Skip to main content Skip to main navigation menu Skip to site footer
Type: Article
Published: 2021-05-10
Page range: 101–118
Abstract views: 230
PDF downloaded: 14

Molecular phylogeny of the grasshopper family Pyrgomorphidae (Caelifera, Orthoptera) reveals rampant paraphyly and convergence of traditionally used taxonomic characters

Department of Zoology, Hazara University, Mansehra, Pakistan Department of Entomology, Texas A&M University, College Station, TX, USA
Department of Entomology, Texas A&M University, College Station, TX, USA Department of Ecology & Evolutionary Biology, University of Michigan, Ann Arbor, MI, USA
Department of Entomology, Texas A&M University, College Station, TX, USA
Orthoptera paraphyly convergence male genitalia mitochondrial genome

Abstract

The grasshopper family Pyrgomorphidae is one of the most colorful orthopteran lineages, and includes biologically fascinating and culturally important species. Recent attempts to reconstruct the phylogeny of this family have resulted in a large degree of conflicts between a morphology-based study and a molecular-based study, mainly due to convergent morphological traits that affected phylogenetic reconstruction. In this study, a molecular phylogeny of Pyrgomorphidae based on 32 ingroup species and mitochondrial genome data is proposed, which is used to test the monophyly of the taxonomic groupings used in the current classification scheme. Using the ancestral character state reconstruction analyses and character mapping, we demonstrate that some of the morphological characters, including the male genitalia, which were considered to be taxonomically important, have evolved convergently across the phylogeny. We discuss the discrepancies between our phylogeny and the previous studies and propose an approach to establish a natural classification scheme for Pyrgomorphidae.

 

References

  1. Arnqvist, G. (1997) The evolution of animal genitalia: distinguishing between hypotheses by single species studies. Biological Journal of the Linnean Society, 60, 365–379.

    https://doi.org/10.1111/j.1095-8312.1997.tb01501.x

    Bradler, S., Robertson, J.A. & Whiting, M.F. (2014) A molecular phylogeny of Phasmatodea with emphasis on Necrosciinae, the most species‐rich subfamily of stick insects. Systematic Entomology, 39, 205–222.

    https://doi.org/10.1111/syen.12055

    Cerritos, R. & Cano-Santana, Z. (2008) Harvesting grasshoppers Sphenarium purpurascens in Mexico for human consumption: A comparison with insecticidal control for managing pest outbreaks. Crop Protection, 27, 473–480.

    https://doi.org/10.1016/j.cropro.2007.08.001

    Chintauan-Marquier, I.C., Legendre, F., Hugel, S., Robillard, T., Grandcolas, P., Nel, A., Zuccon, D. & Desutter-Grandcolas, L. (2016) Laying the foundations of evolutionary and systematic studies in crickets (Insecta, Orthoptera): a multilocus phylogenetic analysis. Cladistics, 32, 54–81.

    https://doi.org/10.1111/cla.12114

    Cigliano, M.M., Braun, H., Eades, D.C. & Otte, D. (2021) Orthoptera Species File. Version 5.0/5.0. Available from: http://Orthoptera.SpeciesFile.org (accessed 23 March 2021)

    COPR (1982) The locust and grasshopper agricultural manual. London: Centre for Overseas Pest Research.

    Dirsh, V.M. (1961) A preliminary revision of the families and subfamilies of Acridoidea (Orthoptera, Insecta). Bulletin of the British Museum (Natural History) Entomology, 10, 351–419.

    https://doi.org/10.5962/bhl.part.16264

    Eades, D.C. (2000) Evolutionary relationships of phallic structures of Acridomorpha (Orthoptera). Journal of Orthoptera Research, 9, 181–210.

    https://doi.org/10.2307/3503648

    Eberhard, W.G. (1985) Sexual selection and animal genitalia. Harvard University Press, Cambridge, Massachusetts, 244 pp.

    https://doi.org/10.4159/harvard.9780674330702

    Edgar, R.C. (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research, 32, 1792–1797.

    https://doi.org/10.1093/nar/gkh340

    Fenn, J.D., Song, H., Cameron, S.L. & Whiting, M.F. (2008) A mitochondrial genome phylogeny of Orthoptera (Insecta) and approaches to maximizing phylogenetic signal found within mitochondrial genome data. Molecular Phylogenetics and Evolution, 49, 59–68.

    https://doi.org/10.1016/j.ympev.2008.07.004

    Flook, P.K., Klee, S. & Rowell, C.H.F. (1999) Combined molecular phylogenetic analysis of the Orthoptera (Arthropoda, Insecta) and implications for their higher systematics. Systematic Biology, 48, 233–253.

    https://doi.org/10.1080/106351599260274

    Flook, P.K., Klee, S. & Rowell, C.H.F. (2000) Molecular phylogenetic analysis of the Pneumoroidea (Orthoptera, Caelifera): Molecular data resolve morphological character conflicts in the basal Acridomorpha. Molecular Phylogenetics and Evolution, 15, 345–354.

    https://doi.org/10.1006/mpev.1999.0759

    Flook, P.K. & Rowell, C.H.F. (1997) The phylogeny of the Caelifera (Insecta, Orthoptera) as deduced from mtrRNA gene sequences. Molecular Phylogenetics and Evolution, 8, 89–103.

    https://doi.org/10.1006/mpev.1997.0412

    Hosken, D.J. & Stockley, P. (2004) Sexual selection and genital evolution. Trends in Ecology & Evolution, 19, 87–93.

    https://doi.org/10.1016/j.tree.2003.11.012

    Katoh, K. & Standley, D.M. (2013) MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability. Molecular Biology and Evolution, 30, 772–780.

    https://doi.org/10.1093/molbev/mst010

    Kevan, D.K.M. (1952a) On the systematic position of two anomalous genera previously placed in the subfamily Pyrgomorphinae (Orth., Acrididae). The Entomologist’s Monthly Magazine, 88, 265–272.

    Kevan, D.K.M. (1952b) A study of the genus Chrotogonus Audinet-Serville, 1839 (Orthop., Acrid., Pyrgomorphinae) I. The subgenera Obbiacris, nov. and Shoacris, nov. Mitteilungen der Schweizerischen Entomologischen Gesellschaft, 25, 87–96.

    Kevan, D.K.M. (1963) A preliminary revision of the genera Mitricephala Bolivar 1898, and Verdulia Bolivar 1905 (Orthoptera: Acridoidea: Pyrgomorphidae). Pacific Insects, 5, 771–795.

    Kevan, D.K.M. (1966a) The Pyrgomorphidae of South America (Orthoptera: Acridoidea). Transactions of the American Entomological Society, 92, 557–584.

    Kevan, D.K.M. (1966b) The tribe Nereniini: with additions to the Pyrgomorphidae (Orthoptera: Acridoidea) from the South Pacific. Pacific Insects, 8, 695–758.

    Kevan, D.K.M. (1968a) Further observations on Sagittacridini, Gymnohippini and Geloiini. Eos, 153, 575–589.

    Kevan, D.K.M. (1968b) A revision of the Pseudomorphacridini (Orthoptera: Acridoidea: Pyrgomorphidae). Oriental Insects, 2, 141–154.

    https://doi.org/10.1080/00305316.1968.10433878

    Kevan, D.K.M. (1968c) A study of the genus Chrotogonus Audinet-Serville, 1838 (Orthoptera: Acridoidea: Pyrgomorphidae) IX. The phallic structures, with a second supplement to the bibliography of the Chrotogonini. The Entomologist’s Monthly Magazine, 104, 10–22.

    https://doi.org/10.4039/Ent100152-2

    Kevan, D.K.M. (1969) A preliminary revision of the Asiatic Chlorizeinini (Orthoptera: Acridoidea: Pyrgomorphidae). Transactions of the American Entomological Society, 94, 355–378.

    Kevan, D.K.M. (1970) A revision of the Desmopterini (Orthoptera: Acridoidea: Pyrgomorphidae) Part II. Desmopterella Ramme, 1941. Pacific Insects, 12, 543–627.

    Kevan, D.K.M. (1982) A new genus and species of Pyrgormorphidae-Pyrgomorphini (Orthoptera, Acridoidea) from northeastern Africa. Annales Entomologicae Fennicae, 48, 89–96.

    Kevan, D.K.M. (1990) Revision of the Mexican Pyrgomorphidae (Orthoptera: Acridoidea) II. A reappraisal of the genus Ichthiacris I. Bolivar, 1905, with descriptions of three new species from Baja California, Mexico. Proceedings of the San Diego Society of Natural History, 1, 1–34.

    Kevan, D.K.M. & Akbar, S.S. (1964) The Pyrgomorphidae (Orthoptera: Acridoidea): Their systematics, tribal divisions and distribution. The Canadian Entomologist, 96, 1505–1536.

    https://doi.org/10.4039/Ent961505-12

    Kevan, D.K.M., Akbar, S.S. & Chang, Y.-C. (1969) The concealed copulatory structures of the Pyrgomorphidae (Orthoptera: Acridoidea). Part I. General introduction. Eos, 44, 165–266.

    Kevan, D.K.M., Akbar, S.S. & Chang, Y.-C. (1970) The concealed copulatory structures of the Pyrgomorphidae (Orthoptera: Acridoidea). Part II. Tribes Fijipyrgini, Verduliini, Brunniellini, Psednurini, Mitricephalini, Geloiini, Sagittacridini, Gymnohippini and Malagasphenini. Eos, 45, 173–228.

    Kevan, D.K.M., Akbar, S.S. & Chang, Y.-C. (1971) The concealed copulatory structures of the Pyrgomorphidae (Orthoptera: Acridoidea). Part III. Tribes Chapmanacridini, Ichthiacridini, Ichthyotettigini, Orthacridini, Popoviini and Nereniini. Eos, 46, 123–210.

    Kevan, D.K.M., Akbar, S.S. & Chang, Y.-C. (1972) The concealed copulatory structures of the Pyrgomorphidae (Orthoptera: Acridoidea). Part IV. Tribes Desmopterini, Monistriini, Chlorizeinini, Poekilocerini and Phymateini. Eos, 47, 137–234.

    Kevan, D.K.M., Akbar, S.S. & Chang, Y.-C. (1974) The concealed copulatory structures of the Pyrgomorphidae (Orthoptera: Acridoidea). Part V. Tribes Schulthessiini, Taphronotini, Dictyophorini, Tagastini, Pseudomorphacridini, Atractomorphini, Sphenariini and Omurini. Eos, 48, 203–294.

    Kevan, D.K.M., Akbar, S.S. & Chang, Y.-C. (1975) The concealed copulatory structures of the Pyrgomorphidae (Orthoptera: Acridoidea). Part VI (Conclusion). Tribes Pyrgomorphini and Chrotogonini. 49, 131–218.

    Kevan, D.K.M. & Chen, Y.-K. (1969) A revised synopsis of the genus Atractomorpha Saussure, 1862 (Orthoptera: Pyrgomorphidae), with an account of the African abberans-group. Zoological Journal of the Linnean Society, 48, 141–198.

    https://doi.org/10.1111/j.1096-3642.1969.tb00710.x

    Kevan, D.K.M. & Hsiung, C.-C. (1985) The tropical and southern African species of Pyrgomorpha Audinet-Serville, 1838, other than the P. conica-group (Orthotpera: Acridoidea: Pyrgomorphidae). Journal of the Entomological Society of South Africa, 48, 49–102.

    Kevan, D.K.M. & Hsiung, C.-C. (1989) The palaearctic species of Pyrgomorpha Audinet-Serville, 1838, other than the P. conica-group (Orthoptera: Acridoidea: Pyrgomorphidae: Pyrgomorphini). II. Biocosme Mésogéen, Nice, 6, 117–152.

    Kevan, D.K.M., Singh, A. & Akbar, S.S. (1964) A revision of the Mexican Pyrgormorphidae (Orthoptera: Acridoidea) I. Genera other than Sphenarium. Proceedings of the Academy of Natural Sciences of Philadelphia, 116, 231–298.

    Key, K.H.L. (1972) A revision of the Psednurini (Orthoptera: Pyrgomorphidae). Australian Journal of Zoology Supplementary Series, 14, 1–72.

    https://doi.org/10.1071/AJZS014

    Lanfear, R., Frandsen, P.B., Wright, A.M., Senfeld, T. & Calcott, B. (2017) PartitionFinder 2: New Methods for Selecting Partitioned Models of Evolution for Molecular and Morphological Phylogenetic Analyses. Molecular Biology and Evolution, 34, 772–773.

    https://doi.org/10.1093/molbev/msw260

    Leavitt, J.R., Hiatt, K.D., Whiting, M.F. & Song, H. (2013) Searching for the optimal data partitioning strategy in mitochondrial phylogenomics: A phylogeny of Acridoidea (Insecta: Orthoptera: Caelifera) as a case study. Molecular Phylogenetics and Evolution, 67, 494–508.

    https://doi.org/10.1016/j.ympev.2013.02.019

    Mariño-Pérez, R. & Song, H. (2018) Phylogeny of the grasshopper family Pyrgomorphidae (Caelifera, Orthoptera) based on morphology. Systematic Entomology, 43, 90–108.

    https://doi.org/10.1111/syen.12251

    Mariño-Pérez, R. & Song, H. (2019) On the origin of the New World Pyrgomorphidae (Insecta: Orthoptera). Molecular Phylogenetics and Evolution, 139, 106537.

    https://doi.org/10.1016/j.ympev.2019.106537

    Miller, M. A., Holder, M. T., Vos, R., Midford, P. R., Liebowitz, T., Chan, L., Hoover, P. & Warnow, T. (2011) The CIPRES Portals. Available from: http://www.phylo.org/sub_sections/portal (accessed 26 April 2021)

    Mugleston, J.D., Naegle, M., Song, H. & Whiting, M.F. (2018) A comprehensive phylogeny of Tettigoniidae (Orthoptera: Ensifera) reveals extensive ecomorph convergence and widespread taxonomic incongruence. Insect Systematics and Diversity, 2, 1–27.

    https://doi.org/10.1093/isd/ixy010

    Otte, D. (1994) Grasshoppers [Acridomorpha] B. Pamphagoidea, Orthoptera Species File. The Orthopterists’ Society and The Academy of Natural Sciences of Philadelphia, Philadelphia, 241 pp.

    Perez-Gelabert, D.E., Dominici, G.O. & Hierro, B. (1995) Jaragua: new genus and two new species of American pyrogomorphids (Orthoptera: Pyrgomorphidae) from Hispanolia, West Indies. Annals of the Entomological Society of America, 88, 31–38.

    https://doi.org/10.1093/aesa/88.1.31

    Rambaut, A. (2006–2009) FigTree: Tree Figure Drawing Tool. Version 1.3.1. Available from: http://tree.bio.ed.ac.uk/software/figtree/ (accessed 26 April 2021)

    Rambaut, A. & Drummond, A.J. (2003–2009) Tracer: MCMC Trace Analysis Tool Version. 1.5.0. Available from: http://tree.bio.ed.ac.uk/software/tracer/ (accessed 26 April 2021)

    Revell, L. J. (2012) phytools: An R package for phylogenetic comparative biology (and other things). Methods in Ecology and Evolution, 3, 217–223.

    https://doi.org/10.1111/j.2041-210X.2011.00169.x

    Ronquist, F., Teslenko, M., van der Mark, P., Ayres, D.L., Darling, A., Hohna, S., Larget, B., Liu, L., Suchard, M.A. & Huelsenbeck, J.P. (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology, 61, 539–542.

    https://doi.org/10.1093/sysbio/sys029

    Rowell, C.H.F. (1967) Experiments on aggregations of Phymateus purpurascens (Orthoptera, Acrididae, Pyrgomorphidae). Journal of Zoology, 152, 179–193.

    https://doi.org/10.1111/j.1469-7998.1967.tb01884.x

    Rowell, C.H.F. & Flook, P.K. (1998) Phylogeny of the Caelifera and the Orthoptera as derived from ribosomal gene sequences. Journal of Orthoptera Research, 7, 147–156.

    https://doi.org/10.2307/3503512

    Song, H., Amédégnato, C., Cigliano, M.M., Desutter-Grandcolas, L., Heads, S.W., Huang, Y., Otte, D. & 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.

    https://doi.org/10.1111/cla.12116

    Song, H., Béthoux, O., Shin, S., Donath, A., Letsch, H., Liu, S., McKenna, D.D., Meng, G., Misof, B., Podsiadlowski, L., Zhou, X., Wipfler, B. & Simon, S. (2020) Phylogenomic analysis sheds light on the evolutionary pathways towards acoustic communication in Orthoptera. Nature Communications, 11, 4939.

    https://doi.org/10.1038/s41467-020-18739-4

    Song, H., Mariño-Pérez, R., Woller, D.A. & Cigliano, M.M. (2018) Evolution, diversification, and biogeography of grasshoppers (Orthoptera: Acrididae). Insect Systematics and Diversity, 2, 1–25.

    https://doi.org/10.1093/isd/ixy008

    Svenson, G.J. & Whiting, M.F. (2004) Phylogeny of Mantodea based on molecular data: evolution of a charismatic predator. Systematic Entomology, 29, 359–370.

    https://doi.org/10.1111/j.0307-6970.2004.00240.x

    Uvarov, B.P. (1977) Grasshoppers and Locusts. Vol. 2. Centre for Overseas Pest Research. London, 613 pp.

    Vaidya, G., Lohman, D.J. & Meier, R. (2011) SequenceMatrix: concatenation software for the fast assembly of multi-gene datasets with character set and codon information. Cladistics, 27, 171–180.

    https://doi.org/10.1111/j.1096-0031.2010.00329.x

    Wenzel, J.W. & Siddall, M. E. (1999) Noise. Cladistics, 15, 51–64.

    https://doi.org/10.1111/j.1096-0031.1999.tb00394.x

    Whitman, D.W. (1990) Grasshopper chemical communication. In: Chapman, R.F. & Joern, A. (Eds), Biology of Grasshoppers. John Wiley & Sons, New York, New York, pp. 357–391.

    Woller, D.A. & Song, H. (2017) Investigating the functional morphology of genitalia during copulation in the grasshopper Melanoplus rotundipennis (Scudder, 1878) via correlative microscopy. Journal of Morphology, 278, 334–359.

    https://doi.org/10.1002/jmor.20642

    Yang, L., Ravikanthachari, N., Mariño-Pérez, R., Deshmukh, R., Wu, M., Rosenstein, A., Kunte, K., Song, H. & Andolfatto, P. (2019) Predictability in the evolution of Orthopteran cardenolide insensitivity. Philosophical Transactions of the Royal Society of London B, 374, 20180246.

    https://doi.org/10.1098/rstb.2018.0246