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Issue: Vol. 4272 No. 4: 31 May 2017
Type: Article
Published: 2017-05-31
DOI: 10.11646/zootaxa.4272.4.3
Page range: 529–550
Abstract views: 178
PDF downloaded: 177

A new Neotibicen cicada subspecies (Hemiptera: Cicadidae) from the southeastern USA forms hybrid zones with a widespread relative despite a divergent male calling song

Dept. of Ecology and Evolutionary Biology, University of Connecticut, 75 N. Eagleville Rd., Storrs, CT 06269 USA
Dept. of Ecology and Evolutionary Biology, University of Connecticut, 75 N. Eagleville Rd., Storrs, CT 06269 USA
Hemiptera Acoustic behavior sexual signals hybridization hybrid zone parapatric distribution speciation

Abstract

A morphologically cryptic subspecies of Neotibicen similaris (Smith and Grossbeck) is described from forests of the Apalachicola region of the southeastern United States. Although the new form exhibits a highly distinctive male calling song, it hybridizes extensively where it meets populations of the nominate subspecies in parapatry, by which it is nearly surrounded. This is the first reported example of hybridization between North American nonperiodical cicadas. Acoustic and morphological characters are added to the original description of the nominate subspecies, and illustrations of complex hybrid song phenotypes are presented. The biogeography of N. similaris is discussed in light of historical changes in forest composition on the southeastern Coastal Plain.

 

References

  1. Alexander, R.D. (1962) The role of behavioral study in cricket classification. Systematic Zoology, 11, 53–72.
    https://doi.org/10.2307/2411453

    Allard, H.A. (1937) Some observations on the behavior of the periodical cicada Magicicada septendecim L. American Naturalist, 71, 588–604.
    https://doi.org/10.1086/280746

    Avise, J.C., Arnold, J., Ball, R.M., Bermingham, E., Lamb, T., Neigel, J.E., Reeb, C.A. & Saunders, N.C. (1987) Intraspecific phylogeography: the mitochondrial DNA bridge between population genetics and systematics. Annual Review of Ecology and Systematics, 18, 489–522.
    https://doi.org/10.1146/annurev.es.18.110187.002421

    Baker E., Price, B.W., Rycroft, D.D., Hill, J. & Smith, V.S. (2015) BioAcoustica: a free and open repository and analysis platform for bioacoustics. Database, 2015, 1–10.
    https://doi.org/10.1093/database/bav054

    Barton, N.H. & Hewitt, G.M. (1985) Analysis of hybrid zones. Annual Review of Ecology and Systematics, 16, 113–148.
    https://doi.org/10.1146/annurev.es.16.110185.000553

    Boer, A.J. de & Duffels, J.P. (1996) Historical biogeography of the cicadas of Wallacea, New Guinea and the West Pacific: a geotectonic explanation. Palaeogeography, Palaeoclimatology, Palaeoecology, 124, 153–177.
    https://doi.org/10.1016/0031-0182(96)00007-7

    Campbell, M.A., Van Leuven, J.T., Meister, R.C., Carey, K.M., Simon, C. & McCutcheon, J.P. (2015) Genome expansion via lineage splitting and genome reduction in the cicada endosymbiont Hodgkinia. Proceedings of the National Academy of Sciencees of the United States of America, 112, 10192–10199.
    https://doi.org/10.1073/pnas.1421386112

    Chilcote, C.A. & Stehr, F.W. (1984) A new record for Magicicada septendecim in Michigan (Homoptera:Cicadidae). Great Lakes Entomologist, 17, 53–54.

    Cole, J.A. (2008) A new cryptic species of cicada resembling Tibicen dorsatus revealed by calling song (Hemiptera: Auchenorrhyncha: Cicadidae). Annals of the Entomological Society of America, 101, 815–823.
    https://doi.org/10.1093/aesa/101.5.815

    Cole, J.A. (2017) A new species of Megatibicen endemic to Mescalero-Monahans shinnery sands (Hemiptera: Auchenorrhyncha: Cicadidae). Zootaxa, 4236 (3), 553–562.
    https://doi.org/10.11646/zootaxa.4236.3.9

    Cooley, J.R. & Marshall, D.C. (2004) Thresholds or comparisons: mate choice criteria and sexual selection in a periodical cicada, Magicicada septendecim (Hemiptera: Cicadidae). Behaviour, 141, 647–673.
    https://doi.org/10.1163/1568539042245187

    Davis, W.T. (1912) A new variety of Rihana (Cicada) sayi Grossbeck (Hemip.). Entomological News, 23, 261–262.

    Davis, W.T. (1918) Mississippi cicadas, with a key to the species of the southeastern United States. Journal of the New York Entomological Society, 26, 141–155.

    Davis, W.T. (1922) An annotated list of the cicadas of Virgina with description of a new species. Journal of the New York Entomological Society, 30, 36–52.

    De Queiroz, K. (2007) Species concepts and species delimitation. Systematic Biology, 56, 879–86.
    https://doi.org/10.1080/10635150701701083

    Delcourt, P.A. (1977) Goshen Springs: Late Quaternary vegetation record for southern Alabama. Ecology, 61, 371–386.
    https://doi.org/10.2307/1935195

    Delcourt, P.A. & Delcourt, H.R. (1977) The Tunica Hills, Louisiana-Mississippi: Late Glacial locality for spruce and deciduous forest species. Quaternary Research, 7, 218–237.
    https://doi.org/10.1016/0033-5894(77)90038-2

    Doolan, J.M. & Young, D. (1989) Relative importance of song parameters during flight phonotaxis and courtship in the bladder cicada Cystosoma saundersii. Journal of Experimental Biology, 141, 113–131.

    Ennen, J.R., Kalis, M.E., Patterson, A.L., Kreiser, B.R., Lovich, J.E., Godwin, J. & Qualls, C.P. (2014) Clinal variation or validation of a subspecies? A case study of the Graptemys nigrinoda complex (Testudines: Emydidae). Biological Journal of the Linnean Society, 111, 810–822.
    https://doi.org/10.1111/bij.12234

    Fleming, C.A. (1975) Acoustic behaviour as a generic character in New Zealand cicadas (Hemiptera: Homoptera). Journal of the Royal Society of New Zealand, 5, 47–64.
    https://doi.org/10.1080/03036758.1975.10419379

    Fonseca, P.J. (2014) Cicada acoustic communication. In: Hedwig, B. (Ed.), Insect Hearing and Acoustic Communication, Animal Signals and Communication. 1. Springer-Verlag, Berlin Heidelberg, pp. 101–121.
    https://doi.org/10.1007/978-3-642-40462-7_7

    Fonseca, P.J., Munch, D. & Hennig, R.M. (2000) How cicadas interpret acoustic signals. Nature, 405, 297–298.

    Frost, C. (2006) History and future of the longleaf pine ecosystem. In: Jose, S., Jokela, E.J. & Miller, D.L. (Eds.), The Longleaf Pine Ecosystem. Springer, New York, pp. 9–48.
    https://doi.org/10.1007/978-0-387-30687-2_2

    Godwin, J.C., Lovich, J.E., Ennen, J.R., Kreiser, B.R., Folt, B. & Lechowicz, C. (2014) Hybridization of two megacephalic map turtles (Testudines: Emydidae: Graptemys) in the Choctawhatchee River drainage of Alabama and Florida. Copeia, 2014, 725–742.
    https://doi.org/10.1643/CH-13-132

    Gustafson, G.T. & Miller, K.B. (2015) The New World whirligig beetles of the genus Dineutus Macleay, 1825 (Coleoptera, Gyrinidae, Gyrininae, Dineutini). ZooKeys, 2015, 1–135.
    https://doi.org/10.3897/zookeys.476.8630

    Hertach, T., Puissant, S., Gogala, M., Trilar, T., Hagmann, R., Baur, H., Kunz, G., Wade, E.J., Loader, S.P., Simon, C. & Nagel, P. (2016) Complex within a complex: Integrative taxonomy reveals hidden diversity in Cicadetta brevipennis (Hemiptera: Cicadidae) and unexpected relationships with a song divergent relative. PLoS ONE, 11, e0165562.
    https://doi.org/10.1371/journal.pone.0165562

    Hill, K.B.R., Marshall, D.C., Moulds, M.S. & Simon, C. (2015) Molecular phylogenetics, diversification, and systematics of Tibicen Latreille 1825 and allied cicadas of the tribe Cryptotympanini, with three new genera and emphasis on species from the USA and Canada (Hemiptera: Auchenorrhyncha: Cicadidae). Zootaxa, 3985 (2), 219–251.
    https://doi.org/10.11646/zootaxa.3985.2.3

    ICZN (1999) International Code of Zoological Nomenclature. 4th Edition. The International Trust of Zoological Nomenclature, London, 306 pp.

    Izzo, A.S. & Gray, D.A. (2004) Cricket song in sympatry: species specificity of song without reproductive character displacement in Gryllus rubens. Annals of the Entomological Society of America, 97 (4), 831–837.

    Jansson, R. & Dynesius, M. (2002) The fate of clades in a world of recurrent climatic change: Milankovitch oscillations and evolution. Annual Review of Ecology and Systematics, 33, 741–777.
    https://doi.org/10.1146/annurev.ecolsys.33.010802.150520

    LaMoreaux, H.K., Brook, G.A. & Knox, J.A. (2009) Late Pleistocene and Holocene environments of the Southeastern United States from the stratigraphy and pollen content of a peat deposit on the Georgia Coastal Plain. Palaeogeography Palaeoclimatology Palaeoecology, 280, 300–312.
    https://doi.org/10.1016/j.palaeo.2009.06.017

    Lee, Y.J. (2015) Description of a new genus, Auritibicen gen. nov., of Cryptotympanini (Hemiptera: Cicadidae) with redescriptions of Auritibicen pekinensis (Haupt, 1924) comb. nov. and Auritibicen slocumi (Chen, 1943) comb. nov. from China and a key to the species of Auritibicen. Zootaxa, 3980 (2), 241–254.
    https://doi.org/10.11646/zootaxa.3980.2.5

    Lee, Y.J. (2016) Description of three new genera, Paratibicen, Gigatibicen, and Ameritibicen, of Cryptotympanini (Hemiptera: Cicadidae) and a key to their species. Journal of Asia-Pacific Biodiversity, 9, 448–454.
    https://doi.org/10.1016/j.japb.2016.09.002

    Lloyd, J.E. (1966) Studies on the flash communication system in Photinus fireflies. Miscellaneous Publications of the Museum of Zoology of the University of Michigan, 130, 1–95.

    Marshall, D.C. & Cooley, J.R. (2000) Reproductive character displacement and speciation in periodical cicadas, with description of a new species, 13-year Magicicada neotredecim. Evolution, 54, 1313–1325.
    https://doi.org/10.1111/j.0014-3820.2000.tb00564.x

    Marshall, D.C., Cooley, J.R., Alexander, R.D. & Moore, T.E. (1996) New records of Michigan Cicadidae (Homoptera), with notes on the use of songs to monitor range changes. Great Lakes Entomologist, 29, 165–169.

    Marshall, D.C. & Hill, K.B.R. 2010. InsectSingers.com: Song recordings and information on acoustically signaling insects, especially cicadas of the United States and Canada. Available from: http://www.insectsingers.com (accessed 2 May 2017)

    Marshall, D.C., Hill, K.B.R., Cooley, J.R. & Simon, C. (2011) Hybridization, mitochondrial DNA taxonomy, and prediction of the early stages of reproductive isolation: Lessons from New Zealand cicadas of the genus Kikihia. Systematic Biology, 60, 482–502.
    https://doi.org/10.1093/sysbio/syr017

    Mendelson, T.C. & Shaw, K.L. (2012) The (mis)concept of species recognition. Trends in Ecology & Evolution, 27, 421–427.
    https://doi.org/10.1016/j.tree.2012.04.001

    Miller, K.B. & Bergsten, J. (2012) Phylogeny and classification of whirligig beetles (Coleoptera: Gyrinidae): relaxed-clock model outperforms parsimony and time-free Bayesian analyses. Systematic Entomology, 37, 706–746.
    https://doi.org/10.1111/j.1365-3113.2012.00640.x

    Moulds, M.S. (2005) An appraisal of the higher classification of cicadas (Hemiptera: Cicadoidea) with special reference to the Australian fauna. Records of the Australian Museum, 57, 375–446.
    https://doi.org/10.3853/j.0067-1975.57.2005.1447

    Moulds, M.S. & Hill, K.B.R. (2015) Phylogeny for the tribe Thophini (Cicadoidea: Cicadidae) with the description of a new subspecies of Thopha sessiliba Distant from Western Australia. Records of the Australian Museum, 67, 55–66.
    https://doi.org/10.3853/j.2201-4349.67.2015.1634

    Noss, R.F., Platt, W.J., Sorrie, B.A., Weakley, A.S., Means, D.B., Costanza, J. & Peet, R.K. (2015) How global biodiversity hotspots may go unrecognized: lessons from the North American Coastal Plain. Diversity and Distributions, 21, 236–244.
    https://doi.org/10.1111/ddi.12278

    Otte, D. (1992) Evolution of cricket songs. Journal of Orthoptera Research, 1, 25–49.
    https://doi.org/10.2307/3503559

    Popple, L.W. (2013) A revision of the Pauropsalta annulata Goding & Froggatt species group (Hemiptera: Cicadidae) based on morphology, calling songs and ecology, with investigations into calling song structure, molecular phylogenetic relationships and a case of hybridisation between two subspecies. Zootaxa, 3730 (1), 1–102.
    https://doi.org/10.11646/zootaxa.3730.1.1

    RDevelopmentCoreTeam. (2011) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available from: http://www.r-project.org/ (accessed 2 May 2017)

    Rice, W.R. & Hostert, E.E. (1993) Laboratory experiments on speciation: What have we learned in 40 years? Evolution, 47, 1637–1653.
    https://doi.org/10.2307/2410209

    Riede, K. (1998) Acoustic monitoring of Orthoptera and its potential for conservation. Journal of Insect Conservation, 2, 217–223.
    https://doi.org/10.1023/A:1009695813606

    Russell, D.A., Rich, F.J., Schneider, V. & Lynch-Stieglitz, J. (2009) A warm thermal enclave in the Late Pleistocene of the South-eastern United States. Biological Review, 84, 173–202.
    https://doi.org/10.1111/j.1469-185X.2008.00069.x

    Sanborn, A.F. (1999) Cicada (Homoptera: Cicadoidea) type material in the collections of the American Museum of Natural History, California Academy of Sciences, Snow Entomological Museum, Staten Island Institute of Arts and Sciences, and the United States National Museum. Florida Entomologist, 82, 34–60.
    https://doi.org/10.2307/3495835

    Sanborn, A.F. (2015) New combinations for six species belonging to Cryptotympanini Handlirsch (Hemiptera: Cicadidae), former members of the genus Tibicen Latreille, 1825. Zootaxa, 4027 (3), 447–50.
    https://doi.org/10.11646/zootaxa.4027.3.9

    Sanborn, A.F. & Heath, M.S. (2012) The cicadas (Hemiptera: Cicadoidea: Cicadidae) of North America north of Mexico. Entomological Society of America, Lanham, MD, 227 pp.

    Sanborn, A.F. & Heath, M.S. (2016) Megatibicen n. gen., a new North American cicada genus (Hemiptera: Cicadidae: Cicadinae: Cryptotympanini). Zootaxa, 4168, 577–582.
    https://doi.org/10.11646/zootaxa.4168.3.10

    Sanborn, A.F. & Heath, M.S. (2017) Priority and synonymy of some North American cicada genera (Hemiptera: Cicadidae: Cicadinae: Cryptotympanini). Zootaxa, 4243, 377–382.
    https://doi.org/10.11646/zootaxa.4243.2.8

    Sanborn, A.F. & Phillips, P. (2013) Biogeography of the cicadas (Hemiptera: Cicadidae) of North America, north of Mexico. Diversity, 5, 166–239.
    https://doi.org/10.3390/d5020166

    Sanborn, A.F., Phillips, P.K. & Gillis, P. (2008) The cicadas of Florida (Hemiptera: Cicadoidea: Cicadidae). Zootaxa, 1916, 1–43.

    Schul, J. (1998) Song recognition by temporal cues in a group of closely related bushcricket species (genus Tettigonia). Journal of Comparative Physiology A Sensory Neural and Behavioral Physiology, 183, 401–410.
    https://doi.org/10.1007/s003590050266

    Schwartz, M.W. (1994) Natural distribution and abundance of forest species and communities in northern Florida. Ecology, 75, 687–705.
    https://doi.org/10.2307/1941727

    Servedio, M.R. & Noor, M.A.F. (2003) The role of reinforcement in speciation: Theory and data. Annual Review of Ecology, Evolution, and Systematics, 34, 339–364.
    https://doi.org/10.1146/annurev.ecolsys.34.011802.132412

    Simmons, J.A., Weaver, E.G., Strother, W.F., Pylka, J.M. & Long, G.R. (1971) Acoustic behavior of three sympatric species of 17-yr cicadas. Journal of the Acoustical Society of America, 49, 93.
    https://doi.org/10.1121/1.1976148

    Smith, J.B. & Grossbeck, J.A. (1907) Studies in certain cicada species. Entomological News, 18, 116–129.

    Stucky, B. (2013) Morphology, bioacoustics, and ecology of Tibicen neomexicensis sp. n., a new species of cicada from the Sacramento Mountains in New Mexico, U.S.A. (Hemiptera, Cicadidae, Tibicen). ZooKeys, 337, 49–71.
    https://doi.org/10.3897/zookeys.337.5950

    Sueur, J. & Aubin, T. (2002) Acoustic communication in the Palearctic red cicada, Tibicina haematodes: chorus organisation, calling-song structure, and signal recognition. Canadian Journal of Zoology, 80, 126–136.
    https://doi.org/10.1139/z01-212

    Sueur, J. & Aubin, T. (2003) Specificity of cicada calling songs in the genus Tibicina (Hemiptera: Cicadidae). Systematic Entomology, 28, 481–492.
    https://doi.org/10.1046/j.1365-3113.2003.00222.x

    Swenson, N.G. & Howard, D.J. (2005) Clustering of contact zones, hybrid zones, and phylogeographic breaks in North America. American Naturalist, 166, 581–591.
    https://doi.org/10.1086/491688

    USGS (2016) Mineral Resources On-Line Spatial Data. Geologic Maps of US States. Vol. 2016. Available from: https://mrdata.usgs.gov/ (accessed 2 May 2017)

    Van Duzee, E.P. (1916) Check list of Hemiptera (excepting the Aphididae, Aleurodidae and Coccidae) of America, north of Mexico. New York Entomological Society, New York, 111 pp.

    Walker, D. & Avise, J.C. (1998) Principles of phylogeography as illustrated by freshwater and terrestrial turtles in the southeastern United States. Annual Review of Ecology and Systematics, 29, 23–58.
    https://doi.org/10.1146/annurev.ecolsys.29.1.23

    Walker, T.J. (1974) Character displacement and acoustic insects. American Zoologist, 14, 1137–11150.
    https://doi.org/10.1093/icb/14.4.1137

    Walker, T.J. (2000) Seasonal occurrence of cicadas in Alachua County, Florida. Available from: http://entnemdept.ifas.ufl.edu/walker/buzz/c700fl2.htm. (accessed 17 December 2016)

    Watts, W.A. (1971) Postglacial and interglacial vegetation history of southern Georgia and central Florida. Ecology, 52, 676–690.
    https://doi.org/10.2307/1934159

    Watts, W.A. (1980) Late-Quaternary vegetation history at White Pond on the inner coastal plain of South Carolina. Quaternary Research, 13, 187–199.
    https://doi.org/10.1016/0033-5894(80)90028-9

    Watts, W.A., Hansen, B.C.S. & Grimm, E.C. (1992) Camel Lake: a 40,000-yr record of vegetational and forest history from northwest Florida. Ecology, 73, 1056–1066.
    https://doi.org/10.2307/1940180

    Webb, T.I. & Bartlein, P.J. (1992) Global changes during the last 3 million years: climatic controls and biotic responses. Annual Review of Ecology and Systematics, 23, 141–173.
    https://doi.org/10.1146/annurev.es.23.110192.001041

    Wiley, C., Ellison, C.K. & Shaw, K.L. (2012) Widespread genetic linkage of mating signals and preferences in the Hawaiian cricket Laupala. Proceedings of the Royal Society Biological Sciences Series B, 279, 1203–1209.
    https://doi.org/10.1098/rspb.2011.1740

    Williams, J.W., Shuman, B.N., Webb, T., Bartlein, P.J. & Leduc, P.L. (2004) Late-Quaternary Vegetation Dynamics in North America: Scaling from Taxa to Biomes. Ecological Monographs, 74, 309–334.
    https://doi.org/10.1890/02-4045

    Wilson, E.O. & Brown, J.W.L. (1953) The subspecies concept and its taxonomic application. Systematic Zoology, 2, 97–111.
    https://doi.org/10.2307/2411818