Reinventing the leaf: multiple origins of leaf-like wings in katydids (Orthoptera : Tettigoniidae)
Joseph Mugleston A C , Michael Naegle A , Hojun Song B , Seth M. Bybee A , Spencer Ingley A , Anton Suvorov A and Michael F. Whiting AA Department of Biology and M.L. Bean Life Science Museum, Brigham Young University, 4102 Life Science Building, Provo, UT 84602, USA.
B Department of Entomology, Texas A&M University, 2475 TAMU, College Station, TX 77843-2475, USA.
C Corresponding author. Email: joseph.mugleston@gmail.com
Invertebrate Systematics 30(4) 335-352 https://doi.org/10.1071/IS15055
Submitted: 4 December 2015 Accepted: 5 March 2016 Published: 31 August 2016
Abstract
Insects have developed incredible means to avoid detection by predators. At least five insect orders have species that resemble leaves. Katydids (Orthoptera : Tettigoniidae) are the most diverse and wide-ranging of the leaf-like insects. At least 14 of the 20 extant katydid subfamilies contain species with leaf-like wings. Although it is undisputed that many katydids resemble leaves, methods for delineating the leaf-like from non-leaf-like forms have varied by author and in many cases are not explicitly stated. We provide a simple ratio method that can be used to differentiate the leaf-like and non-leaf-like forms. Geometric morphometrics were used to validate the ratio method. Leaf-like wings have been independently derived in at least 15 katydid lineages. Relative rates of speciation were found to be greater in the non-leaf-like forms, suggesting that leaf-like wings within Tettigoniidae are not a driver of diversification. Likewise, throughout Tettigoniidae, selection seems to be favouring the transition away from leaf-like wings. However, within the large Phaneropterinae subclade, relative speciation and transition rates between the leaf-like and non-leaf-like forms do not differ significantly.
References
Belwood, J. J. (1993). Anti-predator defences and ecology of neotropical forest katydids, especially the Pseudophyllinae. In ‘The Tettigoniidae: Biology, Systematics, and Evolution’. (Eds W. J. Bailey and D. C. F. Rentz.) pp. 8–26. (Springer-Verlag: New York.)Castner, J. L. (1995). Defensive behavior and display of the leaf-mimicking katydid Pterochroza ocellata (L.) (Orthoptera: Tettigoniidae: Pseudophyllinae: Pterochrozini). Journal of Orthoptera Research 4, 89–92.
| Defensive behavior and display of the leaf-mimicking katydid Pterochroza ocellata (L.) (Orthoptera: Tettigoniidae: Pseudophyllinae: Pterochrozini).Crossref | GoogleScholarGoogle Scholar |
Castner, J. L., and Nickle, D. A. (1995a). Notes on the biology and ecology of the leaf-mimicking katydid Typophyllum bolivari Vignon (Orthoptera: Tettigoniidae: Pseudophyllinae: Pterochrozini). Journal of Orthoptera Research 4, 105–109.
| Notes on the biology and ecology of the leaf-mimicking katydid Typophyllum bolivari Vignon (Orthoptera: Tettigoniidae: Pseudophyllinae: Pterochrozini).Crossref | GoogleScholarGoogle Scholar |
Castner, J. L., and Nickle, D. A. (1995b). Observations on the behavior and biology of leaf-mimicking katydids (Orthoptera: Tettigoniidae: Pseudophyllinae: Pterochrozini). Journal of Orthoptera Research 4, 93–97.
| Observations on the behavior and biology of leaf-mimicking katydids (Orthoptera: Tettigoniidae: Pseudophyllinae: Pterochrozini).Crossref | GoogleScholarGoogle Scholar |
Colgan, D. J., McLauchlan, A., Wilson, G. D. F., Livingston, S. P., Edgecombe, G. D., Macaranas, J., Cassis, G., and Gray, M. R. (1998). Histone H3 and U2 snRNA DNA sequences and arthropod molecular evolution. Australian Journal of Zoology 46, 419–437.
| Histone H3 and U2 snRNA DNA sequences and arthropod molecular evolution.Crossref | GoogleScholarGoogle Scholar |
Conner, W. E. (2014). Adaptive sounds and silences: acoustic anti-predator strategies in insects. In ‘Insect Hearing and Acoustic Communication’. pp. 65–79. (Springer: New York City.)
Crespi, B., and Sandoval, C. (2000). Phylogenetic evidence for the evolution of ecological specialization in Timema walking-sticks. Journal of Evolutionary Biology 13, 249–262.
| Phylogenetic evidence for the evolution of ecological specialization in Timema walking-sticks.Crossref | GoogleScholarGoogle Scholar |
Drummond, A. J., Suchard, M. A., Xie, D., and Rambaut, A. (2012). Bayesian phylogenetics with BEAUti and the BEAST 1.7. Molecular Biology and Evolution 29, 1969–1973.
| 1:CAS:528:DC%2BC38XhtFagu7fO&md5=5ab730c939a1ffbe2d25920cbdfa4ea5CAS | 22367748PubMed |
Eades, D. C., Otte, D., Cigliano, M. M., and Braun, H. (2015). Orthoptera Species File Online. Version 5.0/5.0. Available at http://Orthoptera.SpeciesFile.org [Verified May 2016]
Edmunds, M. (1974). ‘Defence in Animals: a Survey of Anti-predator Defences.’ (Longman Publishing Group: Harlow, UK.)
Fabricant, S. A., and Herberstein, M. E. (2014). Hidden in plain orange: aposematic coloration is cryptic to a colorblind insect predator. Behavioral Ecology 26, 38–44.
FitzJohn, R. G. (2012). Diversitree: comparative phylogenetic analyses of diversification in R. Methods in Ecology and Evolution 3, 1084–1092.
Gwynne, D. T. (2001). ‘Katydids and Bush-Crickets.’ (Comstock Publishing Associates: Sacramento, CA.)
Hultgren, K., and Stachowicz, J. (2009). Evolution of decoration in majoid crabs: a comparative phylogenetic analysis of the role of body size and alternative defensive strategies. American Naturalist 173, 566–578.
| Evolution of decoration in majoid crabs: a comparative phylogenetic analysis of the role of body size and alternative defensive strategies.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1M3lsVekug%3D%3D&md5=f0d4853dea784179d54debd322d6f21eCAS | 19278336PubMed |
Johannesson, K., and Ekendahl, A. (2002). Selective predation favouring cryptic individuals of marine snails (Littorina). Biological Journal of the Linnean Society. Linnean Society of London 76, 137–144.
| Selective predation favouring cryptic individuals of marine snails (Littorina).Crossref | GoogleScholarGoogle Scholar |
Katoh, K., Kuma, K.-i., Toh, H., and Miyata, T. (2005). MAFFT version 5: improvement in accuracy of multiple sequence alignment. Nucleic Acids Research 33, 511–518.
| MAFFT version 5: improvement in accuracy of multiple sequence alignment.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtV2qsbc%3D&md5=7785a0400929a63365fb3915f7988733CAS | 15661851PubMed |
Kearse, M., Moir, R., Wilson, A., Stones-Havas, S., Cheung, M., Sturrock, S., Buxton, S., Cooper, A., Markowitz, S., and Duran, C. (2012). Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28, 1647–1649.
| Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data.Crossref | GoogleScholarGoogle Scholar | 22543367PubMed |
Kumar, S., Nei, M., Dudley, J., and Tamura, K. (2008). MEGA: a biologist-centric software for evolutionary analysis of DNA and protein sequences. Briefings in Bioinformatics 9, 299–306.
| MEGA: a biologist-centric software for evolutionary analysis of DNA and protein sequences.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXpt1artrg%3D&md5=302c29a194672196d3024da2bbca2d40CAS | 18417537PubMed |
Lanfear, R., Calcott, B., Ho, S. Y. W., and Guindon, S. (2012). PartitionFinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses. Molecular Biology and Evolution 29, 1695–1701.
| PartitionFinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xnt1ehsbg%3D&md5=f31991d546b9407c9c5b7aa3e900acc9CAS | 22319168PubMed |
Maddison, W. P., and Maddison, D. R. (2015). Mesquite: a modular system for evolutionary analysis. Version 3.04. Available at http://mesquiteproject.org [Verified June 2016]
Maddison, W. P., Midford, P. E., and Otto, S. P. (2007). Estimating a binary character’s effect on speciation and extinction. Systematic Biology 56, 701–710.
| Estimating a binary character’s effect on speciation and extinction.Crossref | GoogleScholarGoogle Scholar | 17849325PubMed |
Marshall, K. L., and Gluckman, T. L. (2015). The evolution of pattern camouflage strategies in waterfowl and game birds. Ecology and Evolution 5, 1981–1991.
| The evolution of pattern camouflage strategies in waterfowl and game birds.Crossref | GoogleScholarGoogle Scholar | 26045950PubMed |
Mugleston, J. D., Song, H., and Whiting, M. F. (2013). A century of paraphyly: a molecular phylogeny of katydids (Orthoptera: Tettigoniidae) supports multiple origins of leaf-like wings. Molecular Phylogenetics and Evolution 69, 1120–1134.
| A century of paraphyly: a molecular phylogeny of katydids (Orthoptera: Tettigoniidae) supports multiple origins of leaf-like wings.Crossref | GoogleScholarGoogle Scholar | 23891949PubMed |
Nentwig, W. (1985). A tropical caterpillar that mimics faeces, leaves and a snake (Lepidoptera: Oxytenidae: Oxytenis naemia). Journal of Research on the Lepidoptera 24, 136–141.
Nickle, D. A., and Castner, J. L. (1995). Strategies utilized by katydids (Orthoptera: Tettigoniidae) against diurnal predators in rainforests of northeastern Peru. Journal of Orthoptera Research 4, 75–88.
| Strategies utilized by katydids (Orthoptera: Tettigoniidae) against diurnal predators in rainforests of northeastern Peru.Crossref | GoogleScholarGoogle Scholar |
Pinheiro, C., and Freitas, A. (2014). Some possible cases of escape mimicry in neotropical butterflies. Neotropical Entomology 43, 393–398.
| Some possible cases of escape mimicry in neotropical butterflies.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC2s%2FhtVWqtw%3D%3D&md5=d03db8cefc2dc981336869a4ef59b0e9CAS | 27193948PubMed |
R Core Team (2013). R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available at http://www.R-project.org/ [Verified July 2015]
Ragge, D. R. (1955). ‘The Wing-Venation of the Orthoptera Saltatoria with Notes on Dictyopteran Wing-Venation.’ (British Museum: London.)
Rajabizadeh, M., Adriaens, D., Kaboli, M., Sarafraz, J., and Ahmadi, M. (2015). Dorsal colour pattern variation in Eurasian mountain vipers (genus Montivipera): a trade-off between thermoregulation and crypsis. Zoologischer Anzeiger 257, 1–9.
| Dorsal colour pattern variation in Eurasian mountain vipers (genus Montivipera): a trade-off between thermoregulation and crypsis.Crossref | GoogleScholarGoogle Scholar |
Rambaut, A., and Drummond, A. J. (2003). Tracer v1.3. Oxford, UK. Available at http://evolve.zoo.ox.ac.uk/ [Verified May 2016]
Robinson, M. H. (1969). The defensive behaviour of some orthopteroid insects from Panama. Transactions of the Royal Entomological Society of London 121, 281–303.
| The defensive behaviour of some orthopteroid insects from Panama.Crossref | GoogleScholarGoogle Scholar |
Rohlf, F. (2003). TpsRelw, relative warps analysis. 1.36 edn. Department of Ecology and Evolution, State University of New York at Stony Brook: Stony Brook, NY. Available at http://life.bio.sunysb.edu/morph/index.html [Verified June 2016].
Rohlf, F. (2005). TpsDig, digitize landmarks and outlines. 2.05 edn. Department of Ecology and Evolution, State University of New York at Stony Brook: Stony Brook, NY. Available at http://life.bio.sunysb.edu/morph/ [verified June 2016].
Rohlf, F. J., and Slice, D. (1990). Extensions of the procrustes method for the optimal superimposition of landmarks. Systematic Zoology 39, 40–59.
| Extensions of the procrustes method for the optimal superimposition of landmarks.Crossref | GoogleScholarGoogle Scholar |
Ruxton, G. D., Sherratt, T. N., and Speed, M. P. (2004). ‘Avoiding Attack: the Evolutionary Ecology of Crypsis, Warning Signals, and Mimicry.’ (Oxford University Press: Oxford, NY.)
Schmidt, J. O. (1990). ‘Insect Defenses: Adaptive Mechanisms and Strategies of Prey and Predators.’ (SUNY Press, Albany, NY.)
Skelhorn, J., Rowland, H. M., and Ruxton, G. D. (2010a). The evolution and ecology of masquerade. Biological Journal of the Linnean Society 99, 1–8.
Skelhorn, J., Rowland, H. M., Speed, M. P., and Ruxton, G. D. (2010b). Masquerade: camouflage without crypsis. Science 327, 51.
| Masquerade: camouflage without crypsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhs1WksrnE&md5=22835b328eaafce0c02aa30600bb8378CAS | 20044568PubMed |
Song, H., Amédégnato, C., Cigliano, M. M., Desutter‐Grandcolas, L., Heads, S. W., Huang, Y., Otte, D., and Whiting, M. F. (2015). 300 million years of diversification: elucidating the patterns of orthopteran evolution based on comprehensive taxon and gene sampling. Cladistics 31, 621–651.
| 300 million years of diversification: elucidating the patterns of orthopteran evolution based on comprehensive taxon and gene sampling.Crossref | GoogleScholarGoogle Scholar |
Stamatakis, A. (2006). RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22, 2688–2690.
| RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtFKlsbfI&md5=75f7f4dcbee031d89a4fac72e69aca2fCAS | 16928733PubMed |
Svanbäck, R., and Eklöv, P. (2011). Catch me if you can – predation affects divergence in a polyphenic species. Evolution 65, 3515–3526.
| Catch me if you can – predation affects divergence in a polyphenic species.Crossref | GoogleScholarGoogle Scholar | 22133222PubMed |
Svenson, G. J., and Whiting, M. F. (2004). Phylogeny of Mantodea based on molecular data: evolution of a charismatic predator. Systematic Entomology 29, 359–370.
| Phylogeny of Mantodea based on molecular data: evolution of a charismatic predator.Crossref | GoogleScholarGoogle Scholar |
Svenson, G. J., and Whiting, M. F. (2009). Reconstructing the origins of praying mantises (Dictyoptera, Mantodea): the roles of Gondwanan vicariance and morphological convergence. Cladistics 25, 468–514.
| Reconstructing the origins of praying mantises (Dictyoptera, Mantodea): the roles of Gondwanan vicariance and morphological convergence.Crossref | GoogleScholarGoogle Scholar |
Vane-Wright, R., and Boppre, M. (1993). Visual and chemical signalling in butterflies: functional and phylogenetic perspectives. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 340, 197–205.
| Visual and chemical signalling in butterflies: functional and phylogenetic perspectives.Crossref | GoogleScholarGoogle Scholar |
Whiting, M. F. (2002). Mecoptera is paraphyletic: multiple genes and phylogeny of Mecoptera and Siphonaptera. Zoologica Scripta 31, 93–104.
| Mecoptera is paraphyletic: multiple genes and phylogeny of Mecoptera and Siphonaptera.Crossref | GoogleScholarGoogle Scholar |
Wild, A. L., and Maddison, D. R. (2008). Evaluating nuclear protein-coding genes for phylogenetic utility in beetles. Molecular Phylogenetics and Evolution 48, 877–891.
| Evaluating nuclear protein-coding genes for phylogenetic utility in beetles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtVyntL3M&md5=d02ba20a6d532ecb7a5ea2ebf7a76fd2CAS | 18644735PubMed |
Zeuner, F. E. (1936). The subfamilies of Tettigoniidae (Orthoptera). Proceedings of the Royal Entomological Society of London. Series B, Taxonomy 5, 103–109.