Eur. J. Entomol. 119: 337-353, 2022 | DOI: 10.14411/eje.2022.035

Mitochondrial genomes of two wild silkmoths, Samia watsoni and Samia wangi (Lepidoptera: Saturniidae), and their phylogenetic implicationsOriginal article

Decai LU1, Yixin HUANG2,3,*, Stefan NAUMANN4, Ian J. KITCHING5, Zhenbang XU6, Yang SUN1, Xu WANG1,3,*
1 Anhui Provincial Key Laboratory of the Conservation and Exploitation of Biological Resources, Key Laboratory of Biotic Environment and Ecological Safety in Anhui Province, College of Life Sciences, Anhui Normal University, Wuhu, Anhui, China; e-mails: ludecai0000@163.com, wangxu0322@ahnu.edu.cn, sy2019@ahnu.edu.cn
2 Collaborative Innovation Center of Recovery and Reconstruction of Degraded Ecosystem in Wanjiang Basin Co-founded by Anhui Province and Ministry of Education; School of Ecology and Environment, Anhui Normal University, Wuhu, Anhui 241000, China; e-mail: huangyx@ahnu.edu.cn
3 Key Laboratory of the Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of Sciences, No. 1 Beichen West Road, Chaoyang District, Beijing 100101, P.R. China
4 Research Associate of Museum für Naturkunde, Berlin; private address: Hochkirchstrasse 11, 10829 Berlin, Germany; e-mail: sn@saturniidae.com
5 Natural History Museum, Cromwell Road, London SW7 5BD, UK; e-mail: i.kitching@nhm.ac.uk
6 Institute of Resource Plants, Yunnan University, Kunming, Yunnan 650500, China; e-mail: 306252408@qq.com

The wild silkmoth genus Samia Hübner, 1819 (Saturniidae) contains a number of economically important species in industrial silk production. However, the interspecific relationships within the genus remain unclear. We sequence the mitogenomes of Samia watsoni Oberthür, 1914 and Samia wangi Naumann & Peigler, 2001. Both mitogenomes are annotated and found to be cyclized, with 37 genes (13 PCGs, 2 rRNA genes and 22 tRNA genes). Using maximum likelihood and Bayesian inference methods, we analyze these mitogenomes together with a further 68 downloaded from GenBank (65 Bombycoidea and 5 Lasiocampidae as the outgroup) to investigate the phylogenetic relationships both within the genus and those among the three families of the 'SBS' group: Bombycidae, Saturniidae and Sphingidae. The results show that within Samia, S. ricini is closely related to S. canningi, and not S. cynthia of which it has previously been considered to be a subspecies. Although arguments have been proposed to treat S. ricini and S. canningi as conspecific, we choose to accept the morphological arguments and continue to treat them as two separate species. Samia watsoni is corroborated as the sister group of all other Samia species, but nevertheless should be included within Samia rather than being placed in its own monobasic genus. Our analysis recovers the following relationship among the three families of the 'SBS' group: (Saturniidae + (Bombycidae + Sphingidae)). This agrees with previous studies based on analysis of mitogenomes but continues to contradict the results derived from phylogenomic analysis of nuclear genomes.

Keywords: Bombycoidea, Bombycidae, Sphingidae, phylogeny

Received: April 14, 2022; Revised: August 4, 2022; Accepted: August 4, 2022; Published online: August 24, 2022  Show citation

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LU, D., HUANG, Y., NAUMANN, S., KITCHING, I.J., XU, Z., SUN, Y., & WANG, X. (2022). Mitochondrial genomes of two wild silkmoths, Samia watsoni and Samia wangi (Lepidoptera: Saturniidae), and their phylogenetic implications. EJE119, Article 337-353. https://doi.org/10.14411/eje.2022.035
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References

  1. Andrews S. 2020: FastQC. URL: http://www.bioinformatics.babraham.ac.uk/projects/fastqc (last accessed 20 Sep. 2020).
  2. Bernt M., Donath A., Juhling F., Externbrink F., Florentz C., Fritzsch G., Putz J., Middendorf M. & Stadler P.F. 2013: MITOS: improved de novo metazoan mitochondrial genome annotation. - Mol. Phylogenet. Evol. 69: 313-319. Go to original source...
  3. Brechlin R. 2007: Einige Anmerkungen zur Gattung Samia Hübner 1819 ("1816") mit Beschreibung einer neuen Art (Lepido­ptera: Saturniidae). - Entomofauna M1: 56-61.
  4. Chen M.M., Li Y., Chen M., Wang H., Li Q., Xia R.X., Zeng C.Y., Li Y.P., Liu Y.Q. & Qin L. 2014: Complete mitochondrial genome of the atlas moth, Attacus atlas (Lepidoptera: Saturniidae) and the phylogenetic relationship of Saturniidae species. - Gene 545: 95-101. Go to original source...
  5. De Camargo A.J.A., De Camargo N.F., Corrêa D.C.V., De Camargo W.R.F., Vieira E.M., Marini-Filho O. & Amorim F.W. 2016: Diversity patterns and chronobiology of hawkmoths (Lepidoptera, Sphingidae) in the Brazilian Amazon rainforest. - J. Insect Conserv. 20: 629-641. Go to original source...
  6. Dierckxsens N., Mardulyn P. & Smits G. 2016: NOVOPlasty: de novo assembly of organelle genomes from whole genome data. - Nucl. Acids Res. 45(4): e18, 9 pp. Go to original source...
  7. Hamilton C.A., St Laurent R.A., Dexter K., Kitching I.J., Breinholt J.W., Zwick A., Timmermans M.J.T.N., Barber J.R. & Kawahara A.Y. 2019: Phylogenomics resolves major relationships and reveals significant diversification rate shifts in the evolution of silk moths and relatives. - BMC Evol. Biol. 182: 2-13. Go to original source...
  8. Hassanin A., Leger N. & Deutsch J. 2005: Evidence for multiple reversals of asymmetric mutational constraints during the evolution of the mitochondrial genome of Metazoa, and consequences for phylogenetic inferences. - Syst. Biol. 54: 277-298. Go to original source...
  9. Huang J.C., Li X.Y., Li Y.P., Zhang R.S., Chen D.B., Xia R.X. & Liu Y.Q. 2021: DNA barcodes provide evidence for the independent origin of the cultivated silkworms Samia ricini and Samia cynthia. - J. Insects Food Feed 8: 101-107. Go to original source...
  10. Katoh K. & Standley D.M. 2016: A simple method to control over-alignment in the MAFFT multiple sequence alignment program. - Bioinformatics 32: 1933-1942. Go to original source...
  11. Kawahara A.Y. & Breinholt J.W. 2014: Phylogenomics provides strong evidence for relationships of butterflies and moths. - Proc. R. Soc. (B) 281: 20140970, 8 pp. Go to original source...
  12. Kearse M., Moir R., Wilson A., Stones-Havas S., Cheung M., Sturrock S., Buxton S., Cooper A., Markowitz S. & Duran C. et al. 2012: Geneious Basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data. - Bioinformatics 28: 1647-1649. Go to original source...
  13. Kim J.S., Kim M.J., Jeong J.S. & Kim I. 2018: Complete mitochondrial genome of Saturnia jonasii (Lepidoptera: Saturniidae): Genomic comparisons and phylogenetic inference among Bombycoidea. - Genomics 110: 274-282. Go to original source...
  14. Kim M.I., Baek J.Y., Kim M.J., Jeong H.C., Kim K.G., Bae C.H., Han Y.S., Jin B.R. & Kim I. 2009: Complete nucleotide sequence and organization of the mitogenome of the red-spotted apollo butterfly, Parnassius bremeri (Lepidoptera: Papilionidae) and comparison with other lepidopteran insects. - Mol. Cells 28: 347-363. Go to original source...
  15. Kim M.J., Wang A.R., Park J.S. & Kim I. 2014: Complete mitochondrial genomes of five skippers (Lepidoptera: Hesperiidae) and phylogenetic reconstruction of Lepidoptera. - Gene 549: 97-112. Go to original source...
  16. Kim S.R., Kim J.S., Kim K.Y., Kim M.J., Jeong J.S. & Kim I. 2017: Complete mitochondrial genome of the wild silkmoth, Saturnia boisduvalii (Lepidoptera: Saturniidae). - Entomol. Res. 47: 344-351. Go to original source...
  17. Kitching I.J., Rougerie R., Zwick A., Hamilton C.A., St Laurent R.A., Naumann S., Mejia L.B. & Kawahara A.Y. 2018: A global checklist of the Bombycoidea (Insecta: Lepidoptera). - Biodiv. Data J. 6: e22236, 13 pp. Go to original source...
  18. Kumar S., Stecher G., Li M., Knyaz C. & Tamura K. 2018: MEGA X: Molecular Evolutionary Genetics Analysis across Computing Platforms. - Mol. Biol. Evol. 35: 1547-1549. Go to original source...
  19. Lartillot N., Rodrigue N., Stubbs D. & Richer J. 2013: PhyloBayes MPI: phylogenetic reconstruction with infinite mixtures of profiles in a parallel environment. - Syst. Biol. 62: 611-615. Go to original source...
  20. Lee J., Nishiyama T., Shigenobu S., Yamaguchi K., Suzuki Y., Shimada T., Katsuma S. & Kiuchi T. 2021: The genome sequence of Samia ricini, a new model species of lepidopteran insect. - Mol. Ecol. Resour. 21: 327-339. Go to original source...
  21. Lemaire C. & Peigler R.S. 1982: A study of Samia watsoni (Lepidoptera: Saturniidae). - Nouv. Rev. Entomol. 12: 175-182.
  22. Liu Q.N., Zhu B.J., Dai L.S., Wei G.Q. & Liu C.L. 2012: The complete mitochondrial genome of the wild silkworm moth, Actias selene. - Gene 505: 291-299. Go to original source...
  23. Margam V.M., Coates B.S., Hellmich R.L., Agunbiade T., Seufferheld M.J., Sun W., Ba M.N., Sanon A., Binso-Dabire C.L., Baoua I. et al. 2011: Mitochondrial genome sequence and expression profiling for the legume pod borer Maruca vitrata (Lepidoptera: Crambidae). - PLoS one 6(2): e16444, 9 pp. Go to original source...
  24. McLean D. 2002: Adobe Photoshop and Illustrator techniques. - J. Visual Commun. Med. 25: 79-81. Go to original source...
  25. Meier B.H., van Beek J.D., Beaulieu L., Schäfer H., Demura M. & Asakura T. 2000: Solid-state NMR determination of the secondary structure of Samia cynthia ricini silk. - Nature 405: 1077-1079. Go to original source...
  26. Meng G.L., Li Y.Y., Yang C.T. & Liu S.L. 2019: MitoZ: a toolkit for animal mitochondrial genome assembly, annotation and visualization. - Nucl. Acids Res. 47(11): e63, 7 pp. Go to original source...
  27. Naumann S. & Peigler R.S. 2001: Four new species of the silkmoth genus Samia (Lepidoptera: Saturniidae). - Nachr. Entomol. Ver. Apollo (N. F.) 22: 75-83.
  28. Naumann S., Peigler R.S. & Löffler S. 2014: New Samia Hübner, 1819 ("1816") (Lepidoptera: Saturniidae) from Vietnam, with taxonomic updates for the genus. - Eur. Entomologist 5: 101-115.
  29. Park J.S., Kim M.J., Jeong S.Y., Kim S.S. & Kim I. 2016: Complete mitochondrial genomes of two gelechioids, Mesophleps albilinella and Dichomeris ustalella (Lepidoptera: Gelechiidae), with a description of gene rearrangement in Lepidoptera. - Curr. Genetics 62: 809-826. Go to original source...
  30. Peigler R.S. & Calhoun J.V. 2013: Correct authorship of Phalaena ricini and the nomenclatural status of Saturnia canningi. - Trop. Lepid. Res. 23: 39-43.
  31. Peigler R.S. & Naumann S. 2003: A Revision of the Silkmoth Genus Samia. University of the Incarnate Word, San Antonio, TX, 227 + [54] pp.
  32. Rambaut A. 2020: FigTree v1.3.1. URL: http://tree.bio.ed.ac.uk/software/figtree (last accessed 20 Sep. 2020).
  33. Regier J.C., Cook C.P., Mitter C. & Hussey A. 2008: A phylogenetic study of the 'bombycoid complex' (Lepidoptera) using five protein-coding nuclear genes, with comments on the problem of macrolepidopteran phylogeny. - Syst. Entomol. 33: 175-189. Go to original source...
  34. Regier J.C., Zwick A., Cummings M.P., Kawahara A.Y., Cho S., Weller S., Roe A., Baixeras J., Brown J.W., Parr C. et al. 2009: Toward reconstructing the evolution of advanced moths and butterflies (Lepidoptera: Ditrysia): an initial molecular study. - BMC Evol. Biol. 9: 280, 21 pp. Go to original source...
  35. Rozas J., Sanchez-Delbarrio J.C., Messeguer X. & Rozas R. 2003: DnaSP, DNA polymorphism analyses by the coalescent and other methods. - Bioinformatics 19: 2496-2497. Go to original source...
  36. Saita S., Nolte H., Fiedler K.U., Kashkar H., Venne A.S., Zahedi R.P., Krüger M. & Langer T. 2017: PARL mediates Smac proteolytic maturation in mitochondria to promote apoptosis. - Nature Cell Biol. 19: 318-328. Go to original source...
  37. Singh B., Modica-Napolitano J.S. & Singh K.K. 2017: Defining the momiome: promiscuous information transfer by mobile mitochondria and mitochondrial genome. - Semin. Cancer Biol. 47: 1-17. Go to original source...
  38. Trifinopoulos J., Nguyen L.T., Von Haeseler A. & Minh B.Q. 2016: W-IQ-TREE: a fast online phylogenetic tool for maximum likelihood analysis. - Nucl. Acids Res. 44: W232-W235. Go to original source...
  39. Tyrrell D.A.J. 1997: Polymerase chain reaction identifies genes and infectious agents. - British Med. J. 314: 7073, 5 pp. Go to original source...
  40. Wang C.X. & Youle R.J. 2009: The role of mitochondria in apo­ptosis. - Annu. Rev. Genet. 43: 95-118. Go to original source...
  41. Wang X., Chen Z.M., Gu X.S., Wang M., Huang G.H. & Zwick A. 2018: Phylogenetic relationships among Bombycidae s.l. (Lepidoptera) based on analyses of complete mitochondrial genomes. - Syst. Entomol. 44: 490-498. Go to original source...
  42. Wu Y.P., Zhao J.L., Su T.J., Luo A.R. & Zhu C.D. 2016: The complete mitochondrial genome of Choristoneura longicellana (Lepidoptera: Tortricidae) and phylogenetic analysis of Lepidoptera. - Gene 591: 161-176. Go to original source...
  43. Xin Z.Z., Liu Y., Zhu X.Y., Wang Y., Zhang H.B., Zhang D.Z., Zhou C.L., Tang B.P. & Liu Q.N. 2017: Mitochondrial genomes of two Bombycoidea insects and implications for their phylogeny. - Sci. Rep. 7: 6544, 11 pp. Go to original source...
  44. Zhang D., Gao F.L., Jakovliæ I., Zou H., Zhang J., Li W.X. & Wang G.T. 2019: PhyloSuite: An integrated and scalable desktop platform for streamlined molecular sequence data management and evolutionary phylogenetics studies. - Mol. Ecol. Resour. 53: 4416-4425. Go to original source...
  45. Zwick A. 2008: Molecular phylogeny of Anthelidae and other bombycoid taxa (Lepidoptera: Bombycoidea). - Syst. Entomol. 33: 190-209. Go to original source...
  46. Zwick A. 2009: The principal structure of male genital sclerites and muscles of bombycoid moths, with special reference to Anthelidae (Lepidoptera: Bombycoidea). - Arthr. Struct. Devel. 38: 147-161. Go to original source...

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