Hostname: page-component-8448b6f56d-cfpbc Total loading time: 0 Render date: 2024-04-20T01:27:36.574Z Has data issue: false hasContentIssue false
  • English
  • Français

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

Published online by Cambridge University Press:  07 March 2012

Ida M. Conflitti ,
Gerald F. Shields  and
Douglas C. Currie
Ida M. Conflitti
Affiliation:
Department of Ecology and Evolutionary Biology, University of Toronto, Toronto, Ontario M5S 3B2, Canada; and Department of Natural History, Royal Ontario Museum, Toronto, Ontario M5S 2C6, Canada
Gerald F. Shields
Affiliation:
Department of Natural Sciences, Carroll College, Helena, Montana 59601, United States of America
Douglas C. Currie*
Affiliation:
Department of Ecology and Evolutionary Biology, University of Toronto, Toronto, Ontario M5S 3B2, Canada; and Department of Natural History, Royal Ontario Museum, Toronto, Ontario M5S 2C6, Canada
*
1Corresponding author. Department of Natural History, Royal Ontario Museum, 100 Queen's Park, Toronto, Ontario M5S 2C6, Canada (e-mail: dc.currie@utoronto.ca).
Get access Rights & Permissions [Opens in a new window]

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.

Résumé

Les radiations rapides et récentes des lignées évolutives posent des défis aux systématiciens. En utilisant des membres du très divers complexe d'espèces Simulium arcticum Malloch, nous avons testé si le gène code-barre de la sous-unité cytochrome c oxydase I (COI) peut différencier entre espèces jumelles de mouches noires. Les membres du complexe S. arcticum sont monophylétiques par rapport à deux espèces morphologiques du groupe Simulium malyschevi Dorogostaisky et al. et deux espèces cryptiques de Simulium noelleri Friederichs. Parmi les cinq espèces analysées au sein du complexe S. arcticum, seul Simulium negativum Adler et al. est monophylétique. Aucun des autres membres du complexe ne peut être distingué par le code-barre COI. L'incapacité de différencier entre espèces jumelles du complexe S. arcticum provient (1) d'un partage d'haplotypes entre espèces et (2) du chevauchement entre les distributions des distances génétiques inter- et intraspécifiques. Les sources potentielles d'incongruité entre les données des codes-barres et la circonscription des espèces peuvent provenir d'une taxonomie imparfaite, d'une insuffisance d'information génétique, d'une séparation incomplète des lignées, et/ou d'introgression par hybridation. Nous écartons la possibilité d'une taxonomie imparfaite parce que des preuves chromosomiques, écologiques et géographiques soutiennent la validité des espèces reconnues au sein du complexe S. arcticum. Par conséquent, la nomenclature actuelle doit être maintenue en attendant une étude plus approfondie. Nous concluons qu'une ou plusieurs des trois autres sources d'incongruité pourrait être responsable de l'absence de monophylie réciproque entre espèces du complexe S. arcticum.

Type
Original Article
Information
The Canadian Entomologist , Volume 144 , Issue 2 , April 2012 , pp. 323 - 336
Copyright
Copyright © Entomological Society of Canada 2012 

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

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: 846–865.CrossRefGoogle Scholar
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].Google Scholar
Adler, P.H., Currie, D.C., Wood, D.M. 2004. The black flies (Simuliidae) of North America. Cornell University Press, New York.Google Scholar
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: 612–628.CrossRefGoogle Scholar
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: 508–524.CrossRefGoogle Scholar
Barrett, R.D.H., Hebert, P.D.N. 2005. Identifying spiders through DNA barcodes. Canadian Journal of Zoology, 83: 481–491.CrossRefGoogle Scholar
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. 117–132.Google Scholar
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: 252–271.CrossRefGoogle ScholarPubMed
Clement, M., Posada, D., Crandall, K. 2000. TCS: a computer program to estimate gene genealogies. Molecular Ecology, 9: 1657–1660.CrossRefGoogle ScholarPubMed
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: 245–257.CrossRefGoogle ScholarPubMed
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: 1–90.Google Scholar
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. 563–614.Google Scholar
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: 615–655.CrossRefGoogle Scholar
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: 55–61.CrossRefGoogle ScholarPubMed
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: 211–246.CrossRefGoogle Scholar
Felsenstein, J. 1985. Confidence limits on phylogenies: an approach using the bootstrap. Evolution, 39: 783–791.CrossRefGoogle ScholarPubMed
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: 3553–3566.CrossRefGoogle Scholar
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: 294–299.Google ScholarPubMed
Fredeen, F.J.H. 1969. Outbreaks of the black fly Simulium arcticum Malloch in Alberta. Quaestiones Entomologicae, 5: 341–372.Google Scholar
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: 397–423.CrossRefGoogle 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., deWaard, J.R. 2003a. Biological identifications through DNA barcodes. Proceedings of the Royal Society B: Biological Sciences, 270: 313–321.CrossRefGoogle ScholarPubMed
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: S96–S99.CrossRefGoogle ScholarPubMed
Hebert, P.D.N., Stoeckle, M.Y., Zemlak, T.S., Francis, C.M. 2004. Identification of birds through DNA barcodes. PLoS Biology, 2: 1657–1663.CrossRefGoogle ScholarPubMed
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: 847–863.CrossRefGoogle Scholar
Joy, D.A., Craig, D.A., Conn, J.E. 2007. Genetic variation tracks ecological segregation in Pacific island black flies. Heredity, 99: 452–459.CrossRefGoogle ScholarPubMed
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: 535–543.CrossRefGoogle ScholarPubMed
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: 314–318.CrossRefGoogle ScholarPubMed
Meyer, C.P., Paulay, G. 2005. DNA barcoding: error rates based on comprehensive sampling. PLoS Biology, 12: 2229–2238.Google Scholar
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: 1925–1933.CrossRefGoogle ScholarPubMed
Moritz, C., Cicero, C. 2004. DNA barcoding: promise and pitfalls. PLoS Biology, 10: 1529–1531.Google Scholar
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: 1293–1304.CrossRefGoogle ScholarPubMed
Nei, M., Kumar, S. 2000. Molecular evolution and phylogenetics. Oxford University Press, New York.CrossRefGoogle Scholar
Post, R.J., Flook, P.K., Millest, A.L. 1993. Methods for the preservation of insects for DNA studies. Biochemical Systematics and Ecology, 21: 85–92.CrossRefGoogle Scholar
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: 3989–4001.CrossRefGoogle ScholarPubMed
Rivera, J., Currie, D.C. 2009. Identification of Nearctic black flies using DNA barcodes (Diptera: Simuliidae). Molecular Ecology Resources, 9: 224–236.CrossRefGoogle ScholarPubMed
Rothfels, K.H. 1979. Cytotaxonomy of black flies (Simuliidae). Annual Review of Entomology, 24: 507–537.CrossRefGoogle Scholar
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. 67–83.Google Scholar
Rothfels, K.H. 1989. Speciation in black flies. Genome, 32: 500–509.CrossRefGoogle Scholar
Rothfels, K.H., Dunbar, R.W. 1953. The salivary gland chromosomes of the black fly Simulium vittatum Zett. Canadian Journal of Zoology, 31: 226–241.CrossRefGoogle Scholar
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: 511–520.CrossRefGoogle Scholar
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: 39–45.CrossRefGoogle Scholar
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: 32–43.Google Scholar
Shields, G.F., Procunier, W.S. 1982. A cytological description of sibling species of Simulium (Gnus) arcticum (Diptera: Simuliidae). Polar Biology, 1: 181–192.CrossRefGoogle Scholar
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: 235–246.CrossRefGoogle ScholarPubMed
Swofford, D.L. 2003. PAUP*: phylogenetic analysis using parsimony (*and other methods) version 4. Sinauer Associates, Sunderland, Massachusetts.Google Scholar
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: 619–633.CrossRefGoogle ScholarPubMed
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: 1847–1857.CrossRefGoogle ScholarPubMed