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A “complex” problem: delimiting sibling species boundaries in black flies (Diptera: Simuliidae)

  • Ida M. Conflitti (a1), Gerald F. Shields (a2) and Douglas C. Currie (a1)

Abstract

Rapid and recent lineage radiations pose challenges to systematists. Using members of the highly diverse Simulium arcticum Malloch complex, we tested whether the cytochrome c oxidase subunit I (COI) barcoding gene can differentiate black fly sibling species. Members of the S. arcticum complex were monophyletic in relation to two morphospecies and two cryptic species of the Simulium malyschevi Dorogostaisky et al. and Simulium noelleri Friederichs species-groups, respectively. Of five S. arcticum sibling species analysed, only Simulium negativum Adler et al. was monophyletic. No other members of the complex could be distinguished using COI barcodes. The inability to resolve S. arcticum sibling species resulted because (1) haplotypes were shared between species and (2) the distribution of interspecific genetic distances completely overlapped the range of variation within species. Potential sources of incongruence between barcode data and species boundaries include imperfect taxonomy, inadequate genetic information, incomplete lineage sorting, and/or introgressive hybridization. We ruled out imperfect taxonomy because chromosomal, ecological, and distributional evidence support the validity of S. arcticum sibling species. Therefore, current nomenclature should be maintained pending further study. We conclude that one or more of the latter three sources of incongruence could be responsible for the lack of reciprocal monophyly among species of the S. arcticum complex.

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Corresponding author

1Corresponding author. Department of Natural History, Royal Ontario Museum, 100 Queen's Park, Toronto, Ontario M5S 2C6, Canada (e-mail: dc.currie@utoronto.ca).

References

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Adler, P.H., Cheke, R.A., Post, R.J. 2010. Evolution, epidemiology, and population genetics of black flies (Diptera: Simuliidae). Infection Genetics and Evolution, 7: 846865.
Adler, P.H., Crosskey, R.W. 2010. World blackflies (Diptera: Simuliidae): a comprehensive revision of the taxonomic and geographical inventory (2010). Clemson University, South Carolina [online]. Available from http://entweb.clemson.edu/biomia/pdfs/ [accessed 24 January 2011].
Adler, P.H., Currie, D.C., Wood, D.M. 2004. The black flies (Simuliidae) of North America. Cornell University Press, New York.
Adler, P.H., Huang, Y. 2011. Integrated systematics of the Simuliidae (Diptera): evolutionary relationships of the little-known Palearctic black fly Simulium acrotrichum. The Canadian Entomologist, 143: 612628.
Ball, S.L., Hebert, P.D.N., Burian, S.K., Webb, J.M. 2005. Biological identifications of mayflies (Ephemeroptera) using DNA barcodes. Journal of the North American Benthological Society, 24: 508524.
Barrett, R.D.H., Hebert, P.D.N. 2005. Identifying spiders through DNA barcodes. Canadian Journal of Zoology, 83: 481491.
Charnetski, W.A., Haufe, W.O. 1981. Control of S. arcticum Malloch in Northern Alberta, Canada. In Blackflies: the future for biological methods in integrated control. Edited by M. Laird. Academic Press, New York. pp. 117132.
Clary, D.O., Wolstenholme, D.R. 1985. The mitochondrial DNA molecule of Drosophila yakuba: nucleotide sequence, gene organization, and genetic code. Journal of Molecular Evolution, 22: 252271.
Clement, M., Posada, D., Crandall, K. 2000. TCS: a computer program to estimate gene genealogies. Molecular Ecology, 9: 16571660.
Conflitti, I.M., Kratochvil, M.J., Spironello, M., Shields, G.F., Currie, D.C. 2010. Good species behaving badly: non-monophyly of black fly sibling species in the Simulium arcticum complex (Diptera: Simuliidae). Molecular Phylogenetics and Evolution, 57: 245257.
Currie, D.C. 1986. An annotated list of and keys to the immature black flies of Alberta (Diptera: Simuliidae). Memoirs of the Entomological Society of Canada, 134: 190.
Currie, D.C. 1997. Black flies (Diptera: Simuliidae) of the Yukon, with reference to the black fly fauna of northwestern North America. In Insects of the Yukon. Edited by H.V. Danks and J.A. Downes. Biological Survey of Canada (Terrestrial Arthropods), Ottawa, Ontario. pp. 563614.
Davies, D.M., Peterson, B.V. 1956. Observations on the mating, feeding, ovarian development, and oviposition of adult black flies (Simuliidae, Diptera). Canadian Journal of Zoology, 34: 615655.
Day, J.C., Goodall, T.I., Post, R.J. 2008. Confirmation of the species status of the blackfly Simulium galeratum in Britain using molecular taxonomy. Medical and Veterinary Entomology, 22: 5561.
Edwards, F.W. 1920. On the British species of Simulium – II. The early stages; with corrections and additions to Part I. Bulletin of Entomological Research, 11: 211246.
Felsenstein, J. 1985. Confidence limits on phylogenies: an approach using the bootstrap. Evolution, 39: 783791.
Finn, D.S., Theobald, D.M., Black, W.C., Poff, N.L. 2006. Spatial population genetic structure and limited dispersal in a Rocky Mountain alpine stream insect. Molecular Ecology, 15: 35533566.
Folmer, O., Black, M., Hoeh, W., Lutz, R., Vrijenhoek, R. 1994. DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology, 3: 294299.
Fredeen, F.J.H. 1969. Outbreaks of the black fly Simulium arcticum Malloch in Alberta. Quaestiones Entomologicae, 5: 341372.
Funk, D.J., Omland, K.E. 2003. Species-level paraphyly and polyphyly: frequency, causes, and consequences, with insights from animal mitochondrial DNA. Annual Review of Ecology, Evolution, and Systematics, 34: 397423.
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: 9598.
Hebert, P.D.N., Cywinska, A., Ball, S.L., deWaard, J.R. 2003a. Biological identifications through DNA barcodes. Proceedings of the Royal Society B: Biological Sciences, 270: 313321.
Hebert, P.D.N., Ratnasingham, S., deWaard, J.R. 2003b. Barcoding animal life: cytochrome c oxidase subunit 1 divergences among closely related species. Proceedings of the Royal Society B: Biological Sciences, 270: S96S99.
Hebert, P.D.N., Stoeckle, M.Y., Zemlak, T.S., Francis, C.M. 2004. Identification of birds through DNA barcodes. PLoS Biology, 2: 16571663.
Ilmonen, J., Adler, P.H., Malmqvist, B., Cywinska, A. 2009. The Simulium vernum group (Diptera: Simuliidae) in Europe: multiple character sets for assessing species status. Zoological Journal of the Linnean Society, 156: 847863.
Joy, D.A., Craig, D.A., Conn, J.E. 2007. Genetic variation tracks ecological segregation in Pacific island black flies. Heredity, 99: 452459.
Kerr, K.C.R., Stoeckle, M.Y., Dove, C.J., Weigt, L.A., Francis, C.M., Hebert, P.D.N. 2007. Comprehensive DNA barcode coverage of North American birds. Molecular Ecology Notes, 7: 535543.
Koch, D.A., Duncan, G.A., Parsons, T.J., Pruess, K.P., Powers, T.O. 1998. Effect of preservation methods, parasites, and gut content of black flies (Diptera: Simuliidae) on polymerase chain reaction products. Journal of Medical Entomology, 35: 314318.
Meyer, C.P., Paulay, G. 2005. DNA barcoding: error rates based on comprehensive sampling. PLoS Biology, 12: 22292238.
Monaghan, M.T., Balke, M., Gregory, T.R., Vogler, A.P. 2005. DNA-based species delineation in tropical beetles using mitochondrial and nuclear markers. Philosophical Transactions of the Royal Society B: Biological Sciences, 360: 19251933.
Moritz, C., Cicero, C. 2004. DNA barcoding: promise and pitfalls. PLoS Biology, 10: 15291531.
Nardi, F., Carapelli, A., Fanciulli, P.P., Dallai, R., Frati, F. 2001. The complete mitochondrial DNA sequence of the basal Hexapod Tetrodontophora bielanensis: evidence for heteroplasmy and tRNA translocations. Molecular Biology and Evolution, 18: 12931304.
Nei, M., Kumar, S. 2000. Molecular evolution and phylogenetics. Oxford University Press, New York.
Post, R.J., Flook, P.K., Millest, A.L. 1993. Methods for the preservation of insects for DNA studies. Biochemical Systematics and Ecology, 21: 8592.
Pramual, P., Kuvangkadilok, C., Baimai, V., Walton, C. 2005. Phylogeography of the black fly Simulium tani (Diptera: Simuliidae) from Thailand as inferred from mtDNA sequences. Molecular Ecology, 14: 39894001.
Rivera, J., Currie, D.C. 2009. Identification of Nearctic black flies using DNA barcodes (Diptera: Simuliidae). Molecular Ecology Resources, 9: 224236.
Rothfels, K.H. 1979. Cytotaxonomy of black flies (Simuliidae). Annual Review of Entomology, 24: 507537.
Rothfels, K.H. 1981. Cytological approaches to the study of black fly systematics and evolution. In Application of genetics and cytology in insect systematics and evolution. Edited by M.W. Stock. Forest, Wildlife, and Range Experiment Station, University of Idaho, Moscow, Idaho. pp. 6783.
Rothfels, K.H. 1989. Speciation in black flies. Genome, 32: 500509.
Rothfels, K.H., Dunbar, R.W. 1953. The salivary gland chromosomes of the black fly Simulium vittatum Zett. Canadian Journal of Zoology, 31: 226241.
Shields, G.F., Christiaens, B.A., Van Leuven, M.L., Hartman, A.L. 2009. Reproductive status and continuity of taxa of the Simulium arcticum complex (Diptera: Simuliidae) at the Clearwater River, Montana (2007, 2008, and 2009). Western North American Naturalist, 69: 511520.
Shields, G.F., Clausen, G.M., Marchion, C.S., Michel, T.L., Styren, K.C., Riggin, C.N., et al 2007a. The effect of elevation on the distribution of sibling species in the Simulium arcticum complex (Diptera: Simuliidae). Western North American Naturalist, 67: 3945.
Shields, G.F., Pickens, J.A., Clausen, G.M., Strizich, L.M. 2007b. Reproductive status of cytoforms in a black fly complex in Montana. Intermountain Journal of Science, 13: 3243.
Shields, G.F., Procunier, W.S. 1982. A cytological description of sibling species of Simulium (Gnus) arcticum (Diptera: Simuliidae). Polar Biology, 1: 181192.
Smith, M.A., Poyarkov, N.A., Hebert, P.D.N. 2008. CO1 DNA barcoding amphibians: take the chance, meet the challenge. Molecular Ecology Notes, 8: 235246.
Swofford, D.L. 2003. PAUP*: phylogenetic analysis using parsimony (*and other methods) version 4. Sinauer Associates, Sunderland, Massachusetts.
Templeton, A.R., Crandall, K.A., Sing, C.F. 1992. A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping and DNA sequence data. III. Cladogram estimation. Genetics, 132: 619633.
Ward, R.D., Zemlak, T.S., Innes, B.H., Last, P.R., Hebert, P.D.N. 2005. DNA barcoding Australia's fish species. Philosophical Transactions of the Royal Society B: Biological Sciences, 360: 18471857.

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A “complex” problem: delimiting sibling species boundaries in black flies (Diptera: Simuliidae)

  • Ida M. Conflitti (a1), Gerald F. Shields (a2) and Douglas C. Currie (a1)

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