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Towards a new role for vector systematics in parasite control

Published online by Cambridge University Press:  17 June 2011

MAGDALENA ZAROWIECKI ,
JOSE R. LOAIZA  and
JAN E. CONN
MAGDALENA ZAROWIECKI*
Affiliation:
Dept. of Zoology, Natural History Museum, London SW7 5BD, UK
JOSE R. LOAIZA
Affiliation:
Programa Centroamericano de Maestría en Entomología, Vicerrectoría de Investigación y Postgrado, Universidad de Panamá, Republic of Panama Smithsonian Tropical Research Institute, Balboa Ancon, Unit 0948, Republic of Panama
JAN E. CONN
Affiliation:
Griffin Laboratory, The Wadsworth Centre, New York State Department of Health, Slingerlands, NY, USA Department of Biomedical Sciences, School of Public Health, State University of New York at Albany, Albany, New York 12222, USA
*
*Corresponding author: Dept. of Zoology, Natural History Museum, London SW7 5BD, U.K. Tel: 0044-7847129749. Fax: 0044-2079425229. E-mail: [email protected]
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Summary

Vector systematics research is being transformed by the recent development of theoretical, experimental and analytical methods, as well as conceptual insights into speciation and reconstruction of evolutionary history. We review this progress using examples from the mosquito genus Anopheles. The conclusion is that recent progress, particularly in the development of better tools for understanding evolutionary history, makes systematics much more informative for vector control purposes, and has increasing potential to inform and improve targeted vector control programmes.

Keywords

Species complexspeciationbiogeographyvector systematics
Type
Research Article
Information
Parasitology , Volume 138 , Special Issue 13: Systematics as a cornerstone of parasitology , November 2011 , pp. 1723 - 1729
Copyright
Copyright © Cambridge University Press 2011

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References

REFERENCES

Abhayawardana, T. A., Wijesuriya, S. R. E. and Dilrukshi, R. K. C. (1996). Anopheles subpictus complex: distribution of sibling species in Sri Lanka. Indian Journal of Malariology 33, 53–60.Google ScholarPubMed
Baimai, V., Andre, R. G., Harrison, B. A., Kijchalao, U. and Panthusiri, L. (1987). Crossing and chromosomal evidence for 2 additional sibling species within the Taxon Anopheles dirus Peyton and Harrison (Diptera, Culicidae) in Thailand. Proceedings of the Entomological Society of Washington 89, 157–166.Google Scholar
Baum, D. A. and Shaw, K. L. (1995). Geneaological perspectives on the species problem. In Experimental and Molecular Approaches to Plant Biosystematics (eds. Hoch, P. C., and Stephenson, A. G.), pp. 289–203. Missouri Botanical Garden.Google Scholar
Brochero, H. H. L., Li, C. and Wilkerson, R. C. (2007). A newly recognized species in the Anopheles (Nyssorhynchus) albitarsis complex (Diptera : Culicidae) from Puerto Carreno, Colombia. American Journal of Tropical Medicine and Hygiene 76, 1113–1117.CrossRefGoogle ScholarPubMed
Collins, F. H. and 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.CrossRefGoogle ScholarPubMed
Coyne, J. A. and Orr, A. H. (2004). Speciation. Sinauer Associates Inc., Sunderland.Google Scholar
Cummings, M. P., Neel, M. C. and Shaw, K. L. (2008). A genealogical approach to quantifying lineage divergence. Evolution 62, 2411–2422. doi: 10.1111/j.1558-5646.2008.00442.x.Google Scholar
Davis, J. I. and Nixon, K. C. (1992). Populations, genetic variation, and the delimitation of phylogenetic species. Systematic Biology 41, 421–435.CrossRefGoogle Scholar
della Torre, A., Costantini, C., Besansky, N. J., Caccone, A., Petrarca, V., Powell, J. R. and Coluzzi, M. (2002). Speciation within Anopheles gambiae – the glass is half full. Science 298, 115–117.CrossRefGoogle ScholarPubMed
della Torre, A., Merzagora, L., Powell, J. R. and Coluzzi, M. (1997). Selective introgression of paracentric inversions between two sibling species of the Anopheles gambiae complex. Genetics 146, 239–244.CrossRefGoogle ScholarPubMed
DeSalle, R., Egan, M. G. and Siddall, M. (2005). The unholy trinity: taxonomy, species delimitation and DNA barcoding. Philosophical Transactions of the Royal Society B: Biological Sciences 360, 1905–1916.CrossRefGoogle ScholarPubMed
Djogbenou, L., Chandre, F., Berthomieu, A., Dabire, R., Koffi, A., Alout, H. and Weill, M. (2008). Evidence of introgression of the ace-1R mutation and of the ace-1duplication in West African Anopheles gambiae s. s. PLoS ONE 3, e2172.Google Scholar
Dönitz, F. K. W. (1903). Beitrage zur Kenntniss der Anopheles. II. Mittheilung. Zeitschrift für Hygiene und Infektionskrankheiten 43, 215–238.Google Scholar
Doyle, J. J. (1995). The irrelevance of allele tree topologies for species delimitation, and a nontopological alternative. Systematic Biology 20, 574–588.Google Scholar
Drummond, A. J. and Rambaut, A. (2007). BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evolutionary Biology 7, 214.CrossRefGoogle ScholarPubMed
Dupanloup, I., Schneider, S. and Excoffier, L. (2002). A simulated annealing approach to define the genetic structure of populations. Molecular Ecology 11, 2571–2581.CrossRefGoogle ScholarPubMed
Ebach, M. C. and Holdrege, C. (2005). DNA barcoding is no substitute for taxonomy. Nature 434, 697.CrossRefGoogle ScholarPubMed
Emelianov, I., Marec, F. and Mallet, J. (2004). Genomic evidence for divergence with gene flow in host races of the larch budmoth. Proceedings of the Royal Society of London Series B-Biological Sciences 271, 97–105.CrossRefGoogle ScholarPubMed
Falush, D., Stephens, M. and Pritchard, J. K. (2003). Inference of population structure using multilocus genotype data: Linked loci and correlated allele frequencies. Genetics 164, 1567–1587.CrossRefGoogle ScholarPubMed
Foley, D. H., Bryan, J. H., Yeates, D. and Saul, A. (1998). Evolution and systematics of Anopheles: Insights from a molecular phylogeny of Australasian mosquitoes. Molecular Phylogenetics and Evolution 9, 262–275.Google Scholar
Gillies, M. T. and Coetzee, M. (1987). A Supplement to the Anophelinae of Africa South of the Sahara. The South African Institute for Medical Research, Johannesburg, South Africa.Google Scholar
Godfray, H. C. J. (2002). Challenges for taxonomy. Nature 417, 17–19.CrossRefGoogle ScholarPubMed
Good, D. A. and Wake, D. B. (1992). Geographical variation and speciation in the torrent salamanders of the genus Rhyacotriton (Caudata: Rhyacotritonidae). University of California Publications in Zoology 126, 1–91.Google Scholar
Green, C. A., Munstermann, L. E., Tan, S. G., Panyim, S. and Baimai, V. (1992). Population genetic evidence for species A, B, C and D of the Anopheles dirus complex in Thailand and enzyme electromorphs for their identification. Medical and Veterinary Entomology 6, 29–36.Google Scholar
Habtewold, T., Povelones, M., Blagborough, A. M. and Christophides, G. K. (2008). Transmission blocking immunity in the malaria on-vector mosquito Anopheles quadriannulatus species A. PLoS Pathogens 4, e1000070.CrossRefGoogle Scholar
Harbach, R. E. (2004). The classification of genus Anopheles (Diptera : Culicidae): a working hypothesis of phylogenetic relationships. Bulletin of Entomological Research 94, 537–553.CrossRefGoogle ScholarPubMed
Harbach, R. E. (2007). The Culicidae (Diptera): a review of taxonomy, classification and phylogeny. Zootaxa 1668, 591–638.CrossRefGoogle Scholar
Hebert, P. D. N., Stoeckle, M. Y., Zemlak, T. S. and Francis, C. M. (2004). Identification of birds through DNA Barcodes. PLoS Biology 2, e312.Google Scholar
Hey, J. and Nielsen, R. (2004). Multilocus methods for estimating population sizes, migration rates and divergence time, with applications to the divergence of Drosophila pseudoobscura and D. persimilis. Genetics 167, 747–760.CrossRefGoogle Scholar
Highton, R. (1990). Taxonomic treatment of genetically differentiated populations. Herpetologica 46, 114–121.Google Scholar
International Commission on Zoological Nomenclature (ICZN) (1999). International Code of Zoological Nomenclature, Fourth Edition. In International Trust for Zoological Nomenclature London, UK.Google Scholar
Klein, T. A., Lima, J. B. P., Tada, M. S. and Miller, R. (1991). Comparative susceptibility of Anopheline mosquitoes in Rondonia, Brazil to infection by Plasmodium vivax. American Journal of Tropical Medicine and Hygiene 45, 463–470.Google Scholar
Knowles, L. L. (2004). The burgeoning field of statistical phylogeography. Journal of Evolutionary Biology 17, 1–10.Google Scholar
Krzywinski, J., Wilkerson, R. C. and Besansky, N. J. (2001). Toward understanding Anophelinae (Diptera, Culicidae) phylogeny: insights from nuclear single-copy genes and the weight of evidence. Systematic Biology 50, 540–556.CrossRefGoogle ScholarPubMed
Kuhner, M., Yamato, J., Beerli, P., Smith, L., Rynes, E., Walkup, E., Li, C., Sloan, J., Colacurcio, P. and Felsenstein, J. (2005). LAMARC v 2.0, available from http://evolution.gs.washington.edu/lamarc.html. University of Washington.Google Scholar
Lamont, B. B., He, T., Enright, N. J., Krauss, S. L. and Miller, B. P. (2003). Anthropogenic disturbance promotes hybridization between Banksia species by altering their biology. Journal of Evolutionary Biology 16, 551–557.CrossRefGoogle ScholarPubMed
Lawniczak, M. K. N., Emrich, S. J., Holloway, A. K., Regier, A. P., Olson, M., White, B., Redmond, S., Fulton, L., Appelbaum, E., Godfrey, J., Farmer, C., Chinwalla, A., Yang, S.-P., Minx, P., Nelson, J., Kyung, K., Walenz, B. P., Garcia-Hernandez, E., Aguiar, M., Viswanathan, L. D., Rogers, Y.-H., Strausberg, R. L., Saski, C. A., Lawson, D., Collins, F. H., Kafatos, F. C., Christophides, G. K., Clifton, S. W., Kirkness, E. F. and Besansky, N. J. (2010). Widespread divergence between incipient Anopheles gambiae species revealed by whole genome sequences. Science 330, 512–514. doi: 10.1126/science.1195755.CrossRefGoogle ScholarPubMed
Li, C. and Wilkerson, R. C. (2005). Identification of Anopheles (Nyssorhynchus) albitarsis complex species (Diptera : Culicidae) using rDNA internal transcribed spacer 2-based polymerase chain reaction primes. Memorias do Instituto Oswaldo Cruz 100, 495–500.CrossRefGoogle ScholarPubMed
Lima, J. B. P., Valle, D. and Peixoto, A. A. (2004). Analysis of reproductive isolation between sibling species Anopheles albitarsis sensu stricto and Anopheles deaneorum, two malaria vectors belonging to the Albitarsis complex (Diptera : Culicidae). Journal of Medical Entomology 41, 888–893.Google Scholar
Linton, Y.-M., Dusfour, I., Howard, T. M., Ruiz, F., Manh, N. D., Trung, H. D., Sochanta, T., Coosemans, M. and Harbach, R. (2005). Anopheles (Cellia) epiroticus (Diptera:Culicidae), a new malaria vector species in the Southeast Asian Sundaicus complex. Bulletin of Entomological Research 95, 329–339.Google Scholar
Loaiza, J. R., Scott, M. E., Bermingham, E., Rovira, J. and Conn, J. E. (2010). Evidence for Pleistocene population divergence and expansion of Anopheles albimanus in southern Central America. American Journal of Tropical Medicine and Hygiene 82, 156–164. doi: 10.4269/ajtmh.2010.09-0423.Google Scholar
Manguin, S., Garros, C., Dusfour, I., Harbach, R. E. and Coosemans, M. (2008). Bionomics, taxonomy, and distribution of the major malaria vector taxa of Anopheles subgenus Cellia in Southeast Asia: An updated review. Infection, Genetics and Evolution 8, 489–503.CrossRefGoogle ScholarPubMed
Marquardt, W. (Ed.) (2004). Biology of Disease Vectors. Colorado State University, Fort Collins, USA.Google Scholar
Michalakis, Y. and Renaud, F. (2009). Malaria: Evolution in vector control. Nature 462, 298–300.CrossRefGoogle ScholarPubMed
Monaghan, M. T., Balke, M., Gregory, T. R. and 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.Google Scholar
Monteiro, F. A., Escalante, A. A. and Beard, C. B. (2001). Molecular tools and triatomine systematics: a public health perspective. Trends in Parasitology 17, 344–347.Google Scholar
Morgan, K., Linton, Y. M., Somboon, P., Saikia, P., Dev, V., Socheat, D. and Walton, C. (2010). Inter-specific gene flow dynamics during the Pleistocene-dated speciation of forest-dependent mosquitoes in Southeast Asia. Molecular Ecology 19, 2269–2285. doi: 10.1111/j.1365-294X.2010.04635.x.Google Scholar
Motoki, M. T., Wilkerson, R. C. and Sallum, M. A. M. (2009). The Anopheles albitarsis complex with the recognition of Anopheles oryzalimnetes Wilkerson and Motoki, n. sp and Anopheles janconnae Wilkerson and Sallum, n. sp (Diptera: Culicidae). Memorias do Instituto Oswaldo Cruz 104, 823–850.CrossRefGoogle Scholar
Neafsey, D. E., Lawniczak, M. K. N., Park, D. J., Redmond, S. N., Coulibaly, M. B., Traore, S. F., Sagnon, N., Costantini, C., Johnson, C., Wiegand, R. C., Collins, F. H., Lander, E. S., Wirth, D. F., Kafatos, F. C., Besansky, N. J., Christophides, G. K. and Muskavitch, M. A. T. (2010). SNP genotyping defines complex gene-flow boundaries among African malaria vector mosquitoes. Science 330, 514–517. doi: 10.1126/science.1193036.CrossRefGoogle ScholarPubMed
Nosil, P., Egan, S. P. and Funk, D. J. (2007). Heterogenous genomic differentiation between walking-stick ecotypes: ‘Isolation by adaptation’ and multiple roles for divergent selection. Evolution 62, 316–336.CrossRefGoogle ScholarPubMed
Nosil, P., Harmon, L. J. and Seehausen, O. (2009). Ecological explanations for (incomplete) speciation. Trends in Ecology & Evolution 24, 145–156.Google Scholar
O'Loughlin, S. M., Okabayashi, T., Honda, M., Kitazoe, Y., Kishino, H., Somboon, P., Sochantha, T., Nambanya, S., Saikia, P. K., Dev, V. and Walton, C. (2008). Complex population history of two Anopheles dirus mosquito species in Southeast Asia suggests the influence of Pleistocene climate change rather than human-mediated effects. Journal of Evolutionary Biology 21, 1555–1569. doi: 10.1111/j.1420-9101.2008.01606.x.Google Scholar
Pons, J., Barraclough, T. G., Gomez-Zurita, J., Cardoso, A., Duran, D. P., Hazell, S., Kamoun, S., Sumlin, W. D. and Vogler, A. P. (2006). Sequence-based species delimitation for the DNA taxonomy of undescribed insects. Systematic Biology 55, 595–609. doi: 10.1080/10635150600852011.CrossRefGoogle ScholarPubMed
Porter, A. H. (1990). Testing nominal species boundaries using gene flow statistics – The taxonomy of 2 hybridizing Admiral butterflies (Limenitis, Nymphalidae). Systematic Zoology 39, 131–147.CrossRefGoogle Scholar
Posada, D., Crandall, K. A. and Templeton, A. R. (2000). GeoDis: a program for the cladistic nested analysis of the geographical distribution of genetic haplotypes. Molecular Ecology 9, 487–488.CrossRefGoogle ScholarPubMed
Povoa, M. M., de Souza, R. T. L., Lacerda, R. N. L., Santa Rosa, E., Galiza, D., de Souza, J. R., Wirtz, R. A., Schlichting, C. D. and Conn, J. E. (2006). The importance of Anopheles albitarsis E and An. darlingi in human malaria transmission in Boa Vista, state of Roraima, Brazil. Memorias do Instituto Oswaldo Cruz 101, 163–168.CrossRefGoogle Scholar
Powell, J. R., Petrarca, V., della Torre, A., Caccone, A. and Coluzzi, M. (1999). Population structure, speciation, and introgression in the Anopheles gambiae complex. Parassitologia 41, 101–113.Google Scholar
Pritchard, J., Falush, D. and Stephens, M. (2002). Inference of population structure in recently admixed populations. American Journal of Human Genetics 71, 177–177.Google Scholar
Pritchard, J. K., Stephens, M. and Donnelly, P. (2000). Inference of population structure using multilocus genotype data. Genetics 155, 945–959.Google Scholar
Puillandre, N., Baylac, M., Boisselier, M. C., Cruaud, C. and Samadi, S. (2009). An integrative approach to species delimitation in Benthomangelia (Mollusca: Conoidea). Biological Journal of the Linnean Society 96, 696–708.CrossRefGoogle Scholar
Ramsey, J. M., Salinas, E., Rodriguez, M. H. and Beaudoin, R. L. (1994). Effects of transmission-blocking immunity on Plasmodium vivax infections in Anopheles albimanus populations. Journal of Parasitology 80, 88–92.CrossRefGoogle ScholarPubMed
Riehle, M. M., Guelbeogo, W. M., Gneme, A., Eiglmeier, K., Holm, I., Bischoff, E., Garnier, T., Snyder, G. M., Li, X., Markianos, K., Sagnon, N. F. and Vernick, K. D. (2011). A cryptic subgroup of Anopheles gambiae is highly susceptible to human malaria parasites. Science 331, 596–598. doi: 10.1126/science.1196759.CrossRefGoogle ScholarPubMed
Roy, L., Dowling, A. P. G., Chauve, C. M. and Buronfosse, T. (2009). Delimiting species boundaries within Dermanyssus Dugès, 1834 (Acari: Dermanyssidae) using a total evidence approach. Molecular Phylogenetics and Evolution 50, 446–470.CrossRefGoogle ScholarPubMed
Sahu, S. S. (1998). Comparative susceptibility of Anopheles subpictus from fresh and brackish water areas to Plasmodium falciparum infection. Acta Tropica 70, 1–7.Google Scholar
Sallum, M. A. M., Foster, P. G., Li, C., Sithiprasasna, R. and Wilkerson, R. C. (2007). Phylogeny of the Leucosphyrus group of Anopheles (Cellia) (Diptera: Culicidae) based on mitochondrial gene sequences. Annals of the Entomological Society of America 100, 27–35.CrossRefGoogle Scholar
Sallum, M. A. M., Peyton, E. L. and Wilkerson, R. C. (2005). Six new species of the Anopheles leucosphyrus group, reinterpretation of An. elegans and vector implications. Medical and Veterinary Entomology 19, 158–199.CrossRefGoogle ScholarPubMed
Sallum, M. A. M., Schultz, T. R., Foster, P. G., Aronstein, K., Wirtz, R. A. and Wilkerson, R. C. (2002). Phylogeny of Anophelinae (Diptera: Culicidae) based on nuclear ribosomal and mitochondrial DNA sequences. Systematic Entomology 27, 361–382.CrossRefGoogle Scholar
Schloss, P. D. and Handelsman, J. (2005). Introducing DOTUR, a computer program for Defining Operational Taxonomic Units and estimating species richness. Applied and Environmental Microbiology 71, 1501–1506.Google Scholar
Schloss, P. D. and Handelsman, J. (2006). Introducing SONS, a tool for Operational Taxonomic Unit-based comparisons of microbial community memberships and structures. Applied and Environmental Microbiology 72, 6773–6779.Google Scholar
Scotti-Saintagne, C., Mariette, S., Porth, I., Goicoechea, P. G., Barreneche, T., Bodénès, C., Burg, K. and Kremer, A. (2004). Genome scanning for interspecific differentiation between two closely related oak species (Quercus robur L. and Q. petraea (Matt.) Liebl.). Genetics 168, 1615–1626.Google Scholar
Seehausen, O. (2006). Conservation: Losing biodiversity by reverse speciation. Current Biology 16, R334–R337.Google Scholar
Sites, J. W. and Crandall, K. A. (1997). Testing species boundaries in biodiversity studies. Conservation Biology 11, 1289–1297.Google Scholar
Slotman, M. A., Mendez, M. M., della Torre, A., Dolo, G., Toure, Y. T. and Caccone, A. (2006). Genetic differentiation between the Bamako and Savanna chromosomal forms of Anopheles gambiae as indicated by amplified fragment length polymorphism analysis. American Journal of Tropical Medicine and Hygiene 74, 641–648.CrossRefGoogle ScholarPubMed
Sneath, P. H. A. and Sokal, R. R. (1962). Numerical Taxonomy. Nature 193, 855–860.CrossRefGoogle ScholarPubMed
Stockman, A. K., Beamer, D. A. and Bond, J. E. (2006). An evaluation of a GARP model as an approach to predicting the spatial distribution of non-vagile invertebrate species. Diversity and Distributions 12, 81–89.CrossRefGoogle Scholar
Stockman, A. K. and Bond, J. E. (2007). Delimiting cohesion species: extreme population structuring and the role of ecological interchangeability. Molecular Ecology 16, 3374–3392.Google Scholar
Suguna, S. G., Rathinam, K. G., Rajavel, A. R. and Dhanda, V. (1994). Morphological and chromosomal descriptions of new species in the Anopheles subpictus complex. Medical and Veterinary Entomology 8, 88–94.Google Scholar
Templeton, A. R. (1998). Nested clade analyses of phylogeographic data: testing hypotheses about gene flow and population history. Molecular Ecology 7, 381–397.CrossRefGoogle ScholarPubMed
Templeton, A. R. (2001). Using phylogeographic analyses of gene trees to test species status and processes. Molecular Ecology 10, 779–791.Google Scholar
Theobald (1901–1910). A Monograph of the Culicidae of the World. William Clowes & Son Ltd. London, UK 1–10.Google Scholar
Turner, T. L., Hahn, M. W. and Nuzhdin, S. V. (2005). Genomic islands of speciation in Anopheles gambiae. PLoS Biology 3, 1572–1578.CrossRefGoogle ScholarPubMed
Van Bortel, W., Trung, H., Thuan, L., Sochantha, T., Socheat, D., Sumrandee, C., Baimai, V., Keokenchanh, K., Samlane, P., Roelants, P., Denis, L., Verhaeghen, K., Obsomer, V. and Coosemans, M. (2008). The insecticide resistance status of malaria vectors in the Mekong region. Malaria Journal 7, 102.Google Scholar
Via, S. (2009). Natural selection in action during speciation. Proceedings of the National Academy of Sciences, USA 106, 9939–9946. doi: 10.1073/pnas.0901397106.Google Scholar
Vogler, A. P. and Monaghan, M. T. (2007). Recent advances in DNA taxonomy. Journal of Zoological Systematics and Evolutionary Research 45, 1–10.Google Scholar
Wakeley, J. and Hey, J. (1997). Estimating ancestral population parameters. Genetics 145, 847–855.CrossRefGoogle ScholarPubMed
White, G. B. (1985). Anopheles bwambae sp.n., a malaria vector in the Semliki Valley, Uganda, and its relationships with other sibling species of the An. gambiae complex (Diptera, Culicidae). Systematic Entomology 10, 501–522.CrossRefGoogle Scholar
Wiens, J. J. (2007). Species delimitation: New approaches for discovering diversity. Systematic Biology 56, 875–878.Google Scholar
Wiens, J. J. and Penkrot, T. A. (2002). Delimiting species using DNA and morphological variation and discordant species limits in spiny lizards (Sceloporus). Systematic Biology 51, 69–91.CrossRefGoogle ScholarPubMed
Wilkerson, R. C., Reinert, J. F. and Li, C. (2004). Ribosomal DNA ITS2 sequences differentiate six species in the Anopheles crucians Complex (Diptera: Culicidae). Journal of Medical Entomology 41, 392–401.Google Scholar
Wilson, E. O. (2004). Taxonomy as a fundamental discipline. Philosophical Transactions of the Royal Society B: Biological Sciences 359, 739.Google Scholar
Wu, C. I. and Ting, C. T. (2004). Genes and speciation. National Review of Genetics 5, 114–122.CrossRefGoogle ScholarPubMed
Zarowiecki, M. (2009). Speciation and species delineation in the Pyretophorus Series of Anopheles mosquitoes. In Dept. of Life Sciences, Vol. Ph.D. pp. 177. Ph.D. thesis, University of Manchester, Manchester.Google Scholar
Zarowiecki, M., Walton, C., Torres, E., McAlister, E., Htun, P. T., Sumrandee, C., Sochanta, T., Dinh, T. H., Ng, L. C. and Linton, Y.-M. (2011). Pleistocene genetic connectivity in a widespread, open-habitat-adapted mosquito in the Indo-Oriental region. Journal of Biogeography. doi: 10.1111/j.1365-2699.2011.02477.x.Google Scholar