Zoraptera is a small and predominantly tropical insect order with an unresolved higher classification due to the extremely uniform external body morphology. We, therefore, conducted a multigene molecular phylogeny of extant Zoraptera and critically re-evaluated their morphological characters in order to propose a natural infraordinal classification. We recovered a highly-resolved phylogeny with two main clades representing major evolutionary lineages in Zoraptera, for which we propose family ranks. The two families exhibit striking differences in male genitalia and reproductive strategies. Each family contains two subclades (subfamilies) supported by several morphological synapomorphies including the relative lengths of the basal antennomeres, the number and position of metatibial spurs, and the structure of male genitalia. The newly proposed higher classification of Zoraptera includes the family Zorotypidae stat. revid. with Zorotypinae Silvestri, 1913 (Zorotypus stat. revid., Usazoros Kukalova-Peck and Peck, 1993 stat. restit.) and Spermozorinae subfam. nov. (Spermozoros gen. nov.), and Spriralizoridae fam. nov. with Spiralizorinae subfam. nov. (Spiralizoros gen. nov., Scapulizoros gen. nov., Cordezoros gen. nov., Centrozoros Kukalova-Peck and Peck, 1993, stat. restit., Brazilozoros Kukalova-Peck and Peck, 1993, stat. restit.), and Latinozorinae subfam. nov. (Latinozoros Kukalova-Peck and Peck, 1993, stat. restit.). An identification key and morphological diagnoses for all supraspecific taxa are provided.

Department of Biology and Ecology and Institute of Environmental Technologies Faculty of Science University of Ostrava Chittussiho 10 CZ 710 00 Ostrava Czech Republic

Department of Zoology Faculty of Science Palacky University 17 listopadu 50 CZ 771 46 Olomouc Czech Republic

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Mashimo Y., Matsumura Y., Machida R., Dallai R., Gottardo M., Yoshizawa K., Friedrich F., Wipfler B., Beutel R.G. 100 years Zoraptera—A phantom in insect evolution and the history of its investigation. Insect Syst. Evol. 2014;45:371–393. doi: 10.1163/1876312X-45012110. DOI

Choe J.C. Biodiversity of Zoraptera and their little-known biology. In: Foottit R.G., Adler P.H., editors. Insect Biodiversity: Science and Society. 1st ed. Volume 2. John Wiley & Sons Ltd.; New York, NY, USA: 2018. pp. 199–217. DOI

Evangelista D.A., Wipfler B., Béthoux O., Donath A., Fujita M., Kohli M.K., Legendre F., Liu S., Machida R., Misof B., et al. An integrative phylogenomic approach illuminates the evolutionary history of cockroaches and termites (Blattodea) Proc. R. Soc. B. 2019;286:20182076. doi: 10.1098/rspb.2018.2076. PubMed DOI PMC

Montagna M., Tong K.J., Magoga G., Strada L., Tintori A., Ho S.Y., Lo N. Recalibration of the insect evolutionary time scale using Monte San Giorgio fossils suggests survival of key lineages through the End-Permian Extinction. Proc. R. Soc. B. 2019;286:20191854. doi: 10.1098/rspb.2019.1854. PubMed DOI PMC

Matsumura Y., Beutel R.G., Rafael J.A., Yao I., Camara J.T., Lima S.P., Yoshizawa K. The evolution of Zoraptera. Syst. Entomol. 2019 doi: 10.1111/syen.12400. DOI

Beutel R.G., Weide D. Cephalic anatomy of Zorotypus hubbardi (Hexapoda: Zoraptera): New evidence for a relationship with Acercaria. Zoomorphology. 2005;124:121–136. doi: 10.1007/s00435-005-0117-z. DOI

Misof B., Liu S., Meusemann K., Peters R.S., Donath A., Mayer C., Frandsen P.B., Ware J., Flouri T., Beutel R.G., et al. Phylogenomics resolves the timing and pattern of insect evolution. Science. 2014;346:763–767. doi: 10.1126/science.1257570. PubMed DOI

Wipfler B., Letsch H., Frandsen P.B., Kapli P., Mayer C., Bartel D., Buckley T.R., Donath A., Edgerly-Rooks J.S., Fujita M., et al. Evolutionary history of Polyneoptera and its implications for our understanding of early winged insects. Proc. Natl. Acad. Sci. 2019;116:3024–3029. doi: 10.1073/pnas.1817794116. PubMed DOI PMC

Chesters D. The phylogeny of insects in the data-driven era. Syst. Entomol. 2019 doi: 10.1111/syen.12414. DOI

Terry M.D., Whiting M.F. Mantophasmatodea and phylogeny of the lower neopterous insects. Cladistics. 2005;21:240–257. doi: 10.1111/j.1096-0031.2005.00062.x. DOI

Silvestri F. Descrizione di un nuovo ordine di insetti. Boll. Lab. Zool. Gen. Agrar. Portici. 1913;7:193–209.

Mashimo Y., Matsumura Y., Beutel R.G., Njoroge L., Machida R. A remarkable new species of Zoraptera, Zorotypus asymmetristernum sp. n., from Kenya (Insecta, Zoraptera, Zorotypidae) Zootaxa. 2018;4388:407–416. doi: 10.11646/zootaxa.4388.3.6. PubMed DOI

Kukalova-Peck J., Peck S.B. Zoraptera wing structures: Evidence for new genera and relationship with the blattoid orders (Insecta: Blattoneoptera) Syst. Entomol. 1993;18:333–350. doi: 10.1111/j.1365-3113.1993.tb00670.x. DOI

Chao R.F., Chen C.S. Formosozoros newi, a new genus and species of Zoraptera (Insecta) from Taiwan. Pan-Pac. Entomol. 2000;76:24–27.

Engel M.S., Grimaldi D.A. A winged Zorotypus in Miocene amber from the Dominican Republic (Zoraptera: Zorotypidae), with discussion on relationships of and within the order. Acta Geol. Hisp. 2000;35:149–164.

Engel M.S. Phylogeny of the Zoraptera. Entomol. Abh. 2003;61:147–148.

Engel M.S., Grimaldi D.A. The first Mesozoic Zoraptera (Insecta) Am. Mus. Novit. 2002;3362:1–20. doi: 10.1206/0003-0082(2002)362<0001:TFMZI>2.0.CO;2. DOI

Hünefeld F. The genital morphology of Zorotypus hubbardi Caudell, 1918 (Insecta: Zoraptera: Zorotypidae) Zoomorphology. 2007;126:135–151. doi: 10.1007/s00435-007-0033-5. DOI

Dallai R., Mercati D., Gottardo M., Dossey A.T., Machida R., Mashimo Y., Beutel R.G. The male and female reproductive systems of Zorotypus hubbardi Caudell, 1918 (Zoraptera) Arthropod Struct. Dev. 2012;41:337–359. doi: 10.1016/j.asd.2012.01.003. PubMed DOI

Dallai R., Gottardo M., Mercati D., Machida R., Mashimo Y., Matsumura Y., Rafael J.A., Beutel R.G. Comparative morphology of spermatozoa and reproductive systems of zorapteran species from different world regions (Insecta, Zoraptera) Arthropod Struct. Dev. 2014;43:371–383. doi: 10.1016/j.asd.2014.03.001. PubMed DOI

Dallai R., Gottardo M., Mercati D., Rafael J.A., Machida R., Mashimo Y., Matsumutra Y., Beutel R.G. The intermediate sperm type and genitalia of Zorotypus shannoni Gurney: Evidence supporting infraordinal lineages in Zoraptera (Insecta) Zoomorphology. 2015;134:79–91. doi: 10.1007/s00435-014-0244-5. DOI

Boudinot B.E. A general theory of genital homologies for the Hexapoda (Pancrustacea) derived from skeletomuscular correspondences, with emphasis on the Endopterygota. Arthropod Struct. Dev. 2018;47:563–613. doi: 10.1016/j.asd.2018.11.001. PubMed DOI

Yoshizawa K., Johnson K.P. Aligned 18S for Zoraptera (Insecta): Phylogenetic position and molecular evolution. Mol. Phylogenet. Evol. 2005;37:572–580. doi: 10.1016/j.ympev.2005.05.008. PubMed DOI

Ma C., Wang Y., Wu C., Kang L., Liu C. The compact mitochondrial genome of Zorotypus medoensis provides insights into phylogenetic position of Zoraptera. BMC Genom. 2014;15:1156. doi: 10.1186/1471-2164-15-1156. PubMed DOI PMC

Colgan D.J., Cassis G., Beacham E. Setting the molecular phylogenetic framework for the Dermaptera. Insect. Syst. Evol. 2003;34:65–80. doi: 10.1163/187631203788964935. DOI

Kamimura Y. In search of the origin of twin penises: Molecular phylogeny of earwigs (Dermaptera: Forficulina) based on mitochondrial and nuclear ribosomal RNA genes. Ann. Entomol. Soc. Am. 2004;97:903–912. doi: 10.1603/0013-8746(2004)097[0903:ISOTOO]2.0.CO;2. DOI

Jarvis K.J., Haas F., Whiting M.F. Phylogeny of earwigs (Insecta: Dermaptera) based on molecular and morphological evidence: Reconsidering the classification of Dermaptera. Syst. Entomol. 2005;30:442–453. doi: 10.1111/j.1365-3113.2004.00276.x. DOI

Kočárek P., John V., Hulva P. When the body hides the ancestry: Phylogeny of morphologically modified epizoic earwigs based on molecular evidence. PLoS ONE. 2013;8:e66900. doi: 10.1371/journal.pone.0066900. PubMed DOI PMC

Kirstová M., Kundrata R., Kočárek P. Molecular phylogeny and classification of Chelidurella Verhoeff, stat. restit. (Dermaptera: Forficulidae) Insect Syst. Evol. in press.

Folmer O., Black M., Hoeh W., Lutz R., Vrijenhoek R. DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol. Mar. Biol. Biotechnol. 1994;3:294–299. doi: 10.1371/journal.pone.0013102. PubMed DOI

Crandall K.A., Fitzpatrick J.F., Jr. Crayfish molecular systematics: Using a combination of procedures to estimate phylogeny. Syst. Biol. 1996;45:1–26. doi: 10.1093/sysbio/45.1.1. DOI

Whiting M.F., Carpenter J.C., Wheeler Q.D., Wheeler W.C. The Strepsiptera problem: Phylogeny of the holometabolous insect orders inferred from 18S and 28S ribosomal DNA sequences and morphology. Syst. Biol. 1997;46:1–68. doi: 10.1093/sysbio/46.1.1. PubMed DOI

Palumbi S., Martin A., Romaro S., McMillan W.O., Stice L., Grabowski G. The Simple Fool’s Guide to PCR. Version 2.0. University of Hawaii; Honolulu, HI, USA: 2002. pp. 1–45.

Machida R.J., Knowlton N. PCR Primers for metazoan nuclear 18S and 28S ribosomal DNA sequences. PLoS ONE. 2012;7:e46180. doi: 10.1371/journal.pone.0046180. PubMed DOI PMC

Katoh K., Misawa K., Kuma K., Miyata T. MAFFT: A novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res. 2002;30:3059–3066. doi: 10.1093/nar/gkf436. PubMed DOI PMC

Kearse M., Moir R., Wilson A., Stones-Havas S., Cheung M., Sturrock S., Buxton S., Cooper A., Markowitz S., Duran C., et al. Geneious Basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics. 2012;28:1647–1649. doi: 10.1093/bioinformatics/bts199. PubMed DOI PMC

Tamura K., Stecher G., Peterson D., Filipski A., Kumar S. MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol. Biol. Evol. 2013;30:2725–2729. doi: 10.1093/molbev/mst197. PubMed DOI PMC

Lanfear R., Calcott B., Ho S.Y.W., Guindon S. PartitionFinder: Combined selection of partitioning schemes and substitution models for phylogenetic analyses. Mol. Biol. Evol. 2012;29:1695–1701. doi: 10.1093/molbev/mss020. PubMed DOI

Miller M.A., Pfeiffer W., Schwartz T. Creating the CIPRES Science Gateway for inference of large phylogenetic trees; Proceedings of the Gateway Computing Environments Workshop (GCE); New Orleans, LA, USA. 14 November 2010.

Stamatakis A. RAxML-VI-HPC: Maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics. 2006;22:2688–2690. doi: 10.1093/bioinformatics/btl446. PubMed DOI

Stamatakis A., Hoover P., Rougemont J. A rapid bootstrap algorithm for the RAxML web servers. Syst. Biol. 2008;57:758–771. doi: 10.1080/10635150802429642. PubMed DOI

Huelsenbeck J.P., Ronquist F. MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics. 2001;17:754–755. doi: 10.1093/bioinformatics/17.8.754. PubMed DOI

Rambaut A., Drummond A.J., Xie D., Baele G., Suchard M.A. Posterior summarization in Bayesian phylogenetics using Tracer 1.7. Syst. Biol. 2018;67:901–904. doi: 10.1093/sysbio/syy032. PubMed DOI PMC

Xia X., Xie Z., Salemi M., Chen L., Wang Y. An index of substitution saturation and its application. Mol. Phylogenet. Evol. 2003;26:1–7. doi: 10.1016/S1055-7903(02)00326-3. PubMed DOI

Xia X., Lemey P. Assessing substitution saturation with DAMBE. In: Lemey P., Salemi M., Vandamme A.M., editors. The Phylogenetic Handbook: A Practical Approach to DNA and Protein Phylogeny. 2nd ed. Cambridge University Press; Cambridge, UK: 2009. pp. 615–630.

Kočárek P., Wahab R.A., Abdul Kahar S.R. Zorotypus asymmetricus sp. nov. from Brunei Darussalam, Borneo (Insecta: Zoraptera) Zootaxa. 2017;4286:285–290. doi: 10.11646/zootaxa.4286.2.11. DOI

Engel M.S. A new apterous Zorotypus in Miocene amber from the Dominican Republic (Zoraptera: Zorotypidae) Acta Entomol. Slov. 2008;16:127–136.

Holt B.G., Lessard J.-P., Borregaard M.K., Fritz S.A., Araújo M.B., Dimitrov D., Fabre P.-H., Graham C.H., Graves G.R., Jønsson K.A., et al. An update of Wallace’s zoogeographic regions of the World. Science. 2013;339:74–78. doi: 10.1126/science.1228282. PubMed DOI

Wang Y., Engel M.S., Rafael J.A., Dang K., Wu H., Wang Y., Xie Q., Bu W.A. Unique box in 28S rRNA is shared by the enigmatic insect order Zoraptera and Dictyoptera. PLoS ONE. 2013;8:E53679. doi: 10.1371/journal.pone.0053679. PubMed DOI PMC

Gurney A.B. A synopsis of the order Zoraptera, with notes on the biology of Zorotypus hubbardi Caudell. Proc. Entomol. Soc. Wash. 1938;40:57–87.

New T.R. Notes on Neotropical Zoraptera, with descriptions of two new species. Syst. Entomol. 1978;3:361–370. doi: 10.1111/j.1365-3113.1978.tb00005.x. DOI

Rafael J.A., Engel M.S. A new species of Zorotypus from central Amazonia, Brazil (Zoraptera: Zorotypidae) Am. Mus. Novit. 2006;3528:1–11. doi: 10.1206/0003-0082(2006)3528[1:ANSOZF]2.0.CO;2. DOI

Rafael J.A., Godoi F.S., Engel M.S. A new species of Zorotypus from eastern Amazonia, Brazil (Zoraptera: Zorotypidae) Trans. Kans. Acad. Sci. 2008;111:193–202. doi: 10.1660/0022-8443-111.3.193. DOI

Yin Z.W., Li L.Z. Zorotypus huangi sp. nov. (Zoraptera: Zorotypidae) from Yunnan, southern China. Zootaxa. 2017;4300:287–294. doi: 10.11646/zootaxa.4300.2.10. DOI

Mashimo Y., Yoshizawa K., Engel M.S., Ghani I.A., Dallai R., Beutel R.G., Machida R. Zorotypus in Peninsular Malaysia (Zoraptera: Zorotypidae), with the description of three new species. Zootaxa. 2013;3717:498–514. doi: 10.11646/zootaxa.3717.4.4. PubMed DOI

Wang J., Li H., Cai W. Zorotypus weiweii (Zoraptera: Zorotypidae), a new species of angel insects, from Sabah, East Malasia. Zootaxa. 2016;4162:550–558. doi: 10.11646/zootaxa.4162.3.8. PubMed DOI

Huang F.S. Zorotypus chinensis, a new species from China. Acta Entomol. Sin. 1974;17:423–427. (In Chinese, English summary)

Karny H.H. Spolia Mentawiensia. Zoraptera. Treubia. 1927;9:1–5.

New T.R. Zoraptera (Insecta) in east Malaysia: Notes on Zorotypus caudelli Karny. Orient. Insects. 2000;34:77–82. doi: 10.1080/00305316.2000.10417255. DOI

Karny H.H. Zorapteren aus Süd-Sumatra. Treubia. 1922;3:14–29.

Karny H.H. Psocoptera. Insects of Samoa and Other Samoan Terrestrial Arthropoda. Part VII. Other Orders of Insects. British Museum (Natural History); London, UK: 1932. pp. 117–129.

Choe J.C. Zorotypus gurneyi, new species, from Panama and redescription of Z. barberi Gurney (Zoraptera: Zorotypidae) Ann. Entomol. Soc. Am. 1989;82:149–155. doi: 10.1093/aesa/82.2.149. DOI

Choe J.C. Zoraptera of Panama with a review of the morphology, systematics, and biology of the order. In: Quintero D., Aiello A., editors. Insects of Panama and Mesoamerica: Selected Studies. Oxford University Press; Oxford, UK: 1992. pp. 249–256.

Caudell A.N. A new species of Zoraptera from Bolivia. Proc. Entomol. Soc. Wash. 1923;25:60–62.

Bolívar y Pieltain C., Coronado G.L. Estudio de un nuevo Zorotypus proveniente de la Region Amazonica Peruana (Ins., Zoraptera) Ciencia. 1963;22:93–100.

Silvestri F. Descrizione di due specie neotropicali di Zorotypus (Insecta, Zoraptera) Boll. Lab. Entomol. Agrar. Portici. 1946;7:1–12.

Gurney A.B. A new species of Zoraptera from Fiji. Occas. Pap. Bernice P. Bishop Mus. 1939;15:161–165.

Terry M.D., Whiting M.F. Zorotypus novobritannicus n. sp., the first species of the order Zoraptera (Zorotypidae) from the Australasian Ecozone. Zootaxa. 2012;3260:53–61. doi: 10.11646/zootaxa.3260.1.5. DOI

Van Ryn-Tournel J. Presence de l’ordre des Zorapthres au Congo et description de Zorotypus congensis sp. n. Rev. Zool. Bot. Afr. 1971;83:100–110.

Engel M.S. A new Zorotypus from Peru, with notes on related neotropical species (Zoraptera: Zorotypidae) J. Kans. Entomol. Soc. 2000;73:11–20.

New T.R. The order Zoraptera (Insecta) from Christmas Island, Indian Ocean. Invertebr. Syst. 1995;9:243–246. doi: 10.1071/IT9950243. DOI

Weidner H. Mission Zoologique Belge aux iles Galapagos et en Ecuador (N. et J. Leleup 1964–1965) Institut Royal des Sciences Naturelles de Belgique; Bruxelles, Belgium: 1976. Eine neue Zorotypus-Art von den Galapagosinseln, Zorotypus leleupi sp.n. (Zoraptera) pp. 161–176.

Caudell A.N. Zorotypus longicercatus, a new species of Zoraptera from Jamaica. Proc. Entomol. Soc. Wash. 1927;29:144–145.

Zompro O. Inter- and intra-ordinal relationships of the Mantophasmatodea, with comments on the phylogeny of polyneopteran orders (Insecta: Polyneoptera) Mitt. Geol-Paläont. Inst. Univ. Hambg. 2005;89:85–116.

Caudell A.N. Zorotypus swezeyi, a new species of the order Zoraptera from Hawaii. Trans. Am. Entomol. Soc. 1922;48:133–135.

Matsumura Y., Yoshizawa K., Machida R., Mashimo Y., Dallai R., Gottardo M., Kleinteich T., Michels J., Gorb S.N., Beutel R.G. Two intromittent organs in Zorotypus caudelli (Insecta, Zoraptera): The paradoxical coexistence of an extremely long tube and a large spermatophore. Zool. J. Linn. Soc. 2014;112:40–54. doi: 10.1111/bij.12260. DOI

Yin Z., Cai C., Huang D. New zorapterans (Zoraptera) from Burmese amber suggest higher paleodiversity of the order in tropical forests. Cretac. Res. 2018;84:168–172. doi: 10.1016/j.cretres.2017.11.028. DOI

Yin Z., Cai C., Huang D., Engel M.S. Zorotypus dilaticeps sp. nov., a remarkable zorapteran (Zoraptera) in mid-Cretaceous Burmese amber. Cretac. Res. 2018;91:126–130. doi: 10.1016/j.cretres.2018.05.018. DOI

Mashimo Y., Mueller P., Pohl H., Beutel R.G. The “hairy beast”-Zorotypus hirsutus sp. n., an unusual new species of Zoraptera (Insecta) from Burmese amber. Zootaxa. 2018;4508:562–568. doi: 10.11646/zootaxa.4508.4.4. PubMed DOI

Mashimo Y., Mueller P., Beutel R.G. Zorotypus pecten, a new species of Zoraptera (Insecta) from mid-Cretaceous Burmese amber. Zootaxa. 2019;4651:565–577. doi: 10.11646/zootaxa.4651.3.9. PubMed DOI

Chen X., Su G. A new species of Zorotypus (Insecta, Zoraptera, Zorotypidae) and the earliest known suspicious mating behavior of Zorapterans from the mid-cretaceous amber of northern Myanmar. J. Zool. Syst. Evol. Res. 2019;57:555–560. doi: 10.1111/jzs.12283. DOI

Dallai R., Gottardo M., Mercati D., Machida R., Mashimo Y., Beutel R.G. Divergent mating patterns and a unique mode of external sperm transfer in Zoraptera: An enigmatic group of pterygote insects. Naturwissenschaften. 2013;100:581–594. doi: 10.1007/s00114-013-1055-0. PubMed DOI

Choe J.C. Sexual selection and mating system in Zorotypus gurneyi Choe (Insecta: Zoraptera): I. Dominance hierarchy and mating success. Behav. Ecol. Sociobiol. 1994;34:87–93. doi: 10.1007/BF00164179. DOI

Choe J.C. Courtship feeding and repeated mating in Zorotypus barberi (Insecta: Zoraptera) Anim. Behav. 1995;6:1511–1520. doi: 10.1016/0003-3472(95)90072-1. DOI

Choe J.C. The evolution of mating systems in the Zoraptera: Mating variations and sexual conflicts. In: Choe J.C., Crespi B.J., editors. The Evolution of Mating Systems in Insects and Arachnids. Cambridge University Press; Cambridge, UK: 1997. pp. 130–145. DOI

Shetlar D.J. Biological observations on Zorotypus hubbardi Caudell (Zoraptera) Entomol. News. 1978;89:217–223.

Hubbard M.D. A catalog of the order Zoraptera (Insecta) Insecta Mundi. 1990;4:49–66.

Riegel G.T. The distribution of Zorotypus hubbardi (Zoraptera) Ann. Entomol. Soc. Am. 1963;56:744–747. doi: 10.1093/aesa/56.6.744. DOI

Grimaldi D., Engel M.S. Evolution of the Insects. 1st ed. Cambridge University Press; Cambridge, UK: 2005. p. 755.

Curated global occurrence dataset of the insect order Zoraptera

Comparative cytogenetics of three Zoraptera species as a basis for understanding chromosomal evolution in Polyneoptera insects

Cryptic diversity in Zoraptera: Latinozoros barberi (Gurney, 1938) is a complex of at least three species (Zoraptera: Spiralizoridae)

An Immature Dermapteran Misidentified as an Adult Zorapteran: The Case of Formosozoros newi Chao & Chen, 2000