mates in the field cricket, Gryllus bimaculatus. - Anim. Behav. 41: 493-501. Go to original source...
  48. Tamura K., Peterson D., Peterson N., Stecher G., Nei M. & Kumar S. 2011: MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. - Mol. Biol. Evol. 28: 2731-2739. Go to original source...
  49. Toews D.P. & Brelsford A. 2012: The biogeography of mitochondrial and nuclear discordance in animals. - Mol Ecol. 21: 3907-3930. Go to original source...
  50. Tryjanowski P., Hartel T., Baldi A., Szymański P., Tobółka M., Herzon I., Goławski A., Konvicka M., Hromada M., Jerzak L., Kujawa K., Lenda M., Orłowski G., Panek M., Skórka P., Sparks T.H., Tworek S., Wuczyński A. & Żmihorski M. 2011: Conservation of farmland birds faces different challenges in Western and Central-Eastern Europe. - Acta Ornithol. 46: 1-12. Go to original source...
  51. Turelli M. & Moyle L.C. 2007: Asymmetric postmating isolation: Darwin's corollary to Haldane's rule. - Genetics 176: 1059-1088. Go to original source...
  52. Tyler F., Harrison X.A., Bretman A., Veen T., Rodríguez-Muñoz R. & Tregenza T. 2013: Multiple post-mating barriers to hybridization in field crickets. - Mol. Ecol. 22: 1640-1649. Go to original source...
  53. Untergasser A., Cutcutache I., Koressaar T., Ye J., Faircloth B.C., Remm M. & Rozen S.G. 2012: Primer3 - New capabilities and interfaces. - Nucl. Acids Res. 40(15): e115, 12 pp. Go to original source...
  54. Van Oosterhout C., William F., Hutchinson D.P., Wills M. & Shipley P. 2004: Micro-Checker: software for identifying and correcting genotyping errors in microsatellite data. - Mol. Ecol. Notes 4: 535-538. Go to original source...
  55. Veen T., Faulks J., Tyler F., Lloyd J. & Tregenza T. 2011: Premating reproductive barriers between hybridising cricket species differing in their degree of polyandry. - PLoS ONE 6(5): e19531, 7 pp. Go to original source...
  56. Veen T., Faulks J., Tyler F., Lloyd J. & Tregenza T. 2013: Diverse reproductive barriers in hybridising crickets suggests extensive variation in the evolution and maintenance of isolation. - Evol. Ecol. 27: 993-1015. Go to original source...
  57. Witzenberger K.A. & Hochkirch A. 2008: Genetic consequences of animal translocations: A case study using the field cricket, Gryllus campestris L. - Biol. Conserv. 141: 3059-3068. Go to original source...