Skip to main content
SpringerLink
Log in

A time-calibrated mitogenomic phylogeny suggests that Korean Hyalessa fuscata is a bridge between Chinese and Japanese H. maculaticollis

  • Research Article
  • Published:
Journal of Genetics Aims and scope Submit manuscript

Abstract

The cicada species, Hyalessa fuscata and H. maculaticollis (Hemiptera: Cicadidae), share numerous morphological characters, and their status as distinct species remains controversial. We reconstructed a phylogeny based on two new mitogenomes of H. fuscata from Korea and H. maculaticollis from Japan, in combination with GenBank sequences of H. maculaticollis from China and Japan, and other closely related cicada species. Maximum likelihood and Bayesian inference phylogenies showed that H. fuscata from Korea is more closely related to H. maculaticollis from China than either is to H. maculaticollis from Japan. The time-calibrated Bayesian evolutionary analysis by sampling trees (BEAST) phylogeny indicated that the mainland and insular forms diverged approximately 1.7–2.6 million years ago. This coincides with the formation of the East China Sea land bridge between East Asia and the Japanese archipelago, which would provide a dispersal corridor for Hyalessa from the mainland via the Korean peninsula southeastward to Japan. East Asian H. fuscata is a geographic variant that may be considered synonymous with H. maculaticollis.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Figure 1
Figure 2

Similar content being viewed by others

References

  • Bouckaert R., Heled J., Kühnert D., Vaughan T., Wu C. H., Xie D. et al. 2014 BEAST 2: a software platform for Bayesian evolutionary analysis. PLoS Comput. Biol. 10, e1003537.

    Article  Google Scholar 

  • Cameron S. 2014 Insect mitochondrial genomics: implications for evolution and phylogeny. Annu. Rev. Entomol. 59, 95–117.

    Article  CAS  Google Scholar 

  • Den Hollander J. 1995 Acoustic signals as specific mate recognition signals in leafhoppers (Cicadellidae) and planthoppers (Delphacidae) (Homoptera: Auchenorrhyncha). In Speciation and the recognition concept: theory and application, pp. 440-463. Johns Hopkins University Press, Baltimore.

  • Distant W. L. 1905 V.—Rhynchotal notes.—XXIX. J. Nat. Hist. 15, 58–70.

    Google Scholar 

  • Du Z., Hasegawa H., Cooley J. R., Simon C., Yoshimura J., Cai W. et al. 2019 Mitochondrial genomics reveals shared phylogeographic patterns and demographic history among three periodical cicada species groups. Mol. Biol. Evol. 36, 1187–1200.

    Article  CAS  Google Scholar 

  • Dugdale J. S. and Fleming C. A. 1978 New Zealand cicadas of the genus Maoricicada (Homoptera: Tibicinidae). N. z. J. Zool. 5, 295–340.

    Article  Google Scholar 

  • Feng Y., Comes H. P. and Qiu Y. X. 2020 Phylogenomic insights into the temporal-spatial divergence history, evolution of leaf habit and hybridization in Stachyurus (Stachyuraceae). Mol. Phylogenet. Evol. 150, 106878.

    Article  Google Scholar 

  • Hayashi M. 2011 Preliminary notes on some taxonomic changes in Japanese Cicadidae. Cicada 20, 2–5.

    Google Scholar 

  • Hayashi M. and Saisho Y. 2011 The Cicadidae of Japan. Seibundo-shinkosha, Tokyo.

  • Hedges S. B., Marin J., Suleski M., Paymer M. and Kumar S. 2015 Tree of life reveals clock-like speciation and diversification. Mol. Biol. Evol. 32, 835–845.

    Article  CAS  Google Scholar 

  • Ikeda H., Cho Y. B. and Sota T. 2013 Colonization history of the carrion beetle Necrophila jakowlewi (Coleoptera: Silphidae) in Japan inferred from phylogeographic analysis. Zool. Sci. 30, 901–905.

    Article  Google Scholar 

  • Kaizuka S. 1980 Late cenozoic palaeogeography of Japan. GeoJournal, 101–109.

  • Kameda Y. and Kato M. 2011 Terrestrial invasion of pomatiopsid gastropods in the heavy-snow region of the Japanese Archipelago. BMC Evol. Biol. 11, 1–14.

    Article  Google Scholar 

  • Kimura M. 2003 Land connections between Eurasian continent and Japanese Islands–related to human migration. Migr. Diffus. 4, 14–33.

    Google Scholar 

  • Kozlov A. M., Darriba D., Flouri T., Morel B. and Stamatakis A. 2019 RAxML-NG: a fast, scalable and user-friendly tool for maximum likelihood phylogenetic inference. Bioinformatics 35, 4453–4455.

    Article  CAS  Google Scholar 

  • Kumar S., Stecher G., Li M., Knyaz C. and Tamura K. 2018 MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol. Biol. Evol. 35, 1547–1549.

    Article  CAS  Google Scholar 

  • Kurosawa Y. 1969 The Cicadidae from the islands of Tsushima, Japan, preserved in the National Science Museum, Tokyo. Memoir of the National Science Museum, Tokyo 2, 73–78.

    Google Scholar 

  • Lane D. H. 1995 The recognition concept of species applied in an analysis of putative hybridization in New Zealand cicadas of the genus Kikihia (Insecta: Hemiptera: Tibicinidae). In Speciation and the recognition concept: theory and application, pp. 367–421, Johns Hopkins University Press, Baltimore.

  • Lanfear R., Frandsen P. B., Wright A. M., Senfeld T. and Calcott B. 2017 PartitionFinder 2: new methods for selecting partitioned models of evolution for molecular and morphological phylogenetic analyses. Mol. Biol. Evol. 34, 772–773.

    CAS  Google Scholar 

  • Lee Y. J. 2008 Revised synonymic list of Cicadidae (Insecta: Hemiptera) from the Korean Peninsula, with the description of a new species and some taxonomic remarks. Proc. Biol. Soc. Wash 121, 445–467.

    Article  Google Scholar 

  • Lee Y. J. 2010 Cicadas (Insecta: Hemiptera: Cicadidae) of Mindanao, Philippines, with the description of a new genus and a new species. Zootaxa 2351, 14-28–14-28.

  • Li H., Leavengood J. M. Jr., Chapman E. G., Burkhardt D., Song F., Jiang P., et al. 2017 Mitochondrial phylogenomics of Hemiptera reveals adaptive innovations driving the diversification of true bugs. Proc. Royal Soc. B 284, 20171223.

  • Liu Y., Qiu Y., Wang X., Yang H., Hayashi M. and Wei C. 2018 Morphological variation, genetic differentiation and phylogeography of the East Asia cicada Hyalessa maculaticollis (Hemiptera: Cicadidae). Syst. Entomol. 43, 308–329.

    Article  Google Scholar 

  • Łukasik P., Chong R. A., Nazario K., Matsuura Y., Bublitz De A. C., Campbell M. A., et al. 2018 One hundred mitochondrial genomes of cicadas. J. Hered. 110, 247-256.

  • Marshall D. C., Hill K. B. R., Cooley J. R. and Simon C. 2011 Hybridization, mitochondrial DNA phylogeography, and prediction of the early stages of reproductive isolation: lessons from New Zealand cicadas (Genus Kikihia). Syst. Biol. 60, 482–502.

    Article  Google Scholar 

  • Matsuura Y., Moriyama M., Łukasik P., Vanderpool D., Tanahashi M., Meng X. Y. et al. 2018 Recurrent symbiont recruitment from fungal parasites in cicadas. Proc. Natl. Acad. Sci. USA 115, E5970–E5979.

    Article  CAS  Google Scholar 

  • Papadopoulou A., Anastasiou I. and Vogler A. P. 2010 Revisiting the insect mitochondrial molecular clock: the mid-Aegean trench calibration. Mol. Biol. Evol. 27, 1659–1672.

    Article  CAS  Google Scholar 

  • Paterson H. E. H. and Vrba E. S. 1985 The recognition concept of species. In The units of evolution: essays on the nature of species, pp. 139-58. MIT Press, Cambridge.

  • Puissant S. and Lee Y. J. 2016 Description of a new species of the genus Hyalessa China (Hemiptera: Cicadidae: Sonatini) from Yunnan, China, with a key to the species of Hyalessa and a calling song analysis for two Hyalessa species. Zootaxa 4114, 434–446.

    Article  Google Scholar 

  • Rambaut A. and Drummond A. J. 2010 TreeAnnotator version 1.6.1. University of Edinburgh, Edinburgh, UK.

  • Rambaut A., Suchard M. and Drummond A. 2014 MCMC trace analysis tool: Tracer v. 1.6.0.

  • Rambaut A., Drummond A. J., Dong X., Guy B. and Suchard M. A. 2018 Posterior summarization in Bayesian phylogenetics using Tracer 1.7. Syst. Biol. 67, 901–904.

    Article  CAS  Google Scholar 

  • Song N., Cai W. and Li H. 2017 Deep-level phylogeny of Cicadomorpha inferred from mitochondrial genomes sequenced by NGS. Science 7, 1–11.

    Google Scholar 

  • Stål C. 1870 Hemiptera insularum Philippinarum. Bidrag till Philippinska öarnes Hemipter-fauna.

  • Thompson J. D., Higgins D. G. and Gibson T. J. 1994 CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22, 4673–4680.

    Article  CAS  Google Scholar 

  • Villet M. 1995 Intraspecific variability in SMRS signals: some causes and implications in acoustic signaling systems. In Speciation and the recognition concept. Theory and applications, pp. 422–439. The John Hopkins University Press, Baltimore.

  • Wang X., Hayashi M. and Wei C. 2014 On cicadas of Hyalessa maculaticollis complex (Hemiptera, Cicadidae) of China. ZooKeys 25.

  • Zhang D., Ye Z., Yamada K., Zhen Y., Zheng C. and Bu W. 2016 Pleistocene sea level fluctuation and host plant habitat requirement influenced the historical phylogeography of the invasive species Amphiareus obscuriceps (Hemiptera: Anthocoridae) in its native range. BMC Evol. Biol. 16, 1–15.

    Article  Google Scholar 

  • Zhao J., Zhou P., Li X., Zhang L., Jin X. and Xiang X. 2020 Temporal and spatial pattern of Holcoglossum Schltr. (Orchidaceae), an East Asian endemic genus, based on nuclear and chloroplast genes. Front. Ecol. Evol. 8, 245.

Download references

Acknowledgements

This research was funded by the National Research Foundation of Korea (grant number 2015R1A4A1041997), the National Foundation for Science and Technology Development (grant number 19/2020/STS02), and the Graduate University of Science and Technology (grant number: GUST.STS.ĐT2020-ST03).

Author information

Authors and Affiliations

  1. Ewha Womans University, Ewhayeodaegil-52, Seoul, 03760, Republic of Korea

    Hoa Quynh Nguyen & Yikweon Jang

  2. Institute of Chemistry, Vietnam Academy of Science and Technology, No. 18 Hoang Quoc Viet Street, Hanoi, 10072, Vietnam

    Hoa Quynh Nguyen

  3. Vietnam National Museum of Nature, Vietnam Academy of Science and Technology, No. 18 Hoang Quoc Viet, Hanoi, 10072, Vietnam

    Hoa Quynh Nguyen & Thai Hong Pham

  4. Graduate School of Science and Technology, Vietnam Academy of Science and Technology, No. 18 Hoang Quoc Viet, Hanoi, 10072, Vietnam

    Hoa Quynh Nguyen, Thai Hong Pham & Huyen Thi La

  5. Department of Biology, Ho Chi Minh University of Education, Ho Chi Minh, 72711, Vietnam

    Phuong-Thao Ho

  6. Department of Evolution, Ecology, and Organismal Biology, The Ohio State University, Columbus, OH, 43212, USA

    Sungsik Kong

  7. Department of Life Sciences and Division of Ecoscience, Ewha Womans University, Ewhayeodaegil-52, Seoul, 03760, Republic of Korea

    Yoonhyuk Bae & Yikweon Jang

  8. Mientrung Institute for Scientific Research, Vietnam Academy of Science and Technology, 321 Huynh Thuc Khang, Hue, 49117, Vietnam

    Thai Hong Pham

  9. Institute of Biotechnology, Vietnam Academy of Science and Technology, Hanoi, 10072, Vietnam

    Huyen Thi La

Authors
  1. Hoa Quynh Nguyen
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Phuong-Thao Ho
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Sungsik Kong
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yoonhyuk Bae
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Thai Hong Pham
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Huyen Thi La
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Yikweon Jang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Yikweon Jang.

Additional information

Corresponding editor: Steven M. Carr

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file 1

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Nguyen, H.Q., Ho, PT., Kong, S. et al. A time-calibrated mitogenomic phylogeny suggests that Korean Hyalessa fuscata is a bridge between Chinese and Japanese H. maculaticollis. J Genet 102, 9 (2023). https://doi.org/10.1007/s12041-022-01405-7

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s12041-022-01405-7

Keywords

Search

Navigation