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Type: Article
Published: 2024-11-19
Page range: 32-57
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Morphological and molecular variability within widespread Palearctic species Liocoris tripustulatus Fieber (Hemiptera: Heteroptera: Miridae: Mirinae)

Zoological Institute, Russian Academy of Sciences, Universitetskaya nab. 1, St. Petersburg 199034, Russia
All-Russian Institute of Plant Protection, Podbelskogo sh. 3, Pushkin, St. Petersburg, 196608, Russia
Mirini genetic diversity population structure phylogeny species delimitation Pleistocene refugia

Abstract

The works addressing the intraspecific genetic and morphological diversity of the widespread Palearctic plant bug species on their entire distribution ranges are rare. In this study the morphological and molecular variability of Liocoris tripustulatus Fieber, 1858 was assessed. The molecular diversity was investigated based on two mitochondrial markers (cytochrome c oxidase subunit I or COI and 16S rRNA) and a nuclear marker (internal transcribed spacer 1 or ITS1). The genetic, haplotype and population diversity were assessed. The phylogenetic analyses and automatic species delimitation were performed to test for the possible cryptic species. The dating analysis was performed to estimate the clade divergence time. The results showed that the coloration of this species is variable, however, structures are stable, showing some variability in the right paramere shape and sclerotization of the female genitalia. The genetic diversity within the species is shallow. The phylogenetic analyses based on the mitochondrial markers show that the specimens from Georgia and Iran form a well-supported clade. In the phylogenies based on ITS1 specimens from Dagestan Republic (Northern Caucasus) are also included into this clade. The Caucasian-Iranian clade might represent a separate population or species at the early stages of its separation, which originated during the Middle Pleistocene.

References

  1. Aparicio-Puerta E., Gómez-Martín C., Giannoukakos S., Medina J. M., Scheepbouwer C., García-Moreno A., Carmona-Saez P., Fromm B., Pegtel M., Keller A., Marchal J. A. & Hackenberg M. 2022. sRNAbench and sRNAtoolbox 2022 update: accurate miRNA and sncRNA profiling for model and non-model organisms. Nucleic acids research 50(W1): 710–717. https://doi.org/10.1093/nar/gkac363

  2. Arthofer W., Avtzis D. N., Riegler M. & Stauffer C. 2010. Mitochondrial phylogenies in the light of pseudogenes and Wolbachia: re-assessment of a bark beetle dataset. ZooKeys 56: 269–280. https://doi/10.3897/zookeys.56.531

  3. Blair C. & Bryson R.W. 2017. Cryptic diversity and discordance in single-locus species delimitation methods within horned lizards (Phrynosomatidae: Phrynosoma). Molecular Ecology Resources 17: 1168–1182. https://doi/10.1111/1755-0998.12658

  4. Bouckaert R., Heled J., Kühnert D. & et al. 2014. BEAST 2: a software platform for Bayesian evolutionary analysis. PLoS computational biology 10(4): e1003537. https://doi.org/10.1371/journal.pcbi.1003537

  5. Brower A. V. 2006. Problems with DNA barcodes for species delimitation: ‘ten species’ of Astraptes fulgerator reassessed (Lepidoptera: Hesperiidae). Systematics and Biodiversity 4(2): 127–132. https://doi.org/10.1017/S147720000500191X

  6. Cassis G. & Schuh R. T. 2012. Systematics, biodiversity, biogeography, and host associations of the Miridae (Insecta: Hemiptera: Heteroptera: Cimicomorpha). Annual Review of Entomology 57(1): 377–404. https://doi.org/10.1146/annurev-ento-121510-133533

  7. Clement M., Posada D. & Crandall K. A. 2000. TCS: a computer program to estimate gene genealogies. Molecular Ecology 9: 1657–1660.

  8. Davletshin S. Z. & Konstantinov F. V. 2024. Confocal laser scanning microscopy and three-dimensional reconstruction delimit species in a taxonomically challenging group: a revision of the plant bug genus Anapus Stål, 1858 (Heteroptera: Miridae). Insect Systematics & Evolution 55(1): 41–92. https://doi.org/10.1163/1876312x-bja10052

  9. Dzhelali P. A. & Namyatova A. A. (in press). Integrative approach for the identification and delimitation of Orthops species (Heteroptera, Miridae, Mirinae) in the Palearctic. Journal of Zoological Systematics and Evolutionary Research.

  10. Douglas J. & Bouckaert R. 2022. Quantitatively defining species boundaries with more efficiency and more biological realism. Communications Biology 5: 755. https://doi.org/10.1038/s42003-022-03723-z

  11. Douglas J., Jiménez-Silva C. L. & Bouckaert R. 2022. StarBeast3: Adaptive Parallelised Bayesian Inference under the Multispecies Coalescent. Systematic Biology 71(4): 901–916. https://doi.org/10.1093/sysbio/syac010

  12. Eberle J., Husemann M., Doerfler I., & et al. 2021. Molecular biogeography of the fungus-dwelling saproxylic beetle Bolitophagus reticulatus indicates rapid expansion from glacial refugia. Biological Journal of the Linnean Society 133(3): 766–778. https://doi.org/10.1093/biolinnean/blab037

  13. Esenbekova P. A., Kenzhegaliev Y. M. & Homziak J. 2017. Hemiptera (Heteroptera) of Sairam-Ugam National Park, Kazakhstan (fauna, biology, ecology and economic significance). Journal of Entomology and Zoology Studies 5(2): 97–107.

  14. Excoffier L. & Lischer H. E. 2010. Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Molecular ecology resources 10(3): 564–567. https://doi.org/10.1111/j.1755-0998.2010.02847.x

  15. Ferreira S., Oosterbroek P., Starý J., & et al. 2021. The InBIO Barcoding Initiative Database: DNA barcodes of Portuguese Diptera 02-Limoniidae, Pediciidae and Tipulidae. Biodiversity Data Journal 9: e69841. https://doi.org/10.3897/BDJ.9.e69841

  16. Françoso E., Zuntini A. R. & Arias M. C. 2019. Combining phylogeography and future climate change for conservation of Bombus morio and B. pauloensis (Hymenoptera: Apidae). Journal of Insect Conservation 23: 63–73. https://doi.org/10.1007/s10841-018-0114-4

  17. Fujisawa T. & Barraclough T. G. 2013. Delimiting species using single-locus data and the Generalized Mixed Yule Coalescent approach: a revised method and evaluation on simulated data sets. Systematic Biology 62(5): 707–724. https://doi.org/10.1093/sysbio/syt033

  18. Gamerschlag S., Mehlhorn H., Heukelbach J., Feldmeier H. & D’haese J. 2008. Repetitive sequences in the ITS1 region of the ribosomal DNA of Tunga penetrans and other flea species (Insecta, Siphonaptera). Parasitology Research 102: 193–199. https://doi.org/10.1007/s00436-007-0743-0

  19. García-Vázquez D., Bilton D. T., Foster G. N. & Ribera I. 2017. Pleistocene range shifts, refugia and the origin of widespread species in western Palaearctic water beetles. Molecular Phylogenetics and Evolution 114: 122–136. https://doi.org/10.1016/j.ympev.2017.06.007

  20. Goldstein P. Z. & Desalle R. 2011. Integrating DNA barcode data and taxonomic practice: determination, discovery, and description. Bioessays 33(2): 135–147. https://doi.org/10.1002/bies.201000036

  21. Gostel M. R. & Kress W. J. 2022. The expanding role of DNA barcodes: Indispensable tools for ecology, evolution, and conservation. Diversity 14(3): 213. https://doi.org/10.3390/d14030213

  22. Gueuning M., Frey J. E. & Praz C. 2020. Ultraconserved yet informative for species delimitation: ultraconserved elements resolve long‐standing systematic enigma in Central European bees. Molecular Ecology 29(21): 4203–4220. https://doi.org/10.1111/mec.15629

  23. Hebert P. D., Cywinska A., Ball S. L. & Dewaard J. R. 2003. Biological identifications through DNA barcodes. Proceedings of the Royal Society of London. Series B: Biological Sciences 270(1512): 313–321. https://doi.org/10.1098/rspb.2002.2218

  24. Hinomoto N., Muraji M., Noda T., Shimizu T. & Kawasaki K. 2004. Identification of five Orius species in Japan by multiplex polymerase chain reaction. Biological Control 31(3): 276–279. https://doi.org/10.1016/j.biocontrol.2004.07.002

  25. Ho S. Y. & Lo N. 2013. The insect molecular clock. Australian Journal of Entomology 52(2): 101–105. https://doi.org/10.1111/aen.12018

  26. Hortal J., De Bello F., Diniz-Filho J. A. F., Lewinsohn T. M., Lobo J. M., & Ladle R. J. 2015. Seven shortfalls that beset large-scale knowledge of biodiversity. Annual Review of Ecology, Evolution, and Systematics 46: 523–549. https://doi.org/10.1146/annurev-ecolsys-112414-054400

  27. Jinbo U., Kato T. & Ito M. 2011. Current progress in DNA barcoding and future implications for entomology. Entomological Science 14(2): 107–124. https://doi.org/10.1111/j.1479-8298.2011.00449.x

  28. Kerzhner I. M. & Josifov M. 1999. Miridae Hahn, 1831. In: Catalogue of the Heteroptera of the Palaearctic Region. Vol. 3. (Aukema B. & Rieger C., editors) Netherlands Entomological Society, Amsterdam, 577 pp.

  29. Kim J. & Jung S. 2019. Phylogeny of the plant bug subfamily Mirinae (Hemiptera: Heteroptera: Cimicomorpha: Miridae) based on total evidence analysis. Systematic Entomology 44(4): 686–698. https://doi.org/10.1111/syen.12348

  30. Kim H. & Lee S. 2008. Molecular systematics of the genus Megoura (Hemiptera: Aphididae) using mitochondrial and nuclear DNA sequences. Molecules and Cells 25(4): 510–522. https://doi.org/10.1016/S1016-8478(23)17612-6

  31. Konstantinov F. V. 2000. Structure of the male genitalia in plant bugs (Heteroptera: Miridae) and its significance for suprageneric classification. Dissertation, St. Petersburg State University.

  32. Konstantinov F. V. 2003. Male genitalia in Miridae (Heteroptera) and their significanсe for suprageneric classification of the family. Part I: general review, Isometopinae and Psallopinae. Belgium Journal of Entomology 5: 3–36.

  33. Konstantinov A. S., Korotyaev B. A. & Volkovitsh M. G. 2009. Insect biodiversity in the Palearctic Region. Pp. 107–162. In: Insect Biodiversity: Science and Society (Foottit R.G. & Adler P.H., editors). Wiley-Blackwell, 656 pp.

  34. Lauer T. & Weiss M. 2018. Timing of the Saalian-and Elsterian glacial cycles and the implications for Middle–Pleistocene hominin presence in central Europe. Scientific Reports 8: 5111. https://doi.org/10.1038/s41598-018-23541-w

  35. Leigh J. W. & Bryant D. 2015. Popart: full‐feature software for haplotype network construction. Methods in Ecology and Evolution 6: 1110–1116. https://doi.org/10.1111/2041-210X.12410

  36. Leroy S. A. & Arpe K. 2007. Glacial refugia for summer‐green trees in Europe and south‐west Asia as proposed by ECHAM3 time‐slice atmospheric model simulations. Journal of Biogeography 34(12): 2115–2128. https://doi.org/10.1111/j.1365-2699.2007.01754.x

  37. Maddison, W. P. & Knowles L. L. 2006. Inferring phylogeny despite incomplete lineage sorting. Systematic Biology 55(1): 21–30. https://doi.org/10.1080/10635150500354928

  38. Mallo D. & Posada D. 2016. Multilocus inference of species trees and DNA barcoding. Philosophical Transactions of the Royal Society B: Biological Sciences 371(1702): 20150335. https://doi.org/10.1098/rstb.2015.0335

  39. Menard K. L., Schuh R. T. & Woolley J. B. 2014. Total‐evidence phylogenetic analysis and reclassification of the Phylinae (Insecta: Heteroptera: Miridae), with the recognition of new tribes and subtribes and a redefinition of Phylini. Cladistics 30(4): 391–427. https://doi.org/10.1111/cla.12052

  40. Mirarab S., Nakhleh L. & Warnow T. 2021. Multispecies coalescent: theory and applications in phylogenetics. Annual Review of Ecology, Evolution, and Systematics 52(1): 247–268. https://doi.org/10.1146/annurev-ecolsys-012121-095340

  41. Namyatova A. A., Dzhelali P. A. & Konstantinov F. V. 2024. Delimitation of the widely distributed Palearctic Stenodema species (Hemiptera, Heteroptera, Miridae): insights from molecular and morphological data. ZooKeys 1209: 245–294. https://doi.org/10.3897/zookeys.1209.124766

  42. Namyatova A. A. & Konstantinov F. V. 2009. Revision of the genus Orthocephalus Fieber, 1858 (Hemiptera: Heteroptera: Miridae: Orthotylinae). Zootaxa 2316(1): 1–118. https://doi.org/10.11646/zootaxa.2316.1.1

  43. Namyatova A. A., Schwartz, M. D. & Cassis G. 2013. First record of the genus Stenotus Jakovlev from Australia, with two new species, and a list of mirine species from Witchelina Nature Reserve (Insecta: Heteroptera: Miridae: Mirinae: Mirini). Journal of Natural History 47(13-14): 987–1008. https://doi.org/10.1080/00222933.2012.752049

  44. Namyatova A. A., Schwartz M. D. & Cassis G. 2021. Determining the position of Diomocoris, Micromimetus and Taylorilygus in the Lygus-complex based on molecular data and first records of Diomocoris and Micromimetus from Australia, including four new species (Insecta: Hemiptera: Miridae: Mirinae). Invertebrate Systematics 35(1): 90–131. https://doi.org/10.1071/IS20015

  45. Namyatova A. A. & Tyts V. D. 2024. Total-evidence phylogeny of the subfamily Cylapinae and the divergence dates for its subgroupings (Insecta: Heteroptera: Miridae). Zoological Journal of the Linnean Society: zlae008. https://doi.org/10.1093/zoolinnean/zlae008

  46. Namyatova A. A., Tyts V. D. & Bolshakova D. S. 2023. Identification and delimitation of the trans-Palearctic Lygus species (Insecta: Heteroptera: Miridae) using integrative approach. Insect Systematics & Evolution 54(2): 146–192. https://doi.org/10.1071/IS20015

  47. Nylander J. A. A. 2004. MrModeltest v2. Uppsala: Evolutionary Biology Centre, Uppsala University. Available from: https://github.com/nylander/MrModeltest2 (accessed on 17 Jul 2022).

  48. Ogilvie H. A., Bouckaert R. R. & Drummond A. J. 2017. StarBEAST2 brings faster species tree inference and accurate estimates of substitution rates. Molecular Biology and Evolution 34(8): 2101–2114. https://doi.org/10.1093/molbev/msx126

  49. Puillandre N., Lambert A., Brouillet S. & Achaz G. 2012. ABGD, Automatic Barcode Gap Discovery for primary species delimitation. Molecular Ecology 21: 1864–1877. https://doi.org/10.1111/j.1365-294X.2011.05239.x

  50. Rambaut A., Drummond A. J., Xie D., Baele G. & Suchard M. A. 2018. Posterior summarization in Bayesian phylogenetics using Tracer 1.7. Systematic Biology 67(5): 901–904. https://doi.org/10.1093/sysbio/syy032

  51. Raupach M. J., Hendrich L., Küchler S. M., Deister F., Morinière J. & Gossner M. M. 2014. Building-up of a DNA barcode library for true bugs (Insecta: Hemiptera: Heteroptera) of Germany reveals taxonomic uncertainties and surprises. PloS One 9(9): e106940. https://doi.org/10.1371/journal.pone.0106940

  52. Regattieri E., Giaccio B., Galli P., Nomade S., Peronace E., Messina P. & Gemelli M. 2016. A multi-proxy record of MIS 11–12 deglaciation and glacial MIS 12 instability from the Sulmona basin (central Italy). Quaternary Science Reviews 132: 129–145. https://doi.org/10.1016/j.quascirev.2015.11.015

  53. Reid N. M. & Carstens B. C. 2012. Phylogenetic estimation error can decrease the accuracy of species delimitation: a Bayesian implementation of the general mixed Yule-coalescent model. BMC Evolutionary Biology 12: 1–11. https://doi.org/10.1186/1471-2148-12-196

  54. Ronquist F., Teslenko M., Van Der Mark P. & et al. 2012. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61(3): 539–542. https://doi.org/10.1093/sysbio/sys029

  55. Roslin T., Somervuo P., Pentinsaari M. & et al. 2022. A molecular‐based identification resource for the arthropods of Finland. Molecular Ecology Resources 22(2): 803–822. https://doi.org/10.1111/1755-0998.13510

  56. Schwartz M. D. & Foottit R. G. C. 1998. Revision of the Nearctic species of the genus Lygus Hahn, with a review of the Palaearctic species (Heteroptera: Miridae). Memoirs on Entomology, International 10: 1–428.

  57. Schuh R. T. & Weirauch C. 2020. True Bugs of the World (Hemiptera: Heteroptera). Classification and Natural History [2nd ed.]. Siri Scientific Press, Manchester. 800 pp.

  58. Da Silva R., Peloso P., Sturaro M. J., Veneza I., Sampaio I., Schneider H. & Gomes G. 2018. Comparative analyses of species delimitation methods wit molecular data in snappers (Perciformes: Lutjaninae). Mitochondrial DNA Part A 29(7): 1108–1114. https://doi.org/10.1080/24701394.2017.1413364

  59. Southwood T. R. E. & Leston D. 1959. Land and Water Bugs of the British Isles. Frederick Warne and Co., London. 436 pp.

  60. Stamatakis A. 2014. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30(9): 1312–1313. https://doi.org/10.1093/bioinformatics/btu033

  61. Steenman E., Hennig E. I., Jaccard G., Mihailescu E., Fischer S. & Sutter L. 2023. The potential of entomopathogenic nematodes for the management of the mirid bugs Lygus rugulipennis (Poppuis), Liocoris tripustulatus (Fabricius) and Macrolophus pygmaeus (Rambur). Journal of Natural Pesticide Research 6: 100054. https://doi.org/10.1016/j.napere.2023.100054

  62. Szalanski A. L., Austin J. W., Mckern J. A., Steelman C. D. & Gold R. E. 2014. Mitochondrial and ribosomal internal transcribed spacer 1 diversity of Cimex lectularius (Hemiptera: Cimicidae). Journal of medical entomology 45(2): 229–236. https://doi.org/10.1093/jmedent/45.2.229

  63. Tamura K., Stecher G. & Kumar S. 2021. MEGA11: Molecular evolutionary genetics analysis version 11. Molecular Biology and Evolution 38(7): 3022–3027. https://doi.org/10.1093/molbev/msab120

  64. Templeton A. R., Routman E. & Phillips C. A. 1995. Separating population structure from population history: a cladistic analysis of the geographical distribution of mitochondrial DNA haplotypes in the tiger salamander Ambystoma tigrinum. Genetics 140: 767–782. https://doi.org/10.1093/genetics/140.2.767

  65. Vishnevskaya M. S., Saifitdinova A. F. & Lukhtanov V. A. 2016. Karyosystematics and molecular taxonomy of the anomalous blue butterflies (Lepidoptera, Lycaenidae) from the Balkan Peninsula. Comparative Cytogenetics 10(5): 1–85. https://doi.org/10.3897/CompCytogen.v10i5.10944

  66. Vitali F. & Schmitt T. 2017. Ecological patterns strongly impact the biogeography of western Palaearctic longhorn beetles (Coleoptera: Cerambycoidea). Organisms Diversity & Evolution 17(1): 163–180. https://doi.org/10.1007/s13127-016-0290-6

  67. Wheeler A. G. 2001. Biology of the Plant Bugs (Hemiptera: Miridae): Pests, Predators, Opportunists. Cornell University Press, Ithaca and London. 507 pp.

  68. Wynde F. J. & Port G. R. 2012. The use of olfactory and visual cues in host choice by the capsid bugs Lygus rugulipennis Poppius and Liocoris tripustulatus Fabricius. PLoS One 7(12): e46448. https://doi.org/10.1371/journal.pone.0046448

  69. Zhang J., Kapli P., Pavlidis P. & Stamatakis A. 2013. A general species delimitation method with applications to phylogenetic placements. Bioinformatics 29: 2869–2876. https://doi.org/10.1093/bioinformatics/btt499