Ancient aposematic signals might have evolved under different ecological circumstances. Using European Cenozoic amber and phylogenetic reconstruction, we evaluated the evolution of net-winged beetle aposematism. We describe Priabonian Hiekeolycus winkleri sp. nov. from Baltic amber, review known fossil species, and suggest earlier high diversity and morphological conservativeness of European Lycidae since the Eocene. We hypothesize the presence of red and black/red aposematic patterns in Eocene Europe. The analyses suggest the Oligocene to Miocene dispersal of additional species from East Asia and their advergence to autochthonous patterns. Recently dispersed lycids have retained similarities with their East Asian relatives. Net-winged beetles are rare in Europe after the Quaternary climatic oscillations, and we hypothesize a currently relaxed selection for shared aposematic signals. Neophobia, and eventually inborn rejection of brightly colored prey, putatively preserved ancient aposematism under changing conditions. Evidence from paleontology and phylogenetics can provide insight into the long-term persistence of old adaptations under changing conditions.

1 I Schmalhausen Institute of Zoology Bogdan Khmelnitski Street15 01030 Kiev Ukraine

A A Borissiak Paleontological Institute RAS 123 Profsoyuznaya Street 117647 Moscow Russia

A N Severtsov Institute of Ecology and Evolution RAS 33 Leninsky Pr 119071 Moscow Russia

Biodiversity and Molecular Evolution Czech Advanced Technology Research Institute Slechtitelu 27 779 00 Olomouc Czech Republic

Hokkaido University Museum Hokkaido University Kita 10 Nishi 8 Kita ku Sapporo 060 0810 Japan

Insect Centre Donetskaya 13 326 109651 Moscow Russia

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Perkovsky E.E., Rasnitsyn A.P., Vlaskin A.P., Rasnitsyn S.P. Contribution to the study of the structure of amber forest communities based on analysis of syninclusions in the Rovno amber (late Eocene of Ukraine) Paleontol. J. 2012;46:293–301. doi: 10.1134/S0031030112030136. DOI

Kirejtshuk A.G., Azar D. Current knowledge of Coleoptera (Insecta) from the Lower Cretaceous Lebanese amber and taxonomical notes for some Mesozoic groups. Terr. Arthropod Rev. 2013;6:103–134. doi: 10.1163/18749836-06021061. DOI

Wang B., Rust J., Engel M.S., Szwedo J., Dutta S., Nel A., Fan Y., Meng F., Shi G., Jarzembowski E.A., et al. A diverse paleobiota in early Eocene fushun amber from China. Curr. Biol. 2014;24:1606–1610. doi: 10.1016/j.cub.2014.05.048. PubMed DOI

Alekseev V.I. Coleoptera from the middle-upper Eocene European ambers: generic composition, zoogeography and climatic implications. Zootaxa. 2017;4290:401–443. doi: 10.11646/zootaxa.4290.3.1. DOI

Su T., Spicer R.A., Wu F.X., Farnsworth A., Huang J., Del Rio C., Deng T., Ding L., Deng W.Y.D., Huang Y.J., et al. A Middle Eocene lowland humid subtropical "Shangri-La" ecosystem in central Tibet. Proc. Natl. Acad. Sci. USA. 2020;117:32989–32995. doi: 10.1073/pnas.2012647117. PubMed DOI PMC

Gao T., Shih C., Ren D. Behaviors and interactions of insects in mid-mesozoic ecosystems of northeastern China ann. Annu. Rev. Entomol. 2021;66:337–354. doi: 10.1146/annurev-ento-072720-095043. PubMed DOI

Speed M.P. Müllerian mimicry and the psychology of predation. Anim. Behav. 1993;45:571–580. doi: 10.1006/anbe.1993.1067. DOI

Speed M.P. Warning signals, receiver psychology and predator memory. Anim. Behav. 2000;60:269–278. doi: 10.1006/anbe.2000.1430. PubMed DOI

Lindström L., Alatalo R.V., Lyytinen A., Mappes J. Strong antiapostatic selection against novel rare aposematic prey. Proc. Natl. Acad. Sci. USA. 2001;98:9181–9184. doi: 10.1073/pnas.161071598. PubMed DOI PMC

Wilson J.S., Williams K.A., Forister M.L., von Dohlen C.D., Pitts J.P. Repeated evolution in overlapping mimicry rings among North American velvet ants. Nat. Commun. 2012;3:1272. doi: 10.1038/ncomms2275. PubMed DOI

Wilson J.S., Jahner J.P., Forister M.L., Sheehan E.S., Williams K.A., Pitts J.P. North American velvet ants form one of the world’s largest known Mullerian mimicry complexes. Curr. Biol. 2015;25:R704–R706. doi: 10.1016/j.cub.2015.06.053. PubMed DOI

Endler J.A., Mappes J. The current and future state of animal coloration research. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2017;372:20160352. doi: 10.1098/rstb.2016.0352. PubMed DOI PMC

Kunte K., Kizhakke A.G., Nawge V. Evolution of mimicry rings as a window into community dynamics. Annu. Rev. Ecol. Evol. Syst. 2021;52:315–341. doi: 10.1146/annurev-ecolsys-012021-024616. DOI

Paladini A., Takiya D.M., Urban J.M., Cryan J.R. New World spittlebugs (Hemiptera: cercopidae: Ischnorhininae): dated molecular phylogeny, classification, and evolution of aposematic coloration. Mol. Phylogenet. Evol. 2018;120:321–334. doi: 10.1016/j.ympev.2017.12.020. PubMed DOI

Motyka M., Kusy D., Masek M., Bocek M., Li Y., Bilkova R., Kapitán J., Yagi T., Bocak L. Conspicuousness, phylogenetic structure, and origins of Müllerian mimicry in 4000 lycid beetles from all zoogeographic regions. Sci. Rep. 2021;11:5961. doi: 10.1038/s41598-021-85567-x. PubMed DOI PMC

Martínez-Delclòs X., Briggs D.E., Peñalver E. Taphonomy of insects in carbonates and amber. Palaeogeogr. Palaeoclimatol. Palaeoecol. 2004;203:19–64. doi: 10.4202/app.00071.2014. DOI

Xu C., Luo C., Jarzembowski E.A., Fang Y., Wang B. Aposematic coloration from mid-cretaceous kachin amber. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2022;377:20210039. doi: 10.1098/rstb.2021.0039. PubMed DOI PMC

Sendi H., Azar D. New aposematic and presumably repellent bark cockroach from Lebanese amber. Cretac. Res. 2017;72:13–17. doi: 10.1016/j.cretres.2016.11.013. DOI

Vršanský P., Bechly G., Zhang Q., Jarzembowski E.A., Mlynský T., Šmídová L., Barna P., Kúdela M., Aristov D., Bigalk S., et al. Batesian insect-insect mimicry-related explosive radiation of ancient alienopterid cockroaches. Biologia. 2018;73:987–1006.

Xu C., Wang B., Fan L., Jarzembowski E.A., Fang Y., Wang H., Li T., Zhuo D., Ding M., Engel M.S. Widespread mimicry and camouflage among mid-Cretaceous insects. Gondwana Res. 2022;101:94–102. doi: 10.1016/j.gr.2021.07.025. DOI

Wappler T., Garrouste R., Engel M.S., Nel A. Wasp mimicry among Palaeocene reduviid bugs from Svalbard. Acta Palaeontol. Pol. 2013;58:883–887. doi: 10.4202/app.2011.0202. DOI

Tihelka E., Engel M.S., Huang D., Cai C. Mimicry in cretaceous bugs. iScience. 2020;23:101280. doi: 10.1016/j.isci.2020.101280. PubMed DOI PMC

Bocak L., Kundrata R., Fernández C.A., Vogler A.P. The discovery of Iberobaeniidae (Coleoptera: Elateroidea): a new family of beetles from Spain, with immatures detected by environmental DNA sequencing. Proc. Biol. Sci. 2016;283:20152350. doi: 10.1098/rspb.2015.2350. PubMed DOI PMC

Zhang S.Q., Che L.H., Li Y., Liang D., Pang H., Ślipiński A., Zhang P. Evolutionary history of Coleoptera revealed by extensive sampling of genes and species. Nat. Commun. 2018;9:205. doi: 10.1038/s41467-017-02644-4. PubMed DOI PMC

Kazantsev S.V. Phylogeny of the tribe Erotini (Coleoptera, Lycidae), with descriptions of new taxa. Zootaxa. 2004;496:1–48. doi: 10.11646/zootaxa.496.1. DOI

Masek M., Motyka M., Kusy D., Bocek M., Li Y., Bocak L. Molecular phylogeny, diversity and zoogeography of net-winged beetles (Coleoptera: Lycidae) Insects. 2018;9:154. doi: 10.3390/insects9040154. PubMed DOI PMC

Motyka M., Kusy D., Bilkova R., Bocak L. 2022. Neogene Climatic Fluctuations and Poor Connectivity with the Centres of Diversity Shaped the Western Palearctic Net-Winged Beetle Fauna.https://biorxiv.org/cgi/content/short/2022.09.08.507108v1

McKenna D.D., Shin S., Ahrens D., Balke M., Beza-Beza C., Clarke D.J., Donath A., Escalona H.E., Friedrich F., Letsch H., et al. The evolution and genomic basis of beetle diversity. Proc. Natl. Acad. Sci. USA. 2019;116:24729–24737. doi: 10.1073/pnas.1909655116. PubMed DOI PMC

Zherikhin V.V., Sukacheva I.D., Rasnitsyn A.P. Arthropods in contemporary and some fossil resins. Paleontol. J. 2009;43:987–1005. doi: 10.1134/S00310301090900. DOI

Aleksandrova G.N., Zaporozhets N.I. Palynological characteristics of upper cretaceous and paleogene deposits on the west of the sambian peninsula (Kaliningrad region), Part 1. Stratigr. Geol. Correl. 2008;16:295–316. doi: 10.1134/S0869593808030052. DOI

Iakovleva A.I. Detalization of Eocene dinocyst zonation for eastern peritethys. Bull. Mosc. Soc. Naturalists, Geol. Ser. 2017;92:32–48.

Winkler J.R. Three new genera of fossil Lycidae from baltic amber. Mitt. Münchn. Entomol. Ges. 1987;77:61–78.

Kazantsev S.V. A new fossil genus of net-winged beetles, with a brief review of amber Lycidae (Insecta: Coleoptera) Zootaxa. 2013;3608:94–100. doi: 10.11646/zootaxa.3608.1.8. PubMed DOI

Kazantsev S.V. New taxa of Baltic amber soldier beetles (Insecta: Coleoptera: cantharidae) with synonymic and taxonomic notes. Russ. Entomol. J. 2013;22:283–291.

Kazantsev S.V., Bocak L. Protolycus gedaniensis gen. n., sp. n., the first Baltic amber representative of Lycini (Coleoptera, Lycidae, Lycinae). Palaeoentomology 3, 327–332. 37. Kazantsev, S.V., and Bocak, L. (2022). New genus of erotine net-winged beetles, Damzenium gen. nov. (Coleoptera: Lycidae), from Eocene Rovno amber. Zootaxa. 2022;5154:583–589. doi: 10.11646/zootaxa.5154.5.6. PubMed DOI

Kusy D., Motyka M., Fusek L., Li Y., Bocek M., Bilkova R., Ruskova M., Bocak L. Sexually dimorphic characters and shared aposematic patterns mislead the morphology-based classification of the Lycini (Coleoptera: Lycidae) Zool. Zool. J. Linn. Soc. 2021;191:902–927. doi: 10.1093/zoolinnean/zlaa055. DOI

Kazantsev S.V., Bocak L. New genus of erotine net-winged beetles, Damzenium gen. nov. (Coleoptera: Lycidae), from Eocene Rovno amber. Zootaxa. 2022;5154:583–589. doi: 10.11646/zootaxa.5154.5.6. PubMed DOI

Kazantsev S.V., Perkovsky E.E. Imprint of a Helcophorus Fairmaire, 1881: the first net-winged beetle (Coleoptera: Lycidae) from Rovno amber. Zootaxa. 2022;5128:84–90. doi: 10.11646/ZOOTAXA.5128.1.4. PubMed DOI

Moore B.P., Brown W.V. Identification of warning odour components, bitter principles and antifeedants in an aposematic beetle: Metriorrhynchus rhipidius (Coleoptera: Lycidae). Ins. Insect Biochem. 1981;11:493–499. http://hdl.handle.net/102.100.100/293100?index=1

Eisner T., Schroeder F.C., Snyder N., Grant J.B., Aneshansley D.J., Utterback D., Meinwald J., Eisner M. Defensive chemistry of lycid beetles and of mimetic cerambycid beetles that feed on them. Chemoecology. 2008;18:109–119. doi: 10.1007/s00049-007-0398-4. PubMed DOI PMC

Linsley E.G., Eisner T., Klots A.B. Mimetic assemblages of sibling species of lycid beetles. Evolution. 1961;15:15–29. doi: 10.1111/j.1558-5646.1961.tb03126.x. DOI

Motyka M., Kampova L., Bocak L. Phylogeny and evolution of Müllerian mimicry in aposematic Dilophotes: evidence for advergence and size-constraints in evolution of mimetic sexual dimorphism. Sci. Rep. 2018;8:3744. doi: 10.1038/s41598-018-22155-6. PubMed DOI PMC

Motyka M., Bocek M., Kusy D., Bocak L. Interactions in multi-pattern Mullerian communities support origins of new patterns, false structures, imperfect resemblance and mimetic sexual dimorphism. Sci. Rep. 2020;10:11193. doi: 10.1038/s41598-020-68027-w. PubMed DOI PMC

Motyka M., Kusy D., Bocek M., Bilkova R., Bocak L. Phylogenomic and mitogenomic data can accelerate inventorying of tropical beetles during the current biodiversity crisis. Elife. 2021;10:71895. doi: 10.7554/eLife.71895. PubMed DOI PMC

Bocek M., Kusy D., Motyka M., Bocak L. Persistence of multiple patterns and intraspecific polymorphism in multi-species Müllerian communities of net-winged beetles. Front. Zool. 2019;16:38. doi: 10.1186/s12983-019-0335-8. PubMed DOI PMC

Bocak L., Yagi T. Evolution of mimicry patterns in metriorrhynchus (Coleoptera: Lycidae): the history of dispersal and speciation in south East Asia. Evolution. 2010;64:39–52. doi: 10.1111/j.1558-5646.2009.00812.x. PubMed DOI

Taylor C.H. Body size in Batesian mimicry. Evol. Ecol. 2022 doi: 10.1007/s10682-022-10204-6. DOI

Burke K.D., Williams J.W., Chandler M.A., Haywood A.M., Lunt D.J., Otto-Bliesner B.L. Pliocene and Eocene provide best analogs for near-future climates. Proc. Natl. Acad. Sci. USA. 2018;115:13288–13293. doi: 10.1073/pnas.1809600115. PubMed DOI PMC

Sherratt T.N. The evolution of Müllerian mimicry. Naturwissenschaften. 2008;95:681–695. doi: 10.1007/s00114-008-0403-y. PubMed DOI PMC

Chouteau M., Arias M., Joron M. Warning signals are under positive frequency-dependent selection in nature. Proc. Natl. Acad. Sci. USA. 2016;113:2164–2169. doi: 10.1073/pnas.1519216113. PubMed DOI PMC

Kazantsev S.V. New omethid and lampyrid taxa from the baltic amber (insecta: Coleoptera) Zootaxa. 2012;3186:59–63. doi: 10.5281/zenodo.280009. DOI

Kazantsev S.V. A new Luciolinae firefly (Coleoptera: lampyridae) from the Baltic amber. Russ. Entomol. J. 2012;21:319–320.

Kazantsev S. Retromalisus damzeni, gen. et sp. nov., a second Baltic amber taxon of the extinct family Berendtimiridae (Insecta: Coleoptera) J. Nat. Hist. 2020;54:1073–1080. doi: 10.1080/00222933.2020.1781949. DOI

Kazantsev S.V. New Baltic amber soldier beetles (Insecta: Coleoptera: cantharidae) with some taxonomic notes. Palaeoentomology. 2020;3:260–268. doi: 10.11646/palaeoentomology.3.3.7. DOI

Kleine R. Eine Lycidae aus dem Baltischen Bernstein. Entomol. Bl. 1940;36:179–180.

Svenning J.C. Deterministic Plio-Pleistocene extinctions in the European cool-temperate tree flora. Ecol. Lett. 2003;6:646–653. doi: 10.1046/j.1461-0248.2003.00477.x. DOI

Goldner A., Herold N., Huber M. Antarctic glaciation caused ocean circulation changes at the Eocene–Oligocene transition. Nature. 2014;511:574–577. doi: 10.1038/nature13597. PubMed DOI

Mitov P.G., Perkovsky E.E., Dunlop J.A. Harvestmen (arachnida: opiliones) in Eocene Rovno amber (Ukraine) Zootaxa. 2021;4984:43–72. doi: 10.11646/zootaxa.4984.1.6. PubMed DOI

Kvaček Z. Forest flora and vegetation of the European early Palaeogene - a review. Bull. Geosci. 2010;85:63–76. doi: 10.3140/bull.geosci.1146. DOI

Li Y., Gunter N., Pang H., Bocak L. DNA-based species delimitation separates highly divergent populations within morphologically coherent clades of poorly dispersing beetles. Zool. J. Linn. Soc. 2015;175:59–72. doi: 10.1111/zoj.12262. DOI

Sadowski E.-M., Schmidt A.R., Kunzmann L. The hyperdiverse conifer flora of the Baltic amber forest. palb. 2022;304:1–148. doi: 10.1127/palb/2022/0078. DOI

Perkovsky E.E., Rasnitsyn A.P., Vlaskin A.P., Taraschuk M.V. A comparative analysis of the Baltic and Rovno amber arthropod faunas: representative samples. Afr. Invertebr. 2007;48:229–245.

Yamamoto S. Fossil evidence of elytra reduction in ship-timber beetles. Sci. Rep. 2019;9:4938. doi: 10.1038/s41598-019-41310-1. PubMed DOI PMC

Robertson J.A., McHugh J.V., Whiting M.F. A molecular phylogenetic analysis of the pleasing fungus beetles (Coleoptera: erotylidae): evolution of colour patterns, gregariousness and mycophagy. Syst. Entomol. 2004;29:173–187. doi: 10.1111/j.0307-6970.2004.00242.x. DOI

Yang Y., Su J., Yang X.K. Description of six new species of Lycocerus Gorham (Coleoptera, Cantharidae), with taxonomic note and new distribution data of some other species. ZooKeys. 2014;456:85–107. doi: 10.3897/zookeys.456.8465. PubMed DOI PMC

Li Y., Pang H., Bocak L. Molecular phylogeny of Erotini with the description of a new genus from China (Coleoptera: Lycidae) Entomol. Sci. 2017;20:213–223. doi: 10.1111/ens.12245. DOI

Nakane T. Academic Press of Japan; 1969. Fauna Japonica. Lycidae (Insecta: Coleoptera)

Motyka M., Kusy D., Bilkova R., Bocak L. Analysis of the Holarctic Dictyoptera aurora complex (Coleoptera, Lycidae) reveals hidden diversity and geographic structure in Müllerian mimicry ring. Insects. 2022;13:817. doi: 10.3390/insects13090817. PubMed DOI PMC

Kirejtshuk A.G., Kovalev A.V. First fossil representative of the family Omalisidae (Coleoptera, Elateroidea sensu lato) from the Baltic Amber. Paleontol. J. 2015;49:1413–1416. doi: 10.1134/S0031030115130031. DOI

Fanti F., Vitali F. Key to fossil Malthininae, with description of two new species in Baltic amber (Coleoptera Cantharidae) Balt. J. Coleopterol. 2017;17:19–27.

Parisi F., Fanti F. A new fossil species of the extinct tribe Mimoplatycini Kazantsev, 2013 (Coleoptera Cantharidae) Annales de Paléontologie. 2019;105:119–122. doi: 10.1016/j.annpal.2019.04.002. DOI

Lindström L., Alatalo R.V., Mappes J. Imperfect Batesian mimicry – the effects of the frequency and the distastefulness of the model. Proc. R. Soc. Lond. B. 1997;264:149–153. doi: 10.1098/rspb.1997.0022. DOI

Borer M., Van Noort T., Rahier M., Naisbit R.E. Positive frequency-dependent selection on warning color in alpine leaf beetles. Evolution. 2010;64:3629–3633. doi: 10.1111/j.1558-5646.2010.01137.x. PubMed DOI

Marples N.M., Kelly D.J., Thomas R.J. Perspective: the evolution of warning coloration is not paradoxical. Evolution. 2005;59:933–940. doi: 10.1111/j.0014-3820.2005.tb01032.x. PubMed DOI

Ruxton G.D., Allen W.L., Sherratt M.P. Oxford University Press; 2018. Avoiding Attack: The Evolutionary Ecology of Crypsis, Aposematism, and Mimicry.

Holz C., Streil G., Dettner K., Dütemeyer J., Boland W. Intersexual transfer of a toxic terpenoid during copulation and its paternal allocation to developmental stages: quantification of cantharidin in cantharidin-producing oedemerids (Coleoptera: oedemeridae) and canthariphilous pyrochroids (Coleoptera: pyrochroidae) Z. Naturforsch. 1994;49:856–864. doi: 10.1515/znc-1994-11-1222. DOI

Eisner T., Smedley S.R., Young D.K., Eisner M., Roach B., Meinwald J. Chemical basis of courtship in a beetle (Neopyrochroa flabellata): cantharidin as precopulatory "enticing" agent. Proc. Natl. Acad. Sci. USA. 1996;93:6494–6498. doi: 10.1073/pnas.93.13.6494. PubMed DOI PMC

Marples N.M., Roper T.J. Effects of novel colour and smell on the response of naive chicks towards food and water. Anim. Behav. 1996;51:1417–1424. doi: 10.1006/anbe.1996.0145. DOI

Marples N.M., Kelly D.J. Neophobia and dietary conservatism: two distinct processes. Evol. Ecol. 1999;13:641–653. doi: 10.1023/A:1011077731153. DOI

Briolat E.S., Burdfield-Steel E.R., Paul S.C., Rönkä K.H., Seymoure B.M., Stankowich T., Stuckert A.M.M. Diversity in warning coloration: selective paradox or the norm? Biol. Rev. Camb. Philos. Soc. 2019;94:388–414. doi: 10.1111/brv.12460. PubMed DOI PMC

Bininda-Emonds O.R.P. transAlign: using amino acids to facilitate the multiple alignment of protein coding DNA sequences. BMC Bioinf. 2005;6:156. doi: 10.1186/1471-2105-6-156. PubMed DOI PMC

Katoh K., Standley D.M. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol. Biol. Evol. 2013;30:772–780. doi: 10.1093/molbev/mst010. PubMed DOI PMC

Kalyaanamoorthy S., Minh B.Q., Wong T.K.F., von Haeseler A., Jermiin L.S. ModelFinder: fast model selection for accurate phylogenetic estimates. Nat. Methods. 2017;14:587–589. doi: 10.1038/nmeth.4285. PubMed DOI PMC

Minh B.Q., Schmidt H.A., Chernomor O., Schrempf D., Woodhams M.D., Von Haeseler A., Lanfear R. IQ-TREE 2: new models and efficient methods for phylogenetic inference in the genomic era. Mol. Biol. Evol. 2020;37:1530–1534. doi: 10.1093/molbev/msaa015. PubMed DOI PMC

Drummond A.J., Suchard M.A., Xie D., Rambaut A. Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol. Biol. Evol. 2012;29:1969–1973. doi: 10.1093/molbev/mss075. PubMed DOI PMC

Kusy D., Motyka M., Bocek M., Masek M., Bocak L. Phylogenomic analysis resolves the relationships among net-winged beetles (Coleoptera: Lycidae) and reveals the parallel evolution of morphological traits. Syst. Entomol. 2019;44:911–925. doi: 10.1111/syen.12363. DOI

Hoang D.T., Chernomor O., von Haeseler A., Minh B.Q., Vinh L.S. UFBoot2: improving the ultrafast bootstrap approximation. Mol. Biol. Evol. 2018;35:518–522. doi: 10.1093/molbev/msx281. PubMed DOI PMC

Kazantsev S.V. Morphology of Lycidae with some considerations on evolution of the Coleoptera. Elytron. 2005;19:49–226.

Goloboff P.A., Catalano S.A. TNT version 1.5, including a full implementation of phylogenetic morphometrics. Cladistics. 2016;32:221–238. doi: 10.1111/cla.12160. PubMed DOI