Large-scale genomic data reveal the phylogeny and evolution of owlet moths (Noctuoidea).
Journal
Cladistics : the international journal of the Willi Hennig Society
ISSN: 1096-0031
Titre abrégé: Cladistics
Pays: United States
ID NLM: 9881057
Informations de publication
Date de publication:
03 Oct 2023
03 Oct 2023
Historique:
revised:
24
08
2023
received:
21
04
2023
accepted:
28
08
2023
medline:
3
10
2023
pubmed:
3
10
2023
entrez:
3
10
2023
Statut:
aheadofprint
Résumé
The owlet moths (Noctuoidea; ~43-45K described species) are one of the most ecologically diverse and speciose superfamilies of animals. Moreover, they comprise some of the world's most notorious pests of agriculture and forestry. Despite their contributions to terrestrial biodiversity and impacts on ecosystems and economies, the evolutionary history of Noctuoidea remains unclear because the superfamily lacks a statistically robust phylogenetic and temporal framework. We reconstructed the phylogeny of Noctuoidea using data from 1234 genes (946.4 kb nucleotides) obtained from the genome and transcriptome sequences of 76 species. The relationships among the six families of Noctuoidea were well resolved and consistently recovered based on both concatenation and gene coalescence approaches, supporting the following relationships: Oenosandridae + (Notodontidae + (Erebidae + (Nolidae + (Euteliidae + Noctuidae)))). A Yule tree prior with three unlinked molecular clocks was identified as the preferred BEAST analysis using marginal-likelihood estimations. The crown age of Noctuoidea was estimated at 74.5 Ma, with most families originating before the end of the Paleogene (23 Ma). Our study provides the first statistically robust phylogenetic and temporal framework for Noctuoidea, including all families of owlet moths, based on large-scale genomic data.
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : Division of Biological Infrastructure
ID : #1349345
Organisme : Division of Environmental Biology
ID : #1557007
Organisme : National Geographic Early Career Grant
ID : EC-51416R-18
Organisme : NSF GRFP
ID : DGE-1315138
Informations de copyright
© 2023 Willi Hennig Society.
Références
Avise, J.C. and Robinson, T.J., 2008. Hemiplasy: a new term in the lexicon of phylogenetics. Syst. Biol. 57, 503-507.
Bachand, M., Pellerin, S., Côté, S.D., Moretti, M., De Cáceres, M., Brousseau, P.M., Cloutier, C., Hébert, C., Cardinal, É., Martin, J.L. and Poulin, M., 2014. Species indicators of ecosystem recovery after reducing large herbivore density: comparing taxa and testing species combinations. Ecol. Indic. 38, 12-19.
Baele, G., Lemey, P., Bedford, T., Rambaut, A., Suchard, M.A. and Alekseyenko, A.V., 2012. Improving the accuracy of demographic and molecular clock model comparison while accommodating phylogenetic uncertainty. Mol. Biol. Evol. 29, 2157-2167.
Baele, G., Li, W.L.S., Drummond, A.J., Suchard, M.A. and Lemey, P., 2013. Accurate model selection of relaxed molecular clocks in Bayesian phylogenetics. Mol. Biol. Evol. 30, 239-243.
Bazinet, A.L., Cummings, M.P., Mitter, K.T. and Mitter, C.W., 2013. Can RNA-seq resolve the rapid radiation of advanced moths and butterflies (Hexapoda: Lepidoptera: Apoditrysia)? An exploratory study. PLoS One 8, e82615.
Borowiec, M.L., 2016. AMAS: a fast tool for alignment manipulation and computing of summary statistics. PeerJ 2016, e1660.
Bouckaert, R., Heled, J., Kühnert, D., Vaughan, T., Wu, C.-H., Xie, D., Suchard, M.A., Rambaut, A. and Drummond, A.J., 2014. BEAST 2: a software platform for Bayesian evolutionary analysis. PLoS Comput. Biol. 10, 1-6.
Bravo, G.A., Antonelli, A., Bacon, C.D., Bartoszek, K., Blom, M.P.K., Huynh, S., Jones, G., Knowles, L.L., Lamichhaney, S., Marcussen, T., Morlon, H., Nakhleh, L.K., Oxelman, B., Pfeil, B., Schliep, A., Wahlberg, N., Werneck, F.P., Wiedenhoeft, J., Willows-Munro, S. and Edwards, S.V., 2019. Embracing heterogeneity: coalescing the tree of life and the future of phylogenomics. PeerJ 7, e6399.
Corcoran, A.J., Barber, J.R. and Conner, W.E., 2009. Tiger moth jams bat sonar. Science 325, 325-327.
Degnan, J.H. and Rosenberg, N.A., 2009. Gene tree discordance, phylogenetic inference and the multispecies coalescent. Trends Ecol. Evol. 24, 332-340.
Derks, M.F., Smit, S., Salis, L., Schijlen, E., Bossers, A., Mateman, C., Pijl, A.S., de Ridder, D., Groenen, M.A., Visser, M.E. and Megens, H.J., 2015. The genome of winter moth (Operophtera brumata) provides a genomic perspective on sexual dimorphism and phenology. Genome Biol. Evol. 7, 2321-2332.
Djaman, K., Higgins, C., O'Neill, M., Begay, S., Koudahe, K. and Allen, S., 2019. Population dynamics of six major insect pests during multiple crop growing seasons in northwestern New Mexico. Insects 10, 369. https://doi.org/10.3390/insects10110369.
Dowdy, N.J., Keating, S., Lemmon, A.R., Lemmon, E.M., Conner, W.E., Scott Chialvo, C.H., Weller, S.J., Simmons, R.B., Sisson, M.S., and Zaspel, J.M., 2020. A deeper meaning for shallow-level phylogenomic studies: nested anchored hybrid enrichment offers great promise for resolving the tiger moth tree of life (Lepidoptera: Erebidae: Arctiinae). Syst. Entomol. 45, 874-893. Portico. https://doi.org/10.1111/syen.12433
Drummond, A.J., Ho, S.Y.W., Phillips, M.J. and Rambaut, A., 2006. Relaxed phylogenetics and dating with confidence. PLoS Biol. 4, 699-710.
Drummond, A.J., Suchard, M.A., Xie, D. and Rambaut, A., 2012. Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol. Biol. Evol. 29, 1969-1973.
Feng, S., Bai, M., Rivas-González, I., Li, C., Liu, S., Tong, Y., Yang, H., Chen, G., Xie, D., Sears, K.E., Franco, L.M., Gaitan-Espitia, J.D., Nespolo, R.F., Johnson, W.E., Yang, H., Brandies, P.A., Hogg, C.J., Belov, K., Renfree, M.B., Helgen, K.M., Boomsma, J.J., Schierup, M.H. and Zhang, G., 2022. Incomplete lineage sorting and phenotypic evolution in marsupials. Cell 185, 1646-1660.
Galarza, J.A., Dhaygude, K. and Mappes, J., 2017. De novo transcriptome assembly and its annotation for the aposematic wood tiger moth (Parasemia plantaginis). Genomics Data 12, 71-73.
Gatesy, J. and Springer, M.S., 2013. Concatenation versus coalescence versus “concatalescence”. Proc. Natl. Acad. Sci. 110, E1179.
Gatesy, J. and Springer, M.S., 2014. Phylogenetic analysis at deep timescales: unreliable gene trees, bypassed hidden support, and the coalescence/concatalescence conundrum. Mol. Phylogenet. Evol. 80, 231-266.
Goloboff, P.A. and Morales, M.E., 2023. TNT version 1.6, with a graphical interface for MacOS and Linux, including new routines in parallel. Cladistics 39, 144-153.
Gschloessl, B., Dorkeld, F., Berges, H., Beydon, G., Bouchez, O., Branco, M., Bretaudeau, A., Burban, C., Dubois, E., Gauthier, P., Lhuillier, E., Nichols, J., Nidelet, S., Rocha, S., Sauné, L., Streiff, R., Gautier, M. and Kerdelhué, C., 2018. Draft genome and reference transcriptomic resources for the urticating pine defoliator Thaumetopoea pityocampa (Lepidoptera: Notodontidae). Mol. Ecol. Resour. 18, 602-619.
Gu, T., Huang, K., Tian, S., Sun, Y., Li, H., Chen, C. and Hao, D., 2019. Antennal transcriptome analysis and expression profiles of odorant binding proteins in Clostera restitura. Comp. Biochem. Physiol. D Genom. Proteom. 29, 211-220.
Guindon, S., Dufayard, J.-F., Lefort, V., Anisimova, M., Hordijk, W. and Gascuel, O., 2010. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst. Biol. 59, 307-321.
Hardwick, K.M., Ojwang', A.M.E., Stomeo, F., Maina, S., Bichang'a, G., Calatayud, P.A., Filée, J., Djikeng, A., Miller, C., Cepko, L., Darby, A.C., Le Ru, B. and Schaack, S., 2019. Draft genome of Busseola fusca, the maize stalk borer, a major crop pest in sub-Saharan Africa. Genome Biol. Evol. 11, 2203-2207.
Heikkilä, M., Simonsen, T.J. and Solis, M.A., 2018. Reassessment of known fossil Pyraloidea (Lepidoptera) with descriptions of the oldest fossil pyraloid and a crambid larva in Baltic amber. Zootaxa 4483, 101-127.
Hoang, D.T., Chernomor, O., von Haeseler, A., Minh, B.Q. and Vinh, L.S., 2018. UFBoot2: improving the ultrafast bootstrap approximation. Mol. Biol. Evol. 35, 518-522.
Homziak, N.T., Breinholt, J.W., Branham, M.A., Storer, C.G. and Kawahara, A.Y., 2019. Anchored hybrid enrichment phylogenomics resolves the backbone of erebine moths. Mol. Phylogenet. Evol. 131, 99-105.
International Silkworm Genome Consortium, 2008. The genome of a lepidopteran model insect, the silkworm Bombyx mori. Insect Biochem. Mol. Biol. 38, 1036-1045.
Jeffroy, O., Brinkmann, H., Delsuc, F. and Philippe, H., 2006. Phylogenomics: the beginning of incongruence? Trends Genet. 22, 225-231.
Lafontaine, J.D., Fibiger, M., 2006. Revised higher classification of the Noctuoidea (Lepidoptera). Can. Entomol. 138(5), 610-635. https://doi.org/10.4039/n06-012.
Kalyaanamoorthy, S., Minh, B.Q., Wong, T.K.F., von Haeseler, A. and Jermiin, L.S., 2017. ModelFinder: fast model selection for accurate phylogenetic estimates. Nat. Methods 14, 587-589.
Katoh, K. and Standley, D.M., 2013. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol. Biol. Evol. 30, 772-780.
Kawahara, A.Y. and Breinholt, J.W., 2014. Phylogenomics provides strong evidence for relationships of butterflies and moths. Proc. R. Soc. B Biol. Sci. 281, 20140970.
Kawahara, A.Y., Plotkin, D., Espeland, M., Meusemann, K., Toussaint, E.F.A., Donath, A., Gimnich, F., Frandsen, P.B., Zwick, A., dos Reis, M., Barber, J.R., Peters, R.S., Liu, S., Zhou, X., Mayer, C., Podsiadlowski, L., Storer, C., Yack, J.E., Misof, B. and Breinholt, J.W., 2019. Phylogenomics reveals the evolutionary timing and pattern of butterflies and moths. Proc. Natl. Acad. Sci. USA 116, 22657-22663.
Keegan, K.L., Lafontaine, J.D., Wahlberg, N. and Wagner, D.L., 2019. Towards resolving and redefining Amphipyrinae (Lepidoptera, Noctuoidea, Noctuidae): a massively polyphyletic taxon. Syst. Entomol. 44, 451-464.
Keegan, K.L., Rota, J., Zahiri, R., Zilli, A., Wahlberg, N., Schmidt, B.C., Lafontaine, J.D., Goldstein, P.Z. and Wagner, D.L., 2021. Toward a stable global Noctuidae (Lepidoptera) taxonomy. Insect Syst. Divers. 5, 1.
Kitching, I.J., 2002. The phylogenetic relationships of Morgan's Sphinx, Xanthopan morganii (Walker), the tribe Acherontiini, and allied long-tongued hawkmoths (Lepidoptera: Sphingidae, Sphinginae). Zool. J. Linn. Soc. 135, 471-527.
Kitching, I. and Rawlins, J., 1998. Noctuoidea. In: Kristensen, N. (Ed.), Lepidoptera, Vol. 1: Systematics and Evolution. Walter de la Mare, Berlin, pp. 355-401.
Kobayashi, H. and Nonaka, M., 2016. Molecular phylogeny of the Notodontidae: subfamilies inferred from 28S rRNA sequences (Lepidoptera, Noctuoidea, Notodontidae). Tinea 23, 1-83.
Kono, N., Nakamura, H., Ohtoshi, R., Tomita, M., Numata, K. and Arakawa, K., 2019. The bagworm genome reveals a unique fibroin gene that provides high tensile strength. Commun. Biol. 2, 148.
Krueger, F., 2012. Trim galore: a wrapper tool around cutadapt and FastQC to consistently apply quality and adapter trimming to FastQ files, with some extra functionality for MspI-digested RRBS-type (Reduced Representation Bisufite-Seq) libraries.
Kück, P., 2009. ALICUT: A Perlscript which Cuts ALISCORE Identified RSS. Version 2.3. Department of Bioinformatics, Zoologisches Forschungsmuseum A Koenig (ZFMK), Bonn.
Kück, P. and Longo, G.C., 2014. FASconCAT-G: extensive functions for multiple sequence alignment preparations concerning phylogenetic studies. Front. Zool. 11, 1-8.
Kück, P., Meusemann, K., Dambach, J., Thormann, B., von Reumont, B.M., Wägele, J.W. and Misof, B., 2010. Parametric and non-parametric masking of randomness in sequence alignments can be improved and leads to better resolved trees. Front. Zool. 7, 1-12.
Kumar, S., Filipski, A.J., Battistuzzi, F.U., Pond, S.L.K. and Tamura, K., 2012. Statistics and truth in phylogenomics. Mol. Biol. Evol. 29, 457-472.
Kusnezov, N., 1928. Oligamatites martynovi, gen. et sp. n., a fossil amatid lepidopteron from the Oligocene beds of Central Asia. Dokl. Akad. Nauk SSSR 20, 431-436.
Li, X., Hamilton, C.A., St Laurent, R., Ballesteros-Mejia, L., Markee, A., Haxaire, J., Rougerie, R., Kitching, I.J. and Kawahara, A.Y., 2022a. A diversification relay race from Caribbean-Mesoamerica to the Andes: historical biogeography of Xylophanes hawkmoths. Proc. R. Soc. B 289, 20212435.
Li, X., St Laurent, R., Earl, C., Doorenweerd, C., van Nieukerken, E.J., Davis, D.R., Johns, C.A., Kawakita, A., Kobayashi, S., Zwick, A. and Lopez-Vaamonde, C., 2022b. Phylogeny of gracillariid leaf-mining moths: evolution of larval behaviour inferred from phylogenomic and Sanger data. Cladistics 38, 277-300.
Liu, L., Xi, Z., Wu, S., Davis, C.C. and Edwards, S.V., 2015. Estimating phylogenetic trees from genome-scale data. Ann. N. Y. Acad. Sci. 1360, 36-53.
Miller, J.S., 1991. Cladistics and classification of the Notodontidae (Lepidoptera, Noctuoidea) based on larval and adult morphology. Bull. Am. Mus. Nat. Hist. 204, 230.
Minh, B.Q., Nguyen, M.A.T. and von Haeseler, A., 2013. Ultrafast approximation for phylogenetic bootstrap. Mol. Biol. Evol. 30, 1188-1195.
Minh, B.Q., Hahn, M.W. and Lanfear, R., 2020. New methods to calculate concordance factors for phylogenomic datasets. Mol. Biol. Evol. 37, 2727-2733.
Misof, B. and Misof, K., 2009. A Monte Carlo approach successfully identifies randomness in multiple sequence alignments: a more objective means of data exclusion. Syst. Biol. 58, 21-34.
Misof, B., Liu, S., Meusemann, K., Peters, R.S., Donath, A., Mayer, C., Frandsen, P.B., Ware, J., Flouri, T., Beutel, R.G., Niehuis, O., Petersen, M., Izquierdo-Carrasco, F., Wappler, T., Rust, J., Aberer, A.J., Aspöck, U., Aspöck, H., Bartel, D., Blanke, A., Berger, S., Böhm, A., Buckley, T.R., Calcott, B., Chen, J., Friedrich, F., Fukui, M., Fujita, M., Greve, C., Grobe, P., Gu, S., Huang, Y., Jermiin, L.S., Kawahara, A.Y., Krogmann, L., Kubiak, M., Lanfear, R., Letsch, H., Li, Y., Li, Z., Li, J., Lu, H., Machida, R., Mashimo, Y., Kapli, P., McKenna, D.D., Meng, G., Nakagaki, Y., Navarrete-Heredia, J.L., Ott, M., Ou, Y., Pass, G., Podsiadlowski, L., Pohl, H., von Reumont, B.M., Schütte, K., Sekiya, K., Shimizu, S., Slipinski, A., Stamatakis, A., Song, W., Su, X., Szucsich, N.U., Tan, M., Tan, X., Tang, M., Tang, J., Timelthaler, G., Tomizuka, S., Trautwein, M., Tong, X., Uchifune, T., Walzl, M.G., Wiegmann, B.M., Wilbrandt, J., Wipfler, B., Wong, T.K.F., Wu, Q., Wu, G., Xie, Y., Yang, S., Yang, Q., Yeates, D.K., Yoshizawa, K., Zhang, Q., Zhang, R., Zhang, W., Zhang, Y., Zhao, J., Zhou, C., Zhou, L., Ziesmann, T., Zou, S., Li, Y., Xu, X., Zhang, Y., Yang, H., Wang, J., Wang, J., Kjer, K.M. and Zhou, X., 2014. Phylogenomics resolves the timing and pattern of insect evolution. Science 346, 763-767.
Mitchell, A., Mitter, C. and Regier, J.C., 2006. Systematics and evolution of the cutworm moths (Lepidoptera: Noctuidae): evidence from two protein-coding nuclear genes. Syst. Entomol. 31, 21-46.
Mutanen, M., Wahlberg, N. and Kaila, L., 2010. Comprehensive gene and taxon coverage elucidates radiation patterns in moths and butterflies. Proc. R. Soc. B Biol. Sci. 277, 2839-2848.
Naik, M.I., Kumar, M.A., Manjunatha, M. and Shivanna, B.K., 2010. Survey for the pests of castor and natural enemies of castor semilooper. Environ. Ecol. 28, 558-563.
Nguyen, L.T., Schmidt, H.A., von Haeseler, A. and Minh, B.Q., 2015. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol. Biol. Evol. 32, 268-274.
van Nieukerken, E.J., Kaila, L., Kitching, I.J., Kristensen, N.P., Lees, D.C., Minet, J., Mitter, C., Mutanen, M., Regier, J.C., Simonsen, T.J., Wahlberg, N., Yen, S.-H., Zahiri, R., Adamski, D., Baixeras, J., Bartsch, D., Bengtsson, B.Å., Brown, J.W., Bucheli, S.R., Davis, D.R., De Prins, J., De Prins, W., Epstein, M.E., Gentili-Poole, P., Gielis, C., Hättenschwiler, P., Hausmann, A., Holloway, J.D., Kallies, A., Karsholt, O., Kawahara, A.Y., Koster, S.J.C., Kozlov, M.V., Lafontaine, J.D., Lamas, G., Landry, J.-F., Lee, S., Nuss, M., Park, K.-T., Penz, C.M., Rota, J., Schintlmeister, A., Schmidt, B.C., Sohn, J.-C., Solis, M.A., Tarmann, G.M., Warren, A.D., Weller, S.J., Yakovlev, R.V., Zolotuhin, V.V. and Zwick, A., 2011. Order Lepidoptera Linnaeus, 1758. In: Zhang, Z.-Q. (ed.) animal biodiversity: an outline of higher-level classification and survey of taxonomic richness. Zootaxa 3148, 212-221.
Oakley, T.H., Alexandrou, M.A., Ngo, R., Pankey, M.S., Churchill, C.K.C., Chen, W. and Lopker, K.B., 2014. Osiris: accessible and reproducible phylogenetic and phylogenomic analyses within the galaxy workflow management system. BMC Bioinformatics 15, 1-9.
Oppenheim, S.J., Feindt, W., DeSalle, R. and Goldstein, P.Z., 2018. De novo characterization of transcriptomes from two North American Papaipema stem-borers (Lepidoptera: Noctuidae). PLoS One 13, e0191061.
Pease, J.B., Haak, D.C., Hahn, M.W. and Moyle, L.C., 2016. Phylogenomics reveals three sources of adaptive variation during a rapid radiation. PLoS Biol. 14, e1002379.
Pease, J.B., Brown, J.W., Walker, J.F., Hinchliff, C.E. and Smith, S.A., 2018. Quartet sampling distinguishes lack of support from conflicting support in the green plant tree of life. Am. J. Bot. 105, 385-403.
Petersen, M., Meusemann, K., Donath, A., Dowling, D., Liu, S., Peters, R.S., Podsiadlowski, L., Vasilikopoulos, A., Zhou, X., Misof, B. and Niehuis, O., 2017. Orthograph: a versatile tool for mapping coding nucleotide sequences to clusters of orthologous genes. BMC Bioinformatics 18, 1-10.
Rambaut, A. and Drummond, A.J., 2015. TreeAnnotator v1. 8.2. MCMC Output Analysis.
Rambaut, A., Drummond, A.J., Xie, D., Baele, G. and Suchard, M.A., 2018. Posterior summarization in Bayesian phylogenetics using tracer 1.7. Syst. Biol. 67, 901-904.
Ranwez, V. and Douzery, E.J.P., 2018. MACSE v2: toolkit for the alignment of coding sequences accounting for frameshifts and stop codons. Mol. Biol. Evol. 35, 2582-2584.
Regier, J.C., Shultz, J.W., Zwick, A., Hussey, A., Ball, B., Wetzer, R., Martin, J.W. and Cunningham, C.W., 2010. Arthropod relationships revealed by phylogenomic analysis of nuclear protein-coding sequences. Nature 463, 1079-1083.
Regier, J.C., Mitter, C., Mitter, K., Cummings, M.P., Bazinet, A.L., Hallwachs, W., Janzen, D.H. and Zwick, A., 2017. Further progress on the phylogeny of Noctuoidea (Insecta: Lepidoptera) using an expanded gene sample. Syst. Entomol. 42, 82-93.
Reid, E.T.M., 1954. Observations on feeding habits of adult Arcyophora. Proceedings of the Royal Entomological Society of London 23, 200-204.
Sayyari, E., Whitfield, J.B. and Mirarab, S., 2018. DiscoVista: interpretable visualizations of gene tree discordance. Mol. Phylogenet. Evol. 122, 110-115.
Shimodaira, H. and Hasegawa, M., 2002. CONSEL: for assessing the confidence of phylogenetic tree selection. Bioinformatics 17, 1246-1247.
Simmons, R.B., Weller, S.J. and Johnson, S.J., 2012. The evolution of androconia in mimetic tiger moths (Noctuoidea: Erebidae: Arctiinae: Ctenuchina and Euchromiina). Ann. Entomol. Soc. Am. 105, 804-816.
Smith, S.A., Brown, J.W. and Walker, J.F., 2018. So many genes, so little time: A practical approach to divergence-time estimation in the genomic era. PLoS One 13, e0197433.
Sohn, J., Labandeira, C., Davis, D. and Mitter, C., 2012. An annotated catalog of fossil and subfossil Lepidoptera (Insecta: Holometabola) of the world. Zootaxa 3286, 1-132.
Sohn, J., Labandeira, C.C. and Davis, D.R., 2015. The fossil record and taphonomy of butterflies and moths (Insecta, Lepidoptera): implications for evolutionary diversity and divergence-time estimates. BMC Evol. Biol. 15, 1-16.
Springer, M.S. and Gatesy, J., 2016. The gene tree delusion. Mol. Phylogenet. Evol. 94, 1-33.
St Laurent, R.A., Goldstein, P.Z., Miller, S.E. and Robbins, R.K., 2023. Hiding in plain sight: Phylogenomics reveals a new branch on the Noctuoidea tree of life. bioRxiv, 2023-03. https://doi.org/10.1101/2023.03.10.529269
Storer, N.P., Babcock, J.M., Schlenz, M., Meade, T., Thompson, G.D., Bing, J.W. and Huckaba, R.M., 2010. Discovery and characterization of field resistance to Bt maize: Spodoptera frugiperda (Lepidoptera: Noctuidae) in Puerto Rico. J. Econ. Entomol. 103, 1031-1038.
Strimmer, K. and von Haeseler, A., 1997. Likelihood-mapping: A simple method to visualize phylogenetic. Proc. Natl. Acad. Sci. USA 94, 6815-6819.
Suh, A., Smeds, L. and Ellegren, H., 2015. The dynamics of incomplete lineage sorting across the ancient adaptive radiation of neoavian birds. PLoS Biol. 13, e1002224.
Uchibori-Asano, M., Jouraku, A., Uchiyama, T., Yokoi, K., Akiduki, G., Suetsugu, Y., Kobayashi, T., Ozawa, A., Minami, S., Ishizuka, C., Nakagawa, Y., Daimon, T. and Shinoda, T., 2019. Genome-wide identification of tebufenozide resistant genes in the smaller tea tortrix, Adoxophyes honmai (Lepidoptera: Tortricidae). Sci. Rep. 9, 4203.
Wagner, D.L., Schweitzer, D.F., Sullivan, J.B. and Reardon, R.C., 2011. Owlet Caterpillars of Eastern North America. Princeton University Press, Princeton, NJ, p. 576.
Wang, H., Wahlberg, N., Holloway, J.D., Bergsten, J., Fan, X., Janzen, D.H., Hallwachs, W., Wen, L., Wang, M. and Nylin, S., 2015. Molecular phylogeny of Lymantriinae (Lepidoptera, Noctuoidea, Erebidae) inferred from eight gene regions. Cladistics 31, 579-592.
Xie, W., Lewis, P.O., Fan, Y., Kuo, L. and Chen, M.H., 2011. Improving marginal likelihood estimation for Bayesian phylogenetic model selection. Syst. Biol. 60, 150-160.
Xie, Y., Wu, G., Tang, J., Luo, R., Patterson, J., Liu, S., Huang, W., He, G., Gu, S., Li, S., Zhou, X., Lam, T.W., Li, Y., Xu, X., Wong, G.K.S. and Wang, J., 2014. Sequence analysis SOAPdenovo-trans: de novo transcriptome assembly with short RNA-seq reads. Bioinformatics 30, 1660-1666.
Yang, X., Cameron, S.L., Lees, D.C., Xue, D. and Han, H., 2015. A mitochondrial genome phylogeny of owlet moths (Lepidoptera: Noctuoidea), and examination of the utility of mitochondrial genomes for lepidopteran phylogenetics. Mol. Phylogenet. Evol. 85, 230-237.
You, M., Yue, Z., He, W., Yang, X., Yang, G., Xie, M., Zhan, D., Baxter, S.W., Vasseur, L., Gurr, G.M., Douglas, C.J., Bai, J., Wang, P., Cui, K., Huang, S., Li, X., Zhou, Q., Wu, Z., Chen, Q., Liu, C., Wang, B., Li, X., Xu, X., Lu, C., Hu, M., Davey, J.W., Smith, S.M., Chen, M., Xia, X., Tang, W., Ke, F., Zheng, D., Hu, Y., Song, F., You, Y., Ma, X., Peng, L., Zheng, Y., Liang, Y., Chen, Y., Yu, L., Zhang, Y., Liu, Y., Li, G., Fang, L., Li, J., Zhou, X., Luo, Y., Gou, C., Wang, J., Wang, J., Yang, H. and Wang, J., 2013. A heterozygous moth genome provides insights into herbivory and detoxification. Nat. Genet. 45, 220-225.
Zahiri, R., Kitching, I.J., Lafontaine, J.D., Mutanen, M., Kaila, L., Holloway, J.D. and Wahlberg, N., 2011. A new molecular phylogeny offers hope for a stable family level classification of the Noctuoidea (Lepidoptera). Zoologica Scripta 40, 158-173.
Zahiri, R., Holloway, J.D., Kitching, I.J., Lafontaine, J.D., Mutanen, M. and Wahlberg, N., 2012. Molecular phylogenetics of Erebidae (Lepidoptera, Noctuoidea). Syst. Entomol. 37, 102-124.
Zahiri, R., Lafontaine, D., Schmidt, C., Holloway, J.D., Kitching, I.J., Mutanen, M. and Wahlberg, N., 2013a. Relationships among the basal lineages of Noctuidae (Lepidoptera, Noctuoidea) based on eight gene regions. Zoologica Scripta 42, 488-507.
Zahiri, R., Lafontaine, J.D., Holloway, J.D., Kitching, I.J., Schmidt, B.C., Kaila, L. and Wahlberg, N., 2013b. Major lineages of Nolidae (Lepidoptera, Noctuoidea) elucidated by molecular phylogenetics. Cladistics 29, 337-359.
Zahiri, R., Lafontaine, J.D., Schmidt, B.C., Dewaard, J.R., Zakharov, E.V. and Hebert, P.D.N., 2014. A transcontinental challenge - a test of DNA barcode performance for 1,541 species of Canadian Noctuoidea (Lepidoptera). PLoS One 9, 1-12.
Zahiri, R., Holloway, J.D., Rota, J., Schmidt, B.C., Pellinen, M.J., Kitching, I.J., Miller, S.E. and Wahlberg, N., 2023. Evolutionary history of Euteliidae (Lepidoptera, Noctuoidea). Syst. Entomol. 2023, 1-18.
Zaspel, J.M., Scott, C.H., Hill, S.R., Ignell, R., Kononenko, V.S. and Weller, S.J., 2014. Geographic distribution, phylogeny, and genetic diversity of the fruit-and blood-feeding moth Calyptra thalictri Borkhausen (Insecta: Lepidoptera: Erebidae). J. Parasitol. 100, 583-591.
Zhang, Y.N., Jin, J.Y., Jin, R., Xia, Y.H., Zhou, J.J., Deng, J.Y. and Dong, S.L., 2013. Differential expression patterns in chemosensory and non-chemosensory tissues of putative chemosensory genes identified by transcriptome analysis of insect pest the purple stem borer Sesamia inferens (Walker). PLoS One 8, e69715.
Zhang, C., Rabiee, M., Sayyari, E. and Mirarab, S., 2018. ASTRAL-III: polynomial time species tree reconstruction from partially resolved gene trees. BMC Bioinformatics 19, 15-30.
Zwick, A., Regier, J.C. and Zwickl, D.J., 2012. Resolving discrepancy between nucleotides and amino acids in deep-level arthropod phylogenomics: differentiating serine codons in 21-amino-acid models. PLoS One 7, 1-12.