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A combination of molecular and morphological approaches resolves species in the taxonomically difficult genus Procladius Skuse (Diptera: Chironomidae) despite high intra-specific morphological variation

Published online by Cambridge University Press:  10 March 2011

M.E. Carew*
Affiliation:
Victorian Centre for Aquatic Pollution Identification and Management (CAPIM), Department of Zoology, Bio21 Institute, The University of Melbourne, 3010, Australia
S.E. Marshall
Affiliation:
Victorian Centre for Aquatic Pollution Identification and Management (CAPIM), Department of Zoology, Bio21 Institute, The University of Melbourne, 3010, Australia
A.A. Hoffmann
Affiliation:
Victorian Centre for Aquatic Pollution Identification and Management (CAPIM), Department of Zoology, Bio21 Institute, The University of Melbourne, 3010, Australia
*
*Author for correspondence Fax: 61 03 8344 2279 E-mail: mecarew@unimelb.edu.au

Abstract

Molecular approaches for identifying aquatic macroinvertebrate species are increasingly being used but there is ongoing debate about the number of DNA markers needed to differentiate species accurately. Here, we use two mitochondrial genes (cytochrome oxidase I, cytochrome b) and a nuclear gene (carbamoylphosphate synthetase) to differentiate species variation within the taxonomically challenging chironomid genus Procladius from southern Australia, a genus which is important for pollution monitoring. The mitochondrial genes indicated cryptic species that were subsequently linked to morphological variation at the larval and pupal stage. Two species previously described based on morphological criteria were linked to molecular markers, and there was evidence for additional cryptic species. Each genetic marker provided different information, highlighting the importance of considering multiple genes when dissecting taxonomically difficult groups, particularly those used in pollution monitoring.

Type
Research Paper
Copyright
Copyright © Cambridge University Press 2011

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References

Britton, D.K. & McMahon, R.F. (2004) Environmentally and genetically induced shell-shape variation in the freshwater pond snail Physa (Physella) virgata (Gould, 1855). American Malacological Bulletin 19, 93100.Google Scholar
Brown, B.V. (2005) Malaise trap catches and the crisis in neotropical dipterology. American Entomologist 51, 180183.CrossRefGoogle Scholar
Buhay, J.E. & Crandall, K.A. (2009) Taxonomic revision of cave crayfish in the genus Cambarus, Subgenus Aviticambarus (Decapoda: Cambaridae) with descriptions of two new species, C. speleocoopi and C. laconensis, endemic to Alabama, USA. Journal of Crustacean Biology 29, 121134.CrossRefGoogle Scholar
Carew, M.E., Pettigrove, V. & Hoffmann, A.A. (2003) Identifying chironomids (Diptera: Chironomidae) for biological monitoring with PCR-RFLP. Bulletin of Entomological Research 93, 483490.CrossRefGoogle ScholarPubMed
Carew, M.E., Pettigrove, V. & Hoffmann, A.A. (2005) The utility of DNA markers in classical taxonomy: Using cytochrome oxidase I markers to differentiate Australian Cladopelma (Diptera : Chironomidae) midges. Annals of the Entomological Society of America 98, 587594.CrossRefGoogle Scholar
Carew, M.E., Pettigrove, V., Cox, R.L. & Hoffmann, A.A. (2007a) DNA identification of urban Tanytarsini chironomids (Diptera: Chironomidae). Journal of the North American Benthological Society 24, 586599.Google Scholar
Carew, M.E., Pettigrove, V., Cox, R.L. & Hoffmann, A.A. (2007b) The response of Chironomidae to sediment pollution and other environmental characteristics in urban wetlands. Freshwater Biology 52, 24442462.CrossRefGoogle Scholar
Cranston, P.S. (2000) Electronic identification guide to the Australian Chironomidae. Avaliable online at http://entomology.ucdavis.edu/chiropage/index.html (accessed 30 August 2010).Google Scholar
Cranston, P.S. & Martin, J. (1996) Australasian/Oceanian Diptera Catalogue – Web Version. Avaliable online at http://hbs.bishopmuseum.org/aocat/chiro.html (accessed 30 August 2010).Google Scholar
Dermott, R.M. (1991) Deformites in larval Procladius spp. and dominant Chironomini from the St Clair River. Hydrobiologia 219, 171185.CrossRefGoogle Scholar
DeSalle, R., Egan, M.G. & Siddall, M. (2005) The unholy trinity: Taxonomy, species delimitation and DNA barcoding. Philosophical Transactions of the Royal Society, Series B: Biological Sciences 360, 19051916.CrossRefGoogle ScholarPubMed
Ekrem, T., Willassen, E. & Stur, E. (2007) A comprehensive DNA sequence library is essential for identification with DNA barcodes. Molecular Phylogenetics and Evolution 43, 530542.CrossRefGoogle ScholarPubMed
Emery, V.J., Landry, J.F. & Eckert, C.G. (2009) Combining DNA barcoding and morphological analysis to identify specialist floral parasites (Lepidoptera: Coleophoridae: Momphinae: Mompha). Molecular Ecology Resources 9, 217223.CrossRefGoogle ScholarPubMed
Ferri, E., Barbuto, M., Bain, O., Galimberti, A., Uni, S., Guerrero, R., Ferte, H., Bandi, C., Martin, C. & Casiraghi, M. (2009) Integrated taxonomy: Traditional approach and DNA barcoding for the identification of filarioid worms and related parasites (Nematoda). Frontiers in Zoology 6, 1.CrossRefGoogle ScholarPubMed
Finston, T. (2007) Size, shape and development time are plastic traits in salt lake ostracods of the Mytilocypris mytiloides (Ostracoda:Cyprididae) species complex. Marine and Freshwater Research 58, 511518.CrossRefGoogle Scholar
Freeman, P. (1961) The Chironomidae (Diptera) of Australia. Australian Journal of Zoology 9, 611737.CrossRefGoogle Scholar
Guryev, V., Mararevitch, I., Blinov, A. & Martin, J. (2001) Phylogeny of the genus Chironomus (Diptera) inferred from DNA sequences of mitochondrial Cytochrome b and Cytochrome oxidase I. Molecular Phylogenetics and Evolution 19, 921.CrossRefGoogle ScholarPubMed
Hajibabaei, M., Singer, G., Clare, E. & Hebert, P. (2007) Design and applicability of DNA arrays and DNA barcodes in biodiversity monitoring. BMC Biology 5, 24.CrossRefGoogle ScholarPubMed
Hebert, P.N.D., Cywinska, A., Ball, S.L. & deWaard, J.R. (2003) Biological identification through DNA barcodes. Proceedings of the Royal Society of London, Series B: Biological Sciences 270, 313321.CrossRefGoogle ScholarPubMed
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, 1481214817.CrossRefGoogle ScholarPubMed
Kobayashi, T. (1998) Seasonal changes in body size and male genital structures of Procladius choreus (Diptera: Chironomidae: Tanypodinae). Aquatic Insects: International Journal of Freshwater Entomology 20, 165172.CrossRefGoogle Scholar
Martin, J., Guryev, V. & Blinov, A. (2002) Population variability in Chironomus (Camptochironomus) species (Diptera, Nemaocera) with a Holarctic distribution: Evidence of mitochondrial gene flow. Insect Molecular Biology 11, 387397.CrossRefGoogle ScholarPubMed
McKie, B.G. & Cranston, P.S. (2005) Size Matters: Systematic and ecological implications of allometry in the responses of chironomid midge morphological ratios to experimental temperature manipulations. Candaian Journal of Zoology 83, 553568.CrossRefGoogle Scholar
Meier, R., Shiyang, K., Vaidya, G. & Ng, P.K.L. (2006) DNA barcoding and taxonomy in Diptera: A tale of high intraspecific variability and low identification success. Systematic Biology 55, 715728.CrossRefGoogle ScholarPubMed
Meyer, C.P. & Paulay, G. (2005) DNA barcoding: Error rates based on comprehensive sampling. Plos Biology 3, 22292238.CrossRefGoogle ScholarPubMed
Moore, J.W. & Moore, I.A. (1978) Descriptions of larvae of 4 species of Procladius from Great Slave Lake (Chironomidae, Diptera). Canadian Journal of Zoology-Revue Canadienne De Zoologie 56, 20552057.CrossRefGoogle Scholar
Moulton, J.K. (2000) Molecular sequence data resolves basal divergences within Simuliidae (Diptera). Systematic Entomology 25, 95113.CrossRefGoogle Scholar
Moulton, J.K. & Wiegmann, B.M. (2004) Evolution and phylogenetic utility of CAD (rudimentary) among Mesozoic-aged Eremoneuran Diptera (Insecta). Molecular Phylogenetics and Evolution 31, 363378.CrossRefGoogle ScholarPubMed
Novo, M., Almodóvar, A., Fernández, R., Trigo, D. & Díaz Cosín, D.J. (2010) Cryptic speciation of hormogastrid earthworms revealed by mitochondrial and nuclear data. Molecular Phylogenetics and Evolution 56, 507512.CrossRefGoogle ScholarPubMed
Packer, L., Gibbs, J., Sheffield, C. & Hanner, R. (2009) DNA barcoding and the mediocrity of morphology. Molecular Ecology Resources 9, 4250.CrossRefGoogle ScholarPubMed
Page, T.J., Choy, S.C. & Hughes, J.M. (2005) The taxonomic feedback loop: symbiosis of morphology and molecules. Biology Letters 1, 139142.CrossRefGoogle ScholarPubMed
Pettigrove, V. (1989) Larval mouthpart deformities in Procladius paludicola Skuse (Diptera: Chironomidae) from the Murray and Darling rivers, Australia. Hydrobiologia 179, 111118.CrossRefGoogle Scholar
Pfenninger, M., Nowak, C., Kley, C., Steinke, D. & Streit, B. (2007) Utility of DNA taxonomy and barcoding for the inference of larval community structure in morphologically cryptic Chironomus (Diptera) species. Molecular Ecology 16, 19571968.CrossRefGoogle ScholarPubMed
Roback, S. (1982) The Tanypodinae (Diptera: Chironomidae) of Australia II. Proceedings of the Academy of Natural Sciences of Philadelphia 134, 80112.Google Scholar
Sharley, D.J., Pettigrove, V. & Parsons, Y.M. (2004) Molecular identification of Chironomus spp. (Diptera) for biomonitoring of aquatic ecosystems. Australian Journal of Entomology 43, 359365.CrossRefGoogle Scholar
Sinclair, C.S. & Gresens, S.E. (2008) Discrimination of Cricotopus species (Diptera: Chironomidae) by DNA barcoding. Bulletin of Entomological Research 98, 555563.CrossRefGoogle ScholarPubMed
Swofford, D.L. (2003) PAUP*: Phylogenetic analysis using parsimony (* and other methods), version 4.0b 10. (Sinauer Associates: Sunderland, Massachusetts, USA).Google Scholar
Thompson, J.D., Plewniak, F. & Poch, O. (1999) A comprehensive comparison of multiple sequence alignment programs. Nucleic Acids Research 27, 26822690.CrossRefGoogle ScholarPubMed
Tokeshi, M. (1995) Production Ecology. pp. 269296in Armitage, P.D., Cranston, P.S. & Pinder, L.C.V. (Eds) The Chironomidae: The Eecology and Biology of Non-Biting Midges. London, UK, Chapman and Hall.CrossRefGoogle Scholar
Townsend, K.R., Pettigrove, V.J., Carew, M.E. & Hoffmann, A.A. (2009) The effects of sediment quality on benthic macroinvertebrates in the River Murray, Australia. Marine and Freshwater Research 60, 7082.CrossRefGoogle Scholar
Wagner, R., Barták, M., Borkent, A., Courtney, G., Goddeeris, B., Haenni, J.-P., Knutson, L., Pont, A., Rotheray, G., Rozkošný, R., Sinclair, B., Woodley, N., Zatwarnicki, T. & Zwick, P. (2008) Global diversity of dipteran families (Insecta Diptera) in freshwater (excluding Simulidae, Culicidae, Chironomidae, Tipulidae and Tabanidae). Hydrobiologia 595, 489519.CrossRefGoogle Scholar
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, Series B: Biological Sciences 360, 18471857.CrossRefGoogle ScholarPubMed
Warwick, W.F. (1991) Indexing deformities in ligulae and antennae of Procladius larvae (Diptera, Chironomidae) – Application to contaminant-stressed environments. Canadian Journal of Fisheries and Aquatic Sciences 48, 11511166.CrossRefGoogle Scholar