Hostname: page-component-848d4c4894-x24gv Total loading time: 0 Render date: 2024-06-11T11:28:48.040Z Has data issue: false hasContentIssue false
  • English
  • Français

Life history and mitochondrial genomes of Salassinae and Agliinae (Insecta, Lepidoptera): New insights into the loss of cocooning behaviour and phylogeny of Saturniidae

Published online by Cambridge University Press:  09 January 2024

Xuhongyi Zheng Open the ORCID record for Xuhongyi Zheng [Opens in a new window] ,
Zilong Xu ,
Dong Wang  and
Changfa Zhou Open the ORCID record for Changfa Zhou [Opens in a new window]
Xuhongyi Zheng
Affiliation:
The Key Laboratory of Jiangsu Biodiversity and Biotechnology, College of Life Sciences, Nanjing Normal University, Nanjing 210023, China
Zilong Xu
Affiliation:
The Key Laboratory of Jiangsu Biodiversity and Biotechnology, College of Life Sciences, Nanjing Normal University, Nanjing 210023, China
Dong Wang
Affiliation:
The Key Laboratory of Jiangsu Biodiversity and Biotechnology, College of Life Sciences, Nanjing Normal University, Nanjing 210023, China
Changfa Zhou*
Affiliation:
The Key Laboratory of Jiangsu Biodiversity and Biotechnology, College of Life Sciences, Nanjing Normal University, Nanjing 210023, China
*
Corresponding author: Changfa Zhou; Email: zhouchangfa@njnu.edu.cn
Get access Rights & Permissions [Opens in a new window]

Abstract

The subfamilies Salassinae and Agliinae are two monogeneric groups of the family Saturniidae. They were regarded as the non-cocooning saturniids in Asia. Since very little information on their life history and mitogenome has been reported, their origin and evolution are still poorly understood. In this study, nature-imitated rearing is used to record the life history of two Aglia and five Salassa species. In addition, four complete mitogenomes are presented, which are the first ones of these two subfamilies. The results show that both Salassinae and Agliinae have lost their cocooning. Moreover, the phylogenetic analysis demonstrates that the subfamily Saturniinae is not monophyletic due to the inclusion of Agliinae and Salassinae.

Keywords

AgliacaterpillarChinaSalassasilkmoth
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 114 , Issue 1 , February 2024 , pp. 107 - 123
Check for updates
Copyright
Copyright © The Author(s), 2024. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Bernt, M, Donath, A, Juhling, F, Externbrink, F, Florentz, C, Fritzsch, G, Putz, J, Middendorf, M and Stadler, PF (2013) MITOS: improved de novo metazoan mitochondrial genome annotation. Molecular Phylogenetics and Evolution 69, 313–319.CrossRefGoogle ScholarPubMed
Cao, YQ, Ma, C, Chen, JY and Yang, DR (2012) The complete mitochondrial genomes of two ghost moths, Thitarodes renzhiensis and Thitarodes yunnanensis: the ancestral gene arrangement in Lepidoptera. BMC Genomics 13, 1–13.CrossRefGoogle ScholarPubMed
Chen, F, Porter, D and Vollrath, F (2012) Morphology and structure of silkworm cocoons. Materials Science and Engineering: C 32, 772–778.CrossRefGoogle Scholar
Chen, MM, Li, Y, Chen, M, Wang, H, Li, Q, Xia, RX, Zeng, CY, Li, YP, Liu, YQ and 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.CrossRefGoogle ScholarPubMed
Chen, S, Zhou, Y, Chen, Y and Gu, J (2018) fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics (Oxford, England) 34, i884–i890.Google ScholarPubMed
Chen, DB, Zhang, RS, Jin, XD, Yang, J, Li, P and Liu, YQ (2022) First complete mitochondrial genome of Rhodinia species (Lepidoptera: Saturniidae): genome description and phylogenetic implication. Bulletin of Entomological Research 112, 243–252.CrossRefGoogle ScholarPubMed
Craig, CL (2003) Spiderwebs and Silk: Tracing Evolution From Molecules to Genes to Phenotypes. New York, USA: Oxford University Press, 230 pp.CrossRefGoogle Scholar
Eltayba, MT and Magidb, TDA (2013) Relation between female cocoons (pupae) measurements and the number of eggs laid (fecundity) by the wild silk moth Epiphora bauhiniae (Gurin-meneville) Lepidopetera: saturniidae. International Journal of Advance Industrial Engineering 1, 16–19.Google Scholar
Folmer, O, Black, M, Hoeh, W, Lutz, R and Vrijenhoek, R (1994) DNA primers for amplification of mitochondrial cytochrome coxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3, 294–299.Google Scholar
Friedlander, TP, Horst, KR, Regier, JC, Mitter, C, Peigler, RS and Fang, QQ (1998) Two nuclear genes yield concordant relationships within Attacini (Lepidoptera: Saturniidae). Molecular Phylogenetics and Evolution 9, 131–140.CrossRefGoogle ScholarPubMed
Friedlander, TP, Peigler, RS, Regier, JC and Mitter, C (2002) Monophyly, composition, and relationships within Saturniinae (Lepidoptera: Saturniidae): evidence from two nuclear genes. Insect Systematics & Evolution 33, 9–21.CrossRefGoogle Scholar
Kalyaanamoorthy, S, Minh, BQ, Wong, TKF, von Haeseler, A and Jermiin, LS (2017) ModelFinder: fast model selection for accurate phylogenetic estimates. Nature Methods 14, 587–589.CrossRefGoogle ScholarPubMed
Katoh, K and Standley, DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution 30, 772–780.CrossRefGoogle ScholarPubMed
Kim, JS, Kim, MJ, Jeong, JS and Kim, I (2018) Complete mitochondrial genome of Saturnia jonasii (Lepidoptera: Saturniidae): genomic comparisons and phylogenetic inference among Bombycoidea. Genomics 110, 274–282.CrossRefGoogle ScholarPubMed
Kimura, M (1980) A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution 16, 111–120.CrossRefGoogle ScholarPubMed
Lampe, RE (2010) Saturniidae of the World. Their Life Stages From the Eggs to the Adults. Munich, Germany: Verlag Dr Friedrich Pfeil, 368 pp.Google Scholar
Li, W, Zhang, Z, Lin, L and Terenius, O (2017) Antheraea pernyi (Lepidoptera: Saturniidae) and its importance in sericulture, food consumption, and traditional Chinese medicine. Journal of Economic Entomology 110, 1404–1411.CrossRefGoogle ScholarPubMed
Liu, Z and Peigler, RS (2021) The life history and entomophagy of Saturnia centralis and related Saturniidae. The Journal of the Lepidopterists’ Society 75, 174–186.CrossRefGoogle Scholar
Lowe, TM and Chan, PP (2016) tRNAscan-SE On-line: integrating search and context for analysis of transfer RNA genes. Nucleic Acids Research 44, 54–57.CrossRefGoogle ScholarPubMed
Lu, D, Huang, Y, Naumann, S, Kitching, IJ, Xu, Z, Sun, Y and Wang, X (2022) Mitochondrial genomes of two wild silkmoths, Samia watsoni and Samia wangi (Lepidoptera: Saturniidae), and their phylogenetic implications. European Journal of Entomology 119, 337–353.CrossRefGoogle Scholar
Meng, G, Li, Y, Yang, C and Liu, S (2019) MitoZ: a toolkit for mitochondrial genome assembly, annotation and visualization. Nucleic Acids Research 47, e63.CrossRefGoogle ScholarPubMed
Miller, MA, Wayne, P and Terri, S (2011) The CIPRES science gateway: A community resource for phylogenetic analyses. p. 1 in Proceedings of the 2011 TeraGrid Conference: Extreme Digital Discovery, Salt Lake City Utah, 18–21 July 2011 1–8 New York, Association for Computing Machinery. https://doi.org/10.1145/2016741.2016785CrossRefGoogle Scholar
Naumann, S and Lalhmingliani, E (2019) Notes on taxa of the Salassa lemaii group (Lepidoptera: Saturniidae) with the description of a new species from Mizoram, India. BIONOTES 21, 152–158.Google Scholar
Naumann, S, Brosch, U and Nässig, WA (2003) A catalogue and annotated checklist of the subfamily Agliinae PACKARD, 1893 (Lepidoptera: Saturniidae). 1. Review of the Aglia species with description of a new taxon from Sichuan, China. Nachrichten des Entomologischen Vereins Apollo, Frankfurt am Main, NF 24, 173–182.Google Scholar
Nethavhani, Z, Straeuli, R, Hiscock, K, Veldtman, R, Morton, A, Oberprieler, RG and van Asch, B (2022) Mitogenomics and phylogenetics of twelve species of African Saturniidae (Lepidoptera). PeerJ 10, e13275.CrossRefGoogle ScholarPubMed
Oberprieler, RG, Morton, AS and van Noort, S (2021) The life history of Vegetia grimmia (Geyer, 1832) (Saturniidae: Bunaeinae: Micragonini), with an account of its discovery, distribution and taxonomic distinction. Metamorphosis 32, 74–92.CrossRefGoogle Scholar
Peigler, RS and Liu, Z (2022) The life history and phylogeny of Samia watsoni (Saturniidae), A Relict Species Endemic to China. The Journal of the Lepidopterists’ Society 76, 93–101.CrossRefGoogle Scholar
Perna, NT and Kocher, TD (1995) Patterns of nucleotide composition at fourfold degenerate sites of animal mitochondrial genomes. Journal of Molecular Evolution 41, 353–358.CrossRefGoogle ScholarPubMed
Poulton, EB (1888) XV. Notes in 1887 upon lepidopterous larvæ, &c, including a complete account of the life-history of the larvæ of Sphinx convolvuli and Aglia tau. Transactions of the Royal Entomological Society of London 36, 515–606.CrossRefGoogle Scholar
Regier, JC, Grant, MC, Mitter, C, Cook, CP, Peigler, RS and Rougerie, R (2008) Phylogenetic relationships of wild silkmoths (Lepidoptera: Saturniidae) inferred from four protein-coding nuclear genes. Systematic Entomology 33, 219–228.CrossRefGoogle Scholar
Ronquist, F, Teslenko, M, Mark, PVD, Ayres, DL, Darling, A, Höhna, S, Larget, B, Liu, L, Suchard, MA and Huelsenbeck, JP (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61, 539–542.CrossRefGoogle ScholarPubMed
Rougerie, R and Estradel, Y (2008) Morphology of the preimaginal stages of the African emperor moth Bunaeopsis licharbas (Maassen and Weyding): phylogenetically informative characters within the Saturniinae (Lepidoptera: Saturniidae). Journal of Morphology 269, 207–232.CrossRefGoogle ScholarPubMed
Rozas, J, Ferrer-Mata, A, Sánchez-DelBarrio, JC, Guirao-Rico, S, Librado, P, Ramos-Onsins, SE and Alejandro, SG (2017) DnaSP 6: DNA sequence polymorphism analysis of large data sets. Molecular Biology and Evolution 34, 3299–3302.CrossRefGoogle ScholarPubMed
Rubinoff, D and Doorenweerd, C (2020) Systematics and biogeography reciprocally illuminate taxonomic revisions in the silkmoth genus Saturnia (Lepidoptera: Saturniidae). The Journal of the Lepidopterists’ Society 74, 1–6.CrossRefGoogle Scholar
Stamatakis, A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics (Oxford, England) 30, 1312–1313.Google ScholarPubMed
Talavera, G and Castresana, J (2007) Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Systematic Biology 56, 564–577.CrossRefGoogle ScholarPubMed
Tamura, K, Stecher, G and Kumar, S (2021) MEGA 11: molecular evolutionary genetics analysis version 11. Molecular Biology and Evolution 38, 3022–3027.CrossRefGoogle Scholar
Taylor, TA (1964) Notes on the biology of Bunaea alcinoe Cram. (Lepidoptera: Saturniidae). Annals and Magazine of Natural History 7, 17–25.CrossRefGoogle Scholar
Tsukada, M, Kajiura, Z, Shoumura, S and Satoh, S (2012) Spinning behaviors and physical properties of silk fiber from the wild silkworm, Rhodinia fugax. Journal of Silk Science and Technology of Japan 20, 27–33.Google Scholar
Yanai, Z, Sartori, M, Dor, R and Dorchin, N (2017) Molecular phylogeny and morphological analysis resolve a long-standing controversy over generic concepts in Ecdyonurinae mayflies (Ephemeroptera: Heptageniidae). Systematic Entomology 42, 182–193.CrossRefGoogle Scholar
Zhang, W and Kohll, S (2008) Salassa shuyiae n. sp., a new giant silkmoth from Hainan, China (Lepidoptera, Saturniidae, Salassinae). Nachrichten des entomologischen Vereins Apollo N.F 29, 47–52.Google Scholar
Zhang, X, Yue, C, Liu, A and Ma, P (2011) Research on biological characteristics of Neoris haraldi Schawerda. Xinjiang Agricultural Sciences 48, 672–676.Google Scholar
Zhang, D, Gao, F, Jakovli´c, I, Zou, H, Zhang, J, Li, WX and Wang, GT (2020) PhyloSuite: an integrated and scalable desktop platform for streamlined molecular sequence data management and evolutionary phylogenetics studies. Molecular Ecology Resources 20, 348–355.CrossRefGoogle ScholarPubMed