Hostname: page-component-cd9895bd7-jn8rn Total loading time: 0 Render date: 2024-12-19T00:31:59.088Z Has data issue: false hasContentIssue false
  • English
  • Français

Mitochondrial DNA suggests cryptic speciation in Prodiplosis longifila Gagné (Diptera: Cecidomyiidae) associated with geographic distance and host specialization

Published online by Cambridge University Press:  18 January 2018

D.N. Duque-Gamboa ,
M.F. Castillo-Cárdenas ,
L.M. Hernández ,
Y.C. Guzmán ,
M.R. Manzano  and
N. Toro-Perea
D.N. Duque-Gamboa*
Affiliation:
Departamento de Biología, Universidad del Valle, Cali, Colombia
M.F. Castillo-Cárdenas
Affiliation:
Departamento de Biología, Universidad del Valle, Cali, Colombia
L.M. Hernández
Affiliation:
Departamento de Ciencias Agrícolas, Universidad Nacional de Colombia Sede Palmira, Palmira, Colombia
Y.C. Guzmán
Affiliation:
Departamento de Ciencias Agrícolas, Universidad Nacional de Colombia Sede Palmira, Palmira, Colombia
M.R. Manzano
Affiliation:
Departamento de Ciencias Agrícolas, Universidad Nacional de Colombia Sede Palmira, Palmira, Colombia
N. Toro-Perea
Affiliation:
Departamento de Biología, Universidad del Valle, Cali, Colombia
*
*Author for correspondence Phone: +57(2) 3212152 Fax: +57(2) 3212977 E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Prodiplosis longifila is reported as a pest of a wide range of species cultivated in America, including citrus, solanaceous species and asparagus. This species has different behavioural traits that are primarily centred on the oviposition habit and the feeding of larvae, which can change depending on the host. However, scarce information is available on population studies and the natural history of this insect, and uncertainty exists about the taxonomic identity and the geographic distribution of this species. The main objective was to perform a phylogenetic and genetic study of P. longifila populations and to define whether the North American and South American populations belong to the same species or whether a differentiation process had occurred due to geographic distance. A second objective was to determine whether this species showed genetic differentiation by host specialization in South America. The phylogenetic and population analyses based on DNA barcodes (cytochrome oxidase I gene) and a region of the ribosomal DNA (ITS2) revealed divergent clades attributable to geographic distance and host specificity. The North American and South American P. longifila insects were confirmed to be genetically distinct, and the genetic distances exceeded the values expected for intraspecific variation. In South America, the population analysis of P. longifila from tomato, sweet pepper (Solanaceae), Tahiti lime and key lime (Rutaceae) hosts evidenced high genetic differentiation between populations associated with different hosts and an absence of gene flow between these groups, suggesting the corresponding formation of cryptic species.

Keywords

Prodiplosis longifilaCOIITS2genetic differentiationgeographic isolationhost range
Type
Research Papers
Information
Bulletin of Entomological Research , Volume 108 , Issue 6 , December 2018 , pp. 739 - 749
Check for updates
Copyright
Copyright © Cambridge University Press 2018 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Aide, T.M., Clark, M.L., Grau, H.R., López-Carr, D., Levy, M.A., Redo, D., Bonilla-Moheno, M., Riner, G., Andrade-Núñez, M.J. & Muñiz, M. (2013) Deforestation and reforestation of Latin America and the Caribbean (2001–2010). Biotropica 45, 262–271.Google Scholar
Berlocher, S.H. & Feder, J.L. (2002) Sympatric speciation in phytophagous insects: moving beyond controversy? Annual Review of Entomology 47, 773–815.Google Scholar
Bickford, D., Lohman, D.J., Sodhi, N.S., Ng, P.K.L., Meier, R., Winker, K., Ingram, K.K. & Das, I. (2007) Cryptic species as a window on diversity and conservation. Trends in Ecology & Evolution 22, 148–155.Google Scholar
Bolnick, D.I. & Fitzpatrick, B.M. (2007) Sympatric speciation: models and empirical evidence. Annual Review of Ecology, Evolution, and Systematics 38, 459–487.Google Scholar
Bush, G.L. (1975) Modes of animal speciation. Annual Review of Ecology and Systematics 6, 339–364.Google Scholar
Collins, F.H. & Paskewitz, S.M. (1996) A review of the use of ribosomal DNA (rDNA) to differentiate among cryptic Anopheles species. Insect Molecular Biology 5, 1–9.Google Scholar
Cook, M.A., Ozeroff, S.N., Fitzpatrick, S.M. & Roitberg, B.D. (2011) Host-associated differentiation in reproductive behaviour of cecidomyiid midges on cranberry and blueberry. Entomologia Experimentalis et Applicata 141, 8–14.Google Scholar
Darriba, D., Taboada, G.L., Doallo, R. & Posada, D. (2012) Jmodeltest 2: more models, new heuristics and parallel computing. Nature Methods 9, 772–772.Google Scholar
Dent, D. (2000) Insect Pest Management. Wallingford, UK, CABI Publishing.Google Scholar
Dorchin, N., Scott, E.R., Clarkin, C.E., Luongo, M.P., Jordan, S. & Abrahamson, W.G. (2009) Behavioural, ecological and genetic evidence confirm the occurrence of host-associated differentiation in goldenrod gall-midges. Journal of Evolutionary Biology 22, 729–739.Google Scholar
Drès, M. & Mallet, J. (2002) Host races in plant–feeding insects and their importance in sympatric speciation. Philosophical Transactions of the Royal Society of London B: Biological Sciences 357, 471–492.Google Scholar
Edgar, R.C. (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 32, 1792–1797.Google Scholar
Excoffier, L., Laval, G. & Schneider, S. (2005) Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evolutionary Bioinformatics Online 1, 47–50.Google Scholar
Folmer, O., Black, M., Hoeh, W. & Lutz, R. (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3, 294–299.Google Scholar
Gagné, R.J. (1986 a) Revision of Prodiplosis (Diptera: Cecidomyiidae) with descriptions of three new species. Annals of the Entomological Society of America 79, 235–245.Google Scholar
Gagné, R.J. (1986 b) A new Nearctic species of Contarinia (Diptera: Cecidomyiidae) recently introduced into Hawaii on Cupressus (Cupressaceae). Proceedings of the Entomological Society of Washington 88, 127–130.Google Scholar
Gagné, R.J. (1994) The Gall Midges of the Neotropical Region. Ithaca, New York, Cornell University Press.Google Scholar
Gagné, R.J. & Jaschhof, M. (2014) A Catalog of the Cecidomyiidae (Diptera) of the World. 3rd edn. Digital version 2. Washington, USA, USDA.Google Scholar
Guillemaud, T., Ciosi, M., Lombaert, E. & Estoup, A. (2011) Biological invasions in agricultural settings: insights from evolutionary biology and population genetics. Comptes Rendus Biologies 334, 237–246.Google Scholar
Guindon, S. & Gascuel, O. (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology 52, 696–704.Google Scholar
Hall, T.A. (1999) Bioedit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41, 95–98.Google Scholar
Hebert, P.D.N., Cywinska, A. & Ball, S.L. (2003) Biological identifications through DNA barcodes. Proceedings of the Royal Society of London B: Biological Sciences 270, 313–321.Google Scholar
Hebert, P.D.N., Penton, E.H., Burns, J.M., Janzen, D.H. & Hallwachs, W. (2004) Ten species in one: DNA barcoding reveals cryptic species in the neotropical skipper butterfly Astraptes fulgerator. Proceedings of the National Academy of Sciences of the United States of America 101, 14812–14817.Google Scholar
Hernandez, L.M., Guzman, Y.C., Martínez-Arias, A., Manzano, M.R. & Selvaraj, J.J. (2015) The bud midge Prodiplosis longifila: damage characteristics, potential distribution and presence on a new crop host in Colombia. SpringerPlus 4, 205.Google Scholar
Ji, Y., Zhang, D. & He, L. (2003) Evolutionary conservation and versatility of a new set of primers for amplifying the ribosomal internal transcribed spacer regions in insects and other invertebrates. Molecular Ecology Notes 3, 581–585.Google Scholar
Jinbo, U., Kato, T. & Ito, M. (2011) Current progress in DNA barcoding and future implications for entomology. Entomological Science 14, 107–124.Google Scholar
Kanno, H. & Harris, M.O. (2000) Both chemical and physical features of grass leaves influence host selection by the Hessian fly. Journal of Chemical Ecology 26, 2335–2354.Google Scholar
Kikkert, J.R., Hoepting, C.A., Wu, Q., Wang, P., Baur, R. & Shelton, A.M. (2006) Detection of Contarinia nasturtii (Diptera: Cecidomyiidae) in New York, a new pest of cruciferous plants in the United States. Journal of Economic Entomology 99, 1310–1315.Google Scholar
Lampo, M. & Medialdea, V. (1994) Dispersal pattern of the sorghum midge (Diptera: Cecidomyiidae) in sorghum plots. Environmental Entomology 23, 551–555.Google Scholar
Librado, P. & Rozas, J. (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25, 1451–1452.Google Scholar
Mathur, S., Cook, M.A., Sinclair, B.J. & Fitzpatrick, S.M. (2012) DNA barcodes suggest cryptic speciation in Dasineura oxycoccana (Diptera: Cecidomyiidae) on cranberry, Vaccinium macrocarpon, and blueberry, V. corymbosum. Florida Entomologist 95, 387–394.Google Scholar
Miao, J., Wu, Y.Q., Gong, Z.J., He, Y.Z., Duan, Y. & Jiang, Y.L. (2013) Long-distance wind-borne dispersal of Sitodiplosis mosellana Géhin (Diptera:Cecidomyiidae) in Northern China. Journal of Insect Behavior 26, 120–129.Google Scholar
Olson, D.M., Dinerstein, E., Wikramanayake, E.D., Burgess, N.D., Powell, G.V.N., Underwood, E.C., D'amico, J.A., Itoua, I., Strand, H.E. & Morrison, J.C. (2001) Terrestrial ecoregions of the world: a new map of life on earth: a new global map of terrestrial ecoregions provides an innovative tool for conserving biodiversity. BioScience 51, 933–938.Google Scholar
Peakall, R.O.D. & Smouse, P.E. (2006) GENALEX 6: genetic analysis in excel. Population genetic software for teaching and research. Molecular Ecology Notes 6, 288–295.Google Scholar
Pendleton, B.B. & Teetes, G.L. (1994) Sorghum midge dispersal from sorghum. Southwestern Entomologist 19, 1–10.Google Scholar
Pérez-Portela, R., Arranz, V., Rius, M. & Turon, X. (2013) Cryptic speciation or global spread? The case of a cosmopolitan marine invertebrate with limited dispersal capabilities. Scientific Reports 3, 3197.Google Scholar
Pizano, C. & Garcia, H. (2014) El bosque seco tropical en Colombia. Bogotá, DC, Colombia, Instituto de Investigación de Recursos Biológicos Alexander von Humboldt.Google Scholar
Posada, D. & Crandall, K.A. (2001) Intraspecific gene genealogies: trees grafting into networks. Trends in Ecology & Evolution 16, 37–45.Google Scholar
QGIS Development Team (2017) QGIS Geographic Information System. Open Source Geospatial Foundation Project. Available online at https://www.qgis.org/es/site/Google Scholar
Richards, T.J., Shanafelt, D.W. & Fenichel, E.P. (2014) Foreclosures and invasive insect spread: the case of Asian citrus psyllid. American Journal of Agricultural Economics 96, 615–630.Google Scholar
Stireman, J.O. III, Nason, J.D. & Heard, S.B. (2005) Host-associated genetic differentiation in phytophagous insects: general phenomenon or isolated exceptions? Evidence from a goldenrod-insect community. Evolution 59, 2573–2587.Google Scholar
Stokes, K., Stiling, P., Gilg, M.R. & Rossi, A.M. (2012) The gall midge Asphondylia borrichiae (Diptera: Cecidomyiidae): an indigenous example of host-associated genetic divergence in sympatry. Environmental Entomology 41, 1246–1254.Google Scholar
Sylven, E. & Lövgren, L. (1995) Dasineura ingeris sp. n.(Diptera: Cecidomyiidae) on Salix viminalis in Sweden, including comparisons with some other Dasineura species on Salix. Systematic Entomology 20, 59–71.Google Scholar
Tamura, K., Stecher, G., Peterson, D., Filipski, A. & Kumar, S. (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution 30, 2725–2729.Google Scholar
Thomas, Y., Bethenod, M-T., Pelozuelo, L., Frérot, B., Bourguet, D. & Pitnick, S. (2003) Genetic isolation between two sympatric host-plant races of the European corn borer, Ostrinia nubilalis Hübner. I. Sex pheromone, moth emergence timing, and parasitism. Evolution 57, 261–273.Google Scholar
Toews, D.P.L. & Brelsford, A. (2012) The biogeography of mitochondrial and nuclear discordance in animals. Molecular Ecology 21, 3907–3930.Google Scholar
Turelli, M., Barton, N.H. & Coyne, J.A. (2001) Theory and speciation. Trends in Ecology & Evolution 16, 330–343.Google Scholar
Valarezo, O., Canarte, E., Navarrete, B. & Arias de Lopez, M. (2003) Prodiplosis longifilia Diptera:(Cecidomyiidae), principal plaga del tomate en el Ecuador. Diagnóstico, Bioecología y Manejo. Iniap, Promsa y Cedege. Manual no. 51. Ecuador.Google Scholar
Via, S. (1999) Reproductive isolation between sympatric races of pea aphids. I. Gene flow restriction and habitat choice. Evolution 53, 1446–1457.Google Scholar
Via, S. (2001) Sympatric speciation in animals: the ugly duckling grows up. Trends in Ecology & Evolution 16, 381–390.Google Scholar
Walker, T.J. (1964) Cryptic species among sound-producing ensiferan Orthoptera (Gryllidae and Tettigoniidae). The Quarterly Review of Biology 39, 345–355.Google Scholar
Watterson, G.A. & Guess, H.A. (1977) Is the most frequent allele the oldest? Theoretical Population Biology 11, 141–160.Google Scholar
Withers, T.M., Harris, M.O. & Madie, C. (1997) Dispersal of mated female Hessian Flies (Diptera: Cecidomyiidae) in field arrays of host and nonhost plants. Environmental Entomology 26, 1247–1257.Google Scholar
Yao, H., Song, J., Liu, C., Luo, K., Han, J., Li, Y., Pang, X., Xu, H., Zhu, Y. & Xiao, P. (2010) Use of ITS2 region as the universal DNA barcode for plants and animals. PLoS ONE 5, e13102.Google Scholar
Zhang, D.X. & Hewitt, G.M. (2003) Nuclear DNA analyses in genetic studies of populations: practice, problems and prospects. Molecular Ecology 12, 563–584.Google Scholar
Zhang, G.F., Meng, X.Q., Min, L., Qiao, W.N. & Wan, F.H. (2012) Rapid diagnosis of the invasive species, Frankliniella occidentalis (Pergande): a species-specific COI marker. Journal of Applied Entomology 136, 410–420.Google Scholar