Neoteny, the maintenance of larval features in sexually mature adults, is a radical way of generating evolutionary novelty through shifts in relative timing of developmental programmes. While controlled by the environment in facultative neotenics, retention of larval features is obligatory in many species of Lycidae (net-winged beetles). They are studied here as an example of how developmental shifts and ecology interact to produce macroevolutionary impacts. We conducted a phylogenetic analysis of Lycidae based on DNA sequences from nuclear (18S and 28S rRNA) and mitochondrial (rrnL, cox1, cob and nad5) genes from a representative set of lineages (73 species), including 17 neotenic taxa. Major changes of basal relationships compared with those implied in the current classification generally supported three independent origins of neotenics in Lycidae. The southeast Asian Lyropaeinae and Ateliinae were in basal positions indicating evolutionary antiquity, also confirmed by molecular clock estimates, unlike the neotropical leptolycines nested within Calopterini and presumably much younger. neotenics exhibit typical K-selected traits including slow development, large body size, high investment in offspring and low dispersal. This correlated with low species richness and restricted ranges of neotenic lineages compared with their sisters. Yet, these factors did not impede the evolutionary persistence of affected lineages, even without reversals to fully metamorphosed forms, contradicting earlier suggestions of recent evolution from dispersive non-neotenics.

Department of Zoology Faculty of Science Palacky University Trída Svobody 26 Olomouc Czech Republic

Zobrazit více v PubMed

Alberch P. Ontogenesis and morphological diversification. Am. Zool. 1980;20:653–667. doi:10.1093/icb/20.4.653 DOI

Arthur W. The effect of development on the direction of evolution: toward a twenty-first century consensus. Evol. Dev. 2004;6:282–288. doi:10.1111/j.1525-142X.2004.04033.x PubMed DOI

Baker R.H, DeSalle R. Multiple sources of molecular characteristics and the phylogeny of Hawaiian drosophilids. Syst. Biol. 1997;46:654–673. doi:10.2307/2413499 PubMed DOI

Beutel R.G, Bocak L, Bocakova M. Are Polyphaga (Coleoptera) really a basal neopteran lineage: a reply to Kazantsev. Acta Zool. 2007;88:153–158. doi:10.1111/j.1463-6395.2007.00266.x DOI

Bocak L. Review of the genus Scarelus Waterhouse from Sumatra and Malaysia (Coleoptera: Lycidae) Stuttg. Beitr. Naturk., Serie A (Biologie) 1995;535:1–10.

Bocak L. Pendola, a new lycid genus (Coleoptera, Lycidae) from Australian region. Biologia. 2001;57:557–561.

Bocak L, Bocakova M. Revision of the genus Dexoris C. O. Waterhouse (Coleoptera: Lycidae) Acta Entomol. Bohemoslov. 1988;85:194–204.

Bocak L, Bocakova M. New tribe Lyropaeini, with a description of a new species of Lyropaeus (Coleoptera, Lycidae) Polskie Pismo Entomol. 1989;58:717–723.

Bocak L, Bocakova M. Revision of the supergeneric classification of the family Lycidae (Coleoptera) Polskie Pismo Entomol. 1990;59:623–676.

Bocak L, Matsuda K. Review of immature stages of the family Lycidae (Insecta: Coleoptera) J. Nat. Hist. 2003;37:1463–1507. doi:10.1080/00222930210125362 DOI

Bocakova M. Phylogeny and classification of the tribe Calopterini (Coleoptera, Lycidae) Insect Syst. Evol. 2005;35:437–447.

Bocakova M. Review of the tribe Lyropaeini (Coleoptera: Lycidae) Eur. J. Entomol. 2006;103:127–136.

Bocakova M, Bocak L. New Lycidae from Peninsular Malaysia. Entomol. Basilensia. 1999;21:105–109.

Bocakova M, Bocak L, Hunt T, Teraväinen M, Vogler A.P. Molecular phylogenetics of Elateriformia (Coleoptera): evolution of bioluminescence and neoteny. Cladistics. 2007;23:477–496. doi:10.1111/j.1096-0031.2007.00164.x DOI

Bonett R.M, Chippindale P.T. Streambed microstructure predicts evolution of development and life history in the plethodontid salamander Eurycea tynerensis. BMC Biol. 2006;4:6. doi:10.1186/1741-7007-4-6 PubMed DOI PMC

Cicero J.M. Ontophylogenetics of cantharoid larviforms (Coleoptera: Cantharoidea) Coleopt. Bull. 1988;42:105–151.

Crowson R.A. A review of the classification of Cantharoidea (Coleoptera), with the definition of two new families: Cneoglossidae and Omethidae. Rev. Univ. Madrid. 1972;21:35–71.

Crowson R.A. Academic Press; London, UK: 1981. The biology of Coleoptera.

Davies T.J, Barraclough T.G, Chase M.W, Soltis S.P, Soltis D.E, Savolainen V. Darwin's abominable mystery: insights from a supertree of the angiosperms. Proc. Natl Acad. Sci. USA. 2004;101:1904–1909. doi:10.1073/pnas.0308127100 PubMed DOI PMC

De Cock R, Matthysen E. Glow-worm larvae bioluminiscence (Coleoptera: Lampyridae) operates as an aposematic signal upon toads (Bufo bufo) Behav. Ecol. 2003;14:103–108. doi:10.1093/beheco/14.1.103 DOI

Denoel M, Hervant F, Schabetsberger R, Joly P. Short- and long term advantages of an alternative ontogenetic pathway. Biol. J. Linn. Soc. 2002;77:105–112. doi:10.1046/j.1095-8312.2002.00095.x DOI

Giannini N.P, Simmons N.B. A phylogeny of megachiropteran bats (Mammalia: Chiroptera: Pteropodidae) based on the direct optimization analysis of one nuclear and four mitochondrial genes. Cladistics. 2003;19:496–511. doi:10.1111/j.1096-0031.2003.tb00385.x PubMed DOI

Goloboff P.A. Analyzing large data sets in reasonable times: solutions for composite optima. Cladistics. 1999;15:415–428. doi:10.1111/j.1096-0031.1999.tb00278.x PubMed DOI

Gould S.J. Harvard University Press; Cambridge, MA: 1977. Ontogeny and phylogeny.

Gravely F.H. The larvae and pupae of some beetles from Cochin. Rec. Ind. Mus. 1915;11:353–366.

Heaney L.R. A synopsis of climatic and vegetational change in southeast Asia. Clim. Change. 1991;19:53–61. doi:10.1007/BF00142213 DOI

Higgins D.G, Thompson J.D, Gibson T.J. Using Clustal for multiple sequence alignments. Methods Enzymol. 1996;266:383–402. PubMed

Hunt T, et al. A comprehensive phylogeny of beetles reveals the evolutionary origins of a superradiation. Science. 2007;318:1913–1916. doi:10.1126/science.1146954 PubMed DOI

Jablonski D. Micro- and macroevolution: scale and hierarchy in evolutionary biology and paleobiology. Paleobiology. 2000;26(Suppl.):15–52. doi:10.1666/0094-8373(2000)26[15:MAMSAH]2.0.CO;2 DOI

Jablonski D, Roy K. Geographical range and speciation in fossil and living molluscs. Proc. R. Soc. B. 2003;270:401–406. doi:10.1098/rspb.2002.2243 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

Kazantsev S.V. Alyculus, new genus, first brachypterous male lycid (Insecta: Coleoptera) Raffles Bull. Zool. 1999;47:251–255.

Kazantsev S.V. A generic review of Duliticolinae, new subfamily (Coleoptera, Lycidae) Elytron. 2002;16:5–21.

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

Lawrence, J. F. 1982 Coleoptera. In Synopsis and classification of living organisms, vol. 2 (ed. S. P. Parker), pp. 482–553. New York, NY: McGraw-Hill.

Linsley E.G, Eisner T, Klots A.B. Mimetic assemblages of sibling species of lycid beetles. Evolution. 1961;15:15–29. doi:10.2307/2405840 DOI

Mickevich M.F, Farris J.S. The implications of congruence in Menidia. Syst. Zool. 1981;30:351–370. doi:10.2307/2413255 DOI

Miller, R. S. 1991 A revision of the Leptolycini (Coleoptera: Lycidae) with a discussion of paedomorphosis. Dissertation, The Ohio State University, Columbus.

Mjöberg E. The mystery of the so called “trilobite larvae” or “Perty's larvae” definitely solved. Psyche. 1925;32:119–157.

Moore B.P, Brown W.V. Identification of warning odour components, bitter principles and antifeedants in an aposematic beetle: Metriorrhynchus rhipidium (Coleoptera: Lycidae) Insect Biochem. 1981;15:493–499. doi:10.1016/0020-1790(81)90016-0 DOI

Nijhout H.F. Princenton University Press; Princeton, NJ: 1994. Insect hormones.

Posada D, Crandall K.A. Modeltest: testing the model of DNA substitution. Bioinformatics. 1998;14:817–818. doi:10.1093/bioinformatics/14.9.817 PubMed DOI

Ray N, Adams J.M. A GIS-based vegetation map of the world at the Last Glacial Maximum (25,000–15,000 BP) Internet Archaeol. 2001;11:2. http://intarch.ac.uk/journal/issue11/2/1.html

Roff D.A. The evolution of flightlessness: is history important? Evol. Ecol. 1994;8:639–657. doi:10.1007/BF01237847 DOI

Sanderson M.J. Estimation absolute rates of molecular evolution and divergence times: a penalized likelihood approach. Mol. Biol. Evol. 2002;19:101–109. PubMed

Shimodaira H, Hasegawa M. Multiple comparisons of log-likelihoods with applications to phylogenetic inference. Mol. Biol. Evol. 1999;16:1114–1116.

Shull V.L, Vogler A.P, Baker M.D, Maddison D.R, Hammond P.M. Sequence alignment of 18S ribosomal RNA and the basal relationships of adephagan beetles: evidence for monophyly of aquatic families and the placement of Trachypachidae. Syst. Biol. 2001;50:945–969. doi:10.1080/106351501753462894 PubMed DOI

Slowinski J.B, Guyer C. Testing whether certain traits have caused amplified diversification: an improved method based on a model of random speciation and extinction. Am. Nat. 1993;142:1019–1024. doi:10.1086/285586 PubMed DOI

Sorenson, M. D. 1999 TreeRotversion v. 2.0. Boston, MA: Boston University.

Swofford, D. L. 2002 PAUP*: phylogenetic analysis using parsimony v. 4.0b10. Sunderland, MA: Sinauer.

Tallis J.H. Chapman and Hall; New York, NY: 1991. Plant community history: long-term changes in plant distribution and diversity.

Vogler A.P, De Salle R, Assmann T, Knisley C.B, Schultz T.D. Molecular population genetics of the endangered tiger beetle, Cicindela dorsalis (Coleoptera: Cicindelidae) Ann. Entomol. Soc. Am. 1993;86:142–152.

Wagner D.L, Liebherr J.K. Flightlessness in insects. Trends Ecol. Evol. 1992;7:216–220. doi:10.1016/0169-5347(92)90047-F PubMed DOI

Wheeler W.C. Sequence alignment, parameter sensitivity, and the phylogenetic analysis of molecular data. Syst. Biol. 1995;44:321–331. doi:10.2307/2413595 DOI

Wheeler W.C. Optimization alignment: the end of multiple sequence alignment in phylogenetics? Cladistics. 1996;12:1–9. doi:10.1111/j.1096-0031.1996.tb00189.x DOI

Wheeler, W. C., Gladstein, D. S. & De Laet, J. 2002 Poy, v. 3.0.11. See ftp.amnh.org/pub/molecular/poy

Wong A.T.C. A new species of neotenous beetle, Duliticola hoiseni (Insecta: Coleoptera: Cantharoidea: Lycidae) from Peninsular Malaysia and Singapore. Raffles Bull. Zool. 1996;44:173–187.

Wong, A. T. C. 1998 A revision of the neotenous ‘trilobite larvae’ of the genera Duliticola and Platerodrilus (Coleoptera: Cantharoidea: Lycidae). MSc thesis, National University of Singapore, Republic of Singapore.

Phylogenetic analysis reveals a new net-winged beetle genus of Eurrhacini (Coleoptera, Lycidae) from the Pacific slopes of Central America and Ecuador

Rhagophthalmidae Olivier, 1907 (Coleoptera, Elateroidea): described genera and species, current problems, and prospects for the bioluminescent and paedomorphic beetle lineage

Dominican amber net-winged beetles suggest stable paleoenvironment as a driver for conserved morphology in a paedomorphic lineage

Phylogenomic and mitogenomic data can accelerate inventorying of tropical beetles during the current biodiversity crisis

An unusual elateroid lineage from mid-Cretaceous Burmese amber (Coleoptera: Elateroidea)

Hide-and-Seek with Tiny Neotenic Beetles in One of the Hottest Biodiversity Hotspots: Towards an Understanding of the Real Diversity of Jurasaidae (Coleoptera: Elateroidea) in the Brazilian Atlantic Forest

Conspicuousness, phylogenetic structure, and origins of Müllerian mimicry in 4000 lycid beetles from all zoogeographic regions

Cretophengodidae, a new Cretaceous beetle family, sheds light on the evolution of bioluminescence

Biodiversity Inventory and Distribution of Metriorrhynchina Net-Winged Beetles (Coleoptera: Lycidae), with the Identification of Generic Ranges

Hidden diversity in the Brazilian Atlantic rainforest: the discovery of Jurasaidae, a new beetle family (Coleoptera, Elateroidea) with neotenic females

Where did the pupa come from? The timing of juvenile hormone signalling supports homology between stages of hemimetabolous and holometabolous insects

Genome sequences identify three families of Coleoptera as morphologically derived click beetles (Elateridae)

Molecular Phylogeny, Diversity and Zoogeography of Net-Winged Beetles (Coleoptera: Lycidae)

Incomplete sclerotization and phylogeny: The phylogenetic classification of Plastocerus (Coleoptera: Elateroidea)

Phylogeny and evolution of Müllerian mimicry in aposematic Dilophotes: evidence for advergence and size-constraints in evolution of mimetic sexual dimorphism

The comparison of molecular and morphology-based phylogenies of trichaline net-winged beetles (Coleoptera: Lycidae: Metriorrhynchini) with description of a new subgenus

Slowly dispersing neotenic beetles can speciate on a penny coin and generate space-limited diversity in the tropical mountains

The discovery of Iberobaeniidae (Coleoptera: Elateroidea): a new family of beetles from Spain, with immatures detected by environmental DNA sequencing

The taxonomy and diversity of Platerodrilus (Coleoptera, Lycidae) inferred from molecular data and morphology of adults and larvae

Molecular phylogeny reveals high diversity, geographic structure and limited ranges in neotenic net-winged beetles platerodrilus (coleoptera: lycidae)