A Preliminary mitochondrial cytochrome c oxidase-I-based phylogeographic and phylogenetic analysis of Eurasian Acanthocinus griseus (Coleoptera, Cerambycidae)

Abstract

Acanthocinus griseus (Fabricius, 1792) (Coleoptera: Cerambycidae, Lamiinae, Acanthocinini) has long been known for its role in the decay process of the wood in the forest ecosystem, and two critical features of the species, inhabiting standing trees and being a vector of pine wood nematodes Bursaphelenchus spp., have been noted recently. Therefore, understanding the current relationships and possible migration scenarios has been further required to assess invasion risks. The present work provided a preliminary comprehension of the phylogenetic relationships of A. griseus based on the mitochondrial cytochrome c oxidase-I (COI) gene region (658 bp), with sequences produced in the present study, from the specimens collected from timberyards, ports and forests of Kocaeli Province, Turkey, and with available sequences in GenBank of inhabitants of Eurasia, and of intercepted specimens in ports. The intraspecific genetic distance of A. griseus was 1.37-0,3%, while the interspecific distance was 10,79-13,37%, except the closeness of an A. griseus haplotype (AGR1) to A. sachalinensis (0,3%) more than its conspecifics (4,71-5,47%). The ML and BI analyses suggested identical topologies. The statistical parsimony network drew a reticular branching diagram without grouping across countries or geographic regions, which addresses ongoing gene flow. Most haplotypes from Turkey were clustered around a central haplotype (AGR11), which may point to a bottleneck effect. A haplotype previously intercepted in USA ports was identical to a haplotype sampled in Kocaeli. The present study suggests that the relationship between A. griseus and A. sachalinensis should be reconsidered from both morphological and molecular points of view. In addition, the possible ongoing intraspecific gene flow within A. griseus might be due to facilitated migration by the international wood trade.

Keywords

• Intraspecific gene flow
• shared haplotype
• international wood trade
• migration
• vector
• pine wilt nematode.

Kaynakça

1. Allen, E., Noseworthy, M., Ormsby, M. (2017). Phytosanitary measures to reduce the movement of forest pests with the international trade of wood products. Biological invasions, 19, 3365-3376. https://doi.org/10.1007/s10530-017-1515-0
2. Aksöyek, E., İbiş, O., Özcan, S., Moradi, M., Tez, C. (2017). DNA barcoding of three species (Canis aureus, Canis lupus and Vulpes vulpes) of Canidae. Mitochondrial DNA Part A 28(5), 747-755. doi.org/10.1080/24701394.2016.1180512
3. Armstrong, K.F., Ball, S.L. (2005). DNA barcodes for biosecurity: invasive species identification. Philosophical Transactions of the Royal Society B: Biological Sciences, 360(1462), 1813-1823.
4. Atak, Ş., Uçkan, F. Ayoub, H.K.S. (2021). A faunistic study on Cerambycidae (Coleoptera) of Kocaeli province (Turkey). Bitki Koruma Bülteni 61(2), 33-43. doi.org/10.16955/bitkorb.796414
5. Ayberk, H., Ozdikmen, H., Cebeci, H. (2014). A serious pest alert for Turkey: a newly introduced invasive longhorned beetle, Anoplophora glabripennis (Cerambycidae: Lamiinae). Florida Entomologist, 97(4), 1852-1855.
6. Bense, U. (1995). Longhorn Beetles: Illustrated Key to the Cerambycidae and Vesperidae of Europe=Bockkäfer (117). Weikersheim, Germany, Margraf Verlag.
7. Bílý, S., Mehl, O. (1989). Longhorn Beetles (Coleoptera, Cerambycidae) of Fennoscandia and Denmark (22). Leiden, Brill.
8. Cocoş, D., Etxebeste, I., Schroeder, M. (2017). An efficient detection method for the red‐listed beetle Acanthocinus griseus based on attractant‐baited traps. Insect Conservation and Diversity, 10(4), 294-301. https://doi.org/10.1111/icad.12224s

9. Collins, R.A., Armstrong, K.F., Meier, R., Yi, Y., Brown, S.D., Cruickshank, R.H., Keeling, S., Johnston, C. (2012). Barcoding and border biosecurity: identifying cyprinid fishes in the aquarium trade. PloS one, 7(1), e28381.
10. Çakmak, Y.E., Ayoub, H.K.S. Uckan, F. (2019). Size divergence of Rhagium inquisitor: sexual similarity versus environmental variability. Feb-Fresenius Environmental Bulletin 28, 7593-7602.
11. Çakmak, Y.E., Soydabaş-Ayoub, H.K. Uckan, F. (2020). A preliminary phylogenetic analysis of ribbed-pine-borer (Rhagium inquisitor) based on mitochondrial COI sequences. Journal of Asia-Pacific Entomology 23(3), 809-815. doi.org/10.1016/j.aspen.2020.06.008
12. Dearborn, K. W., Heard, S. B., Sweeney, J., Pureswaran, D. S. (2016). Displacement of Tetropium cinnamopterum (Coleoptera: Cerambycidae) by its invasive congener Tetropium fuscum. Environmental Entomology, 45(4), 848-854.
13. Edgar, R.C. (2004). MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic acids research 32(5), 1792-1797. doi.org/10.1093/nar/gkh340
14. Folmer, O., Black, M., Hoeh, W., Lutz, R., Vrijenhoek, R. (1994). DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3(5), 294-299.
15. Fukuda, K. (1997). Physiological process of the symptom development and resistance mechanism in pine wilt disease. Journal of forest research, 2(3), 171-181.
16. Grebennikov, V.V., Jendek, E., Smirnov, M.E. (2017). Diagnostic and phylogenetic utility of the first DNA barcode library for longhorn beetles (Coleoptera: Cerambycidae) from the Russian Far East. Zootaxa, 4276(3), 441-445.
17. Guindon, S., Dufayard, J.F., Lefort, V., Anisimova, M., Hordijk, W. Gascuel, O. (2010). New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Systematic Biology, 59(3), 307-321. doi.org/10.1093/sysbio/syq010
18. Haack, R.A., Britton, K.O., Brockerhoff, E.G., Cavey, J.F., Garrett, L.J., Kimberley, M., Lowenstein, F., Nuding, A., Olson, L.J., Turner, J., Vasilaky, K.N. (2014). Effectiveness of the International Phytosanitary Standard ISPM No. 15 on reducing wood borer infestation rates in wood packaging material entering the United States. PLoS One 9(5).
19. Hajibabaei, M., Smith, M. A., Janzen, D. H., Rodriguez, J. J., Whitfield, J. B., Hebert, P. D. (2006). A minimalist barcode can identify a specimen whose DNA is degraded. Molecular Ecology Notes, 6(4), 959-964.
20. Hebert, P. D., Ratnasingham, S., De Waard, J. R. (2003). Barcoding animal life: cytochrome c oxidase subunit 1 divergences among closely related species. Proceedings of the Royal Society of London. Series B: Biological Sciences, 270(suppl_1), S96-S99.
21. Hebert, P.D., Penton, E.H., Burns, J.M., Janzen, D.H., Hallwachs, W., (2004a). Ten species in one: DNA barcoding reveals cryptic species in the neotropical skipper butterfly Astraptes fulgerator. Proceedings of the National Academy of Sciences, 101(41), 14812-14817.
22. Hebert, P.D., Stoeckle, M.Y., Zemlak, T.S., Francis, C.M., (2004b). Identification of birds through DNA barcodes. PLoS Biol. 2 (10).
23. Hernández-Triana, L.M., Chaverri, L.G., Rodriguez-Perez, M.A., Prosser, S.W., Hebert, P.D., Gregory, T.R., Johnson, N. (2015). DNA barcoding of Neotropical black flies (Diptera: Simuliidae): Species identification and discovery of cryptic diversity in Mesoamerica. Zootaxa, 3936(1), 93-114.
24. Hulme, P.E. (2009). Trade, transport and trouble: managing invasive species pathways in an era of globalisation. Journal of Applied Ecology, 46(1), 10-18.
25. Hurst, G.D., Jiggins, F.M. (2005). Problems with mitochondrial DNA as a marker in population, phylogeographic and phylogenetic studies: the effects of inherited symbionts. Proceedings of the Royal Society B: Biological Sciences, 272(1572), 1525-1534.
26. Kearse, M., Moir, R., Wilson, A., Stones-Havas, S., Cheung, M., Sturrock, S., ... Drummond, A. (2012) Geneious Basic: an integrated and extendable desktop software platform for the organisation and analysis of sequence data. Bioinformatics, 28(12), 1647-1649. doi.org/10.1093/bioinformatics/bts199
27. Kumar, S., Stecher, G., Li, M., Knyaz, C., Tamura, K. (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Molecular Biology and Evolution, 35(6), 1547. doi.org/10.1093/molbev/msy096
28. Lanfear, R., Frandsen, P.B., Wright, A.M., Senfeld, T., Calcott, B. (2017). PartitionFinder 2: new methods for selecting partitioned models of evolution for molecular and morphological phylogenetic analyses. Molecular Biology and Evolution, 34(3), 772-773.
29. Leigh, J. W., Bryant, D. (2015) POPART: full-feature software for haplotype network construction. Methods in Ecology and Evolution 6(9), 1110-1116. doi.org/10.1111/2041-210X.12410
30. Lindhe, A., Jeppsson, T., Ehnström, B. (2010). Longhorn beetles in Sweden-changes in distribution and abundance over the last two hundred years. Entomologisk Tidskrift, 131(4), 241-508.
31. Linit, M. J. (1988). Nematode-vector relationships in the pine wilt disease system. Journal of Nematology, 20, 227-235.
32. Martikainen, P. (2002). Ecology and conservation status of Acanthocinus griseus (Fabricius, 1792)(Coleoptera: Cerambycidae) in Finland. Entomologica Fennica, 13(1), 41-50.
33. Moritz, C., Cicero, C. Godfray, C. (2004) DNA barcoding: promise and pitfalls. PLoS biology 2(10), e354. doi.org/10.1371/journal.pbio.0020354
34. Paterson, I.D., Mangan, R., Downie, D.A., Coetzee, J.A., Hill, M.P., Burke,A. M., ... Compton, S.G. (2016). Two in one: cryptic species discovered in biological control agent populations using molecular data and crossbreeding experiments. Ecology and Evolution, 6(17), 6139-6150.
35. Pentinsaari, M., Hebert, P.D., Mutanen, M. (2014) Barcoding beetles: a regional survey of 1872 species reveals high identification success and unusually deep interspecific divergences. PLoS One 9(9): e108651. doi.org/10.1371/journal.pone.0108651
36. Richards, E.J., Servedio, M.R., Martin, C.H. (2019) Searching for sympatric speciation in the genomic era. BioEssays, 41(7), 1900047. doi.org/10.1002/bies.201900047
37. Roderick, G. K. (1996). Geographic structure of insect populations: gene flow, phylogeography, and their uses. Annual Review of Entomology, 41(1), 325-352.
38. Ronquist, F., Huelsenbeck, J.P. (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19(12), 1572-1574. doi.org/10.1093/bioinformatics/btg180
39. Rougerie R., Lopez-Vaamonde C., Barnouin T., Delnatte J., Moulin N., Noblecourt T., Nusillard B., Parmain G., Soldati F. Bouget C. (2015) PASSIFOR: A reference library of DNA barcodes for French saproxylic beetles (Insecta, Coleoptera). Biodiversity Data Journal, 3: e4078. doi: 10.3897/BDJ.3.e4078
40. Rozas, J., Ferrer-Mata, A., Sánchez-DelBarrio, J.C., Guirao-Rico, S., Librado, P., Ramos-Onsins, S. E., Sánchez-Gracia, A. (2017). DnaSP 6: DNA sequence polymorphism analysis of large data sets. Molecular Biology and Evolution, 34(12), 3299-3302.
41. Rulik, B., Eberle, J., von der Mark, L., Thormann, J., Jung, M., Köhler, F., Apfel, W., Weigel, A., Kopetz, A., Köhler, J. Fritzlar, F. (2017) Using taxonomic consistency with semi‐automated data pre‐processing for high quality DNA barcodes. Methods in Ecology and Evolution 8(12), 1878-1887. doi.org/10.1111/2041-210X.12824
42. Ryss, A., Vieira P., Mota, M., Kulinich, O. (2005). A Synopsis of the genus Bursaphelenchus Fuchs, 1937 (Aphelenchida: Parasitaphelenchidae) with keys to species. Nematology 7, 393-458.
43. Sambrook, J., Russell, D.W. (2006). Purification of nucleic acids by extraction with phenol: chloroform. Cold Spring Harbor Protocols, 2006(1), pdb-prot4455. doi:10.1101/pdb.prot093450
44. Simon, C., Frati, F., Beckenbach, A., Crespi, B., Liu, H., Flook, P. (1994) Evolution, weighting, and phylogenetic utility of mitochondrial gene sequences and a compilation of conserved polymerase chain reaction primers. Annals of the Entomological Society of America 87(6), 651-701. doi.org/10.1093/aesa/87.6.651
45. Solano, E., Mancini, E., Ciucci, P., Mason, F., Audisio, P., Antonini, G. (2013). The EU protected taxon Morimus funereus Mulsant, 1862 (Coleoptera: Cerambycidae) and its western Palaearctic allies: systematics and conservation outcomes. Conservation Genetics, 14(3), 683-694. doi.org/10.1007/s10592-013-0461-3
46. Soydabaş, H.K., Uçkan, F., Atak, Ş. (2017). Phylogenetic status of Lamiinae (Cerambycidae: Coleoptera) species from Kocaeli province based COI gene sequences. In: XIII. Congress of Ecology and Environment with International Participation-UKECEK 2017, pp.136.
47. Soydabaş Ayoub, H.K. (2021). Nüklear ve mitokondriyal DNA dizileri kullanılarak Kocaeli ilindeki Cerambycidae (Coleoptera) türlerinin filogenetik analizi. [Doktora Tezi], Kocaeli Üniversitesi, Kocaeli, Türkiye.
48. Soydabaş-Ayoub, H. K., Uckan, F. (2022). Time-scaled phylogenetic analysis of extant Lamiinae (Coleoptera, Cerambycidae) species of East of Marmara Basin, Türkiye, and their evolutionary similarity with the Eurasian congeners. bioRxiv, 2022-09. https://doi.org/10.1101/2022.09.10.507409
49. Soydabaş-Ayoub, H. K., Uçkan, F., Atak, Ş., Şimşek, B. Ş., İbiş, O. (2022). Assessment of the phylogenetic relationships within the spondylidine branch of Spondylidinae (Coleoptera, Cerambycidae). Insect Systematics & Evolution, 54(3), 281-311. https://doi.org/10.1163/1876312X-bja10042
50. Stamatakis, A. (2014). RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics, 30(9), 1312-1313.
51. Tamura, S., Shoda-Kagaya, E. (2022). Genetic Differences among Established Populations of Aromia bungii (Faldermann, 1835)(Coleoptera: Cerambycidae) in Japan: Suggestion of Multiple Introductions. Insects, 13(2), 217. https://doi.org/10.3390/insects13020217
52. Templeton, A.R., Crandall, K.A., Sing, C.F. (1992). A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping and DNA sequence data. III. Cladogram estimation. Genetics 132(2), 619-633. https://doi.org/10.1093/genetics/132.2.619
53. Torres-Vila, L. M., Bonal, R. (2019). DNA barcoding of large oak-living cerambycids: Diagnostic tool, phylogenetic insights and natural hybridisation between Cerambyx cerdo and Cerambyx welensii (Coleoptera: Cerambycidae). Bulletin of entomological research, 109(5), 583-594. doi:10.1017/S0007485318000925
54. Townsend, J.P., Lopez-Giraldez, F. (2010). Optimal selection of gene and ingroup taxon sampling for resolving phylogenetic relationships. Systematic Biology 59(4), 446-457. doi.org/10.1093/sysbio/syq025
55. Tülek, A., Kepenekçi, İ., İmren, M., Akbulut, S., Tülek, B., Koca, A. S., Özdikmen, H. (2019). Detection of Bursaphelenchus mucronatus associated with Acanthocinus griseus on Pinus nigra in the northwestern Turkey. Nematropica, 49(2), 220–228.
56. Wallin, H., Nylander, U., Kvamme, T. (2009). Two sibling species of Leiopus Audinet-Serville, 1835 (Coleoptera: Cerambycidae) from Europe: L. nebulosus (Linnaeus, 1758) and L. linnei sp. nov. Zootaxa, 2010(1), 31-45.
57. Wang L, Li C, Luo Y, Wang G, Dou Z, Haq IU, Shang S, Cui M. (2023). Current and future control of the wood‐boring pest Anoplophora glabripennis. Insect Science. https://doi.org/10.1111/1744-7917.13187
58. Wang, Q., Leschen, R. A. (2003). Identification and distribution of Arhopalus species (Coleoptera: Cerambycidae: Aseminae) in Australia and New Zealand. New Zealand Entomologist, 26(1), 53-59.
59. Wang, Y., Chen, F., Wang, L., Li, M. (2021). Investigation of beetle species that carry the pine wood nematode, Bursaphelenchus xylophilus (Steiner and Buhrer) Nickle, in China. Journal of Forestry Research, 32(4), 1745-1751. https://doi.org/10.1007/s11676-020-01146-2
60. Ward, R.D., Zemlak, T.S., Innes, B.H., Last, P.R., Hebert, P.D. (2005). DNA barcoding Australia's fish species. Philosophical Transactions of the Royal Society B: Biological Sciences, 360(1462), 1847-1857.
61. Wollenberg Valero, K.C., Marshall, J.C., Bastiaans, E., Caccone, A., Camargo, A., Morando, M., M.L., Pabijan, M., Russello, M.A., Sinervo, B., Werneck, F.P. (2019). Patterns, mechanisms and genetics of speciation in reptiles and amphibians. Genes 10(9), 646. doi.org/10.3390/genes10090646
62. Wu, Y., Trepanowski, N.F., Molongoski, J.J., Reagel, P.F., Lingafelter, S.W., Nadel, H. (2017). Identification of wood-boring beetles (Cerambycidae and Buprestidae) intercepted in trade-associated solid wood packaging material using DNA barcoding and morphology. Scientific Reports, 7, 40316.