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Geographical versus ecological isolation of closely related black flies (Diptera: Simuliidae) inferred from phylogeny, geography, and ecology

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Abstract

To investigate patterns of geographical and ecological separation among morphologically similar, closely related species of black flies, we integrated ecological, geographical, and phylogenetic information, based on multiple gene sequences, for 12 species in the subgenus Gomphostilbia in Thailand. Molecular characters supported the monophyly of the Simulium ceylonicum species group, but not of the Simulium batoense species group, suggesting that revisionary work is needed for the latter. Both ecological and geographical isolation of similar taxa were revealed. Stream velocity and altitude were among the principal ecological factors differing between closely related species. Most closely related species in the subgenus Gomphostilbia overlap geographically, suggesting the possibility of sympatric speciation driven by ecological divergence. Geographical isolation via dispersal also might have contributed to species divergence, while Pleistocene climate changes possibly influenced population genetic structure, demographic history, and speciation of some members of the subgenus.

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References

  • Adler, P. H. (1988). Ecology of black fly sibling species. In K. C. Kim & R. W. Merritt (Eds.), Black flies: ecology, population management, and annotated world list (pp. 63–76). University Park: Pennsylvania State University Press.

    Google Scholar 

  • Adler, P.H. & Crosskey. R.W. (2012). World blackflies (Diptera: Simuliidae): a comprehensive revision of the taxonomic and geographical inventory [2012]. http://entweb.clemson.edu/biomia/pdfs/blackflyinventory.pdf Accessed 25 April 2012.

  • Adler, P. H., & Kim, K. C. (1984). Ecological characterization of two sibling species, IIIL-1 and IS-7, in the Simulium vittatum complex (Diptera: Simuliidae). Canadian Journal of Zoology, 62, 1308–1315.

    Article  Google Scholar 

  • Adler, P. H., & McCreadie, J. W. (1997). The hidden ecology of black flies: Sibling species and ecological scale. American Entomologist, 43, 153–161.

    Google Scholar 

  • Boakye, D. A., Back, C., Fiasorgbor, G. K., Sib, A. P. P., & Coulibaly, Y. (1998). Sibling species distributions of the Simulium damnosum complex in the West African Onchocerciasis Control Programme area during the decade 1984–93, following intensive larviciding since 1974. Medical Veterinary and Entomology, 12, 345–358.

    Article  CAS  Google Scholar 

  • Cannon, C. H., & Manos, P. S. (2003). Phylogeography of the Southeast Asian stone oaks (Lithocarpus). Journal of Biogeography, 30, 211–226.

    Article  Google Scholar 

  • Carstens, B. C., & Knowles, L. L. (2007). Shifting distributions and speciation: Species divergence during rapid climatic change. Molecular Ecology, 16, 619–627.

    Article  PubMed  Google Scholar 

  • 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). Molecuar Phylogenetics and Evolution, 57, 245–257.

    Article  CAS  Google Scholar 

  • Coyne, J. A., & Orr, H. A. (2004). Speciation. Sunderland: Sinauer.

    Google Scholar 

  • Farris, J. S., Källersjö, M., Kluge, A. G., & Bult, C. (1995). Testing significance of incongruence. Cladistics, 10, 315–319.

    Article  Google Scholar 

  • Gathorne-Hardy, F. J., Syaukani, Davies, R. G., Eggleton, P., & Jones, D. T. (2002). Quaternary rainforest refugia in South-East Asia: Using termites (Isoptera) as indicators. Biological Journal of the Linnean Society, 75, 453–466.

    Article  Google Scholar 

  • Graham, C. H., Ron, S. R., Santos, J. C., & Schneider, C. J. (2004). Integrating phylogenetics and environmental niche models to explore speciation mechanisms in dendrobatid frogs. Evolution, 58, 1781–1793.

    PubMed  Google Scholar 

  • Haffer, J. (1969). Speciation in Amazonian forest birds. Science, 165, 131–137.

    Article  PubMed  CAS  Google Scholar 

  • Huelsenbeck, J. P., & Ronquist, F. R. (2001). MRBAYES: Bayesian inference of phylogeny. Bioinformatics, 17, 754–755.

    Article  PubMed  CAS  Google Scholar 

  • Jitklang, S., Kuvangkadilok, C., Baimai, V., Takaoka, H., & Adler, P. H. (2008). Cytogenetics and morphotaxonomy of the Simulium (Gomphostilbia) ceylonicum species group (Diptera: Simuliidae) in Thailand. Zootaxa, 1917, 1–28.

    Google Scholar 

  • Johnson, N. K., & Cicero, C. (2004). New mitochondrial DNA data affirm the importance of Pleistocene speciation in North American birds. Evolution, 58, 1122–1130.

    PubMed  Google Scholar 

  • Joy, D. A., & Conn, J. E. (2001). Molecular and morphological phylogenetic analysis of an insular radiation in Pacific black flies (Simulium). Systematic Biology, 50, 18–38.

    Article  PubMed  CAS  Google 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.

    Article  PubMed  CAS  Google Scholar 

  • Knowles, L. L. (2001). Did the Pleistocence glaciations promote divergence? Tests of explicit refugial models in montane grasshoppers. Molecular Ecology, 10, 691–701.

    Article  PubMed  CAS  Google Scholar 

  • Kuvangkadilok, C., & Takaoka, H. (2000). Taxonomic notes on Simuliidae (Diptera) from Thailand: description of a new species and new distributional records of nine known species. Japanese Journal of Tropical Medicine and Hygiene, 28, 167–175.

    Google Scholar 

  • Kuvangkadilok, C., Boonkemtong, C., & Phayuhasena, S. (1999). Distribution of the larvae of blackflies (Diptera: Simuliidae) at Doi Inthanon National Park, northern Thailand. The Southeast Asian Journal of Tropical Medicine and Public Health, 30, 328–337.

    PubMed  CAS  Google Scholar 

  • Kuvangkadilok, C., Lualon, U., & Baimai, V. (2008). Cytotaxonomy of Simulium siamense Takaoka and Suzuki (Diptera: Simuliidae) in Thailand. Genome, 51, 972–987.

    Article  PubMed  Google Scholar 

  • Mayr, E. (1963). Animal species and evolution. Cambridge: Harvard University Press.

    Google Scholar 

  • Mayr, E., & O’Hara, R. J. (1986). The biogeographic evidence supporting the Pleistocene forest refuge hypothesis. Evolution, 40, 55–67.

    Article  Google Scholar 

  • McCreadie, J. W., & Adler, P. H. (1998). Scale, time, space, and predictability: species distributions of preimaginal black flies (Diptera: Simuliidae). Oecologia, 114, 79–92.

    Article  Google Scholar 

  • McCreadie, J.W., Adler, P.H., Grillet, M.E. & Hamada, N. (2006). Sampling statistics in understanding distributions of black fly larvae (Diptera: Simuliidae). Acta Entomologica Serbica Supplement, 89–96.

  • Morgan, K., Linton, Y., Somboon, P., Saikia, P., Dev, V., Socheat, D., & 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.

    Article  PubMed  CAS  Google Scholar 

  • Morin, P. J. (1999). Community ecology. Malden: Blackwell Science.

    Google Scholar 

  • Nylander, J.A.A. (2004). MrModeltest 2.2. Program distributed by the author. Evolutionary Biology Centre, Uppsala University, Sweden.

  • O’Loughlin, S., Okabayashi, T., Honda, M., Kitazoe, Y., Kishino, H., Somboon, P., Sochantha, T., Nambanya, S., Saikia, P. K., Dev, V., & Walton, C. (2008). Complex population history of two Anopheles dirus mosquito species in South Asia suggests the influence of Pleistocene climate change rather than human-mediated effects. Journal of Evolutionary Biology, 21, 1555–1569.

    Article  PubMed  Google Scholar 

  • Orr, M. R., & Smith, T. B. (1998). Ecology and speciation. Trends in Ecology & Evolution, 13, 502–505.

    Article  CAS  Google Scholar 

  • Palmer, R. W., & Craig, D. A. (2000). An ecological classification of primary labral fans of filter feeding black fly (Diptera: Simuliidae) larvae. Canadian Journal of Zoology, 78, 199–218.

    Article  Google Scholar 

  • Peterson, A. T., Soberón, J., & Sánchez-Cordero, V. (1999). Conservatism of ecological niches in evolutionary time. Science, 285, 1265–1267.

    Article  PubMed  CAS  Google Scholar 

  • Phasuk, J., Chanpaisaeng, P., Adler, P. H., & Courtney, G. W. (2005). Chromosomal and morphological taxonomy of larvae of Simulium (Gomphostilbia) (Diptera: Simuliidae) in Thailand. Zootaxa, 1052, 49–60.

    Google Scholar 

  • Phayuhasena, S., Colgan, D. J., Kuvangkadilok, C., Pramual, P., & Baimai, V. (2010). Phylogenetic relationships among the black fly species (Diptera: Simuliidae) of Thailand based on mult ple gene sequences. Genetica, 138, 633–648.

    Article  PubMed  Google Scholar 

  • Posada, D. (2008). jModelTest: Phylogenetic model averaging. Molecular Biology and Evolution, 25, 1253–1256.

    Article  PubMed  CAS  Google Scholar 

  • Pramual, P., & Kuvangkadilok, C. (2009). Agricultural land use and black fly (Diptera: Simuliidae) species richness and species assemblages in tropical streams, Northeastern Thailand. Hydrobiologia, 625, 173–184.

    Article  Google Scholar 

  • Pramual, P., & Tangkawanit, U. (2008). A new species of Simulium (Gomphostilbia) (Diptera: Simuliidae) from northeastern Thailand. Medical Entomology and Zoology, 59, 297–303.

    Google Scholar 

  • Pramual, P., & Wongpakam, K. (2010). Seasonal variation of black fly (Diptera: Simuliidae) species diversity and community structure in tropical streams of Thailand. Entomological Science, 13, 17–28.

    Article  Google Scholar 

  • Pramual, P., & Wongpakam, K. (2011). Cytogenetics of Simulium siamense Takaoka and Suzuki, 1984 (Diptera: Simuliidae) in northeastern Thailand. Aquatic Insects, 33, 171–184.

    Article  Google 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.

    Article  PubMed  CAS  Google Scholar 

  • Pramual, P., Wongpakam, K., & Adler, P. H. (2011a). Cryptic biodiversity and phylogenetic relationships revealed by DNA barcoding of Oriental black flies in the subgenus Gomphostilbia (Diptera: Simuliidae). Genome, 54, 1–10.

    Article  PubMed  CAS  Google Scholar 

  • Pramual, P., Kongim, B., & Nanork, P. (2011b). Phylogeography of Simulium siamense Takaoka and Suzuki complex (Diptera: Simuliidae) in Thailand. Entomological Science, 14, 428–436.

    Article  Google Scholar 

  • Rambaut, A. & Drummond, A.J. (2004). Tracer 1.3. http://beastbioedacuk/Tracer. Accessed 27 May 2010.

  • Rodriguez, R., Oliver, J. L., Marin, A., & Medina, J. R. (1990). The general stochastic model of nucleotide substitution. Journal of Theoretical Biology, 142, 485–501.

    Article  PubMed  CAS  Google Scholar 

  • Rothfels, K. (1989). Speciation in black flies. Genome, 32, 500–509.

    Article  Google Scholar 

  • Schluter, D. (1998). Ecological causes of speciation. In D. Howard & S. Berlocher (Eds.), Endless forms: Species and speciation (pp. 114–129). New York: Oxford University Press.

    Google Scholar 

  • Schluter, D. (2001). Ecology and the origin of species. Trends in Ecology & Evolution, 16, 372–380.

    Article  Google Scholar 

  • Simon, C., Frati, F., Beckenbach, A., Crespi, B., Liu, H., & Flook, P. (1994). Evolution, weighting, and phylogenetic utility of mitochondrial gene sequences and a compilation of conserved polymerase chain reaction primers. Annals of the Entomological Society of America, 87, 651–701.

    CAS  Google Scholar 

  • Swofford, D. L. (2002). PAUP*: Phylogenetic analysis using parsimony (*and other methods). Version 4.b.10. Sunderland: Sinauer.

    Google Scholar 

  • Takaoka, H., & Choochote, W. (2004). A list of and keys to black flies (Diptera: Simuliidae) in Thailand. Tropical Medicine and Health, 32, 189–197.

    Article  Google Scholar 

  • Takaoka, H., & Davies, D. M. (1995). The black flies (Diptera: Simuliidae) of West Malaysia. Fukuoka: Kyushu University Press.

    Google Scholar 

  • Takaoka, H., & Suzuki, H. (1984). The blackflies (Diptera: Simuliidae) from Thailand. Japanese Journal of Sanitary Zoology, 36, 7–45.

    Google Scholar 

  • Takaoka, H., Srisuka, W., & Saeung, A. (2010). Description of the female of Simulium (Gomphostilbia) gombakense (Diptera: Simuliidae) from Thailand. Medical Entomology and Zoology, 61, 111–114.

    Google Scholar 

  • Takaoka, H., Sofian-Azirun, M., Hashim, R., & Ya’cob, Z. (2011). Two new species of Simulium (Gomphostilbia) (Diptera: Simuliidae) from Peninsular Malaysia, with keys to Peninsular Malaysian members of the Simulium ceylonicum species-group. ZooKeys, 118, 53–74.

    Article  PubMed  Google Scholar 

  • Tamura, K., & Nei, M. (1993). Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Molecular Biology and Evolution, 10, 512–526.

    PubMed  CAS  Google Scholar 

  • Thanwisai, A., Kuvangkadilok, C., & Baimai, V. (2006). Molecular phylogeny of black flies (Diptera:Simuliidae) from Thailand, using ITS2 rDNA. Genetica, 128, 177–204.

    Article  PubMed  CAS  Google Scholar 

  • Thompson, J. D., Gibson, T. J., Plewniak, F., Jeanmougin, F., & Higgins, D. G. (1997). The ClustalX windows interface: Flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research, 24, 4876–4882.

    Article  Google Scholar 

  • Weins, J. J. (2004). Speciation and ecology revisited: phylogenetic niche conservatism and the origin of species. Evolution, 58, 193–197.

    Google Scholar 

  • Woodruff, D. S. (2003). Neogene marine transgressions, palaeogeography and biogeographic transitions on the Thai-Malay Peninsula. Journal of Biogeography, 30, 551–567.

    Article  Google Scholar 

  • Zhang, Y. (2006). Balancing food availability and hydrodynamic constraint: Phenotypic plasticity and growth in Simulium noelleri blackfly larvae. Oecologia, 147, 39–46.

    Article  PubMed  Google Scholar 

  • Zhang, Y., & Malmqvist, B. (1996). Relationships between labral fan morphology, body size and habitat in North Swedish blackfly larvae (Diptera: Simuliidae). Biological Journal of the Linnean Society, 59, 261–280.

    Google Scholar 

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Acknowledgments

This work was supported financially by the Thailand Research Fund, Commission on Higher Education and Mahasarakham University (MRG5380053). We thank J. Dodgson (Mahasarakham University, Thailand) for comments on an earlier version of the manuscript.

Conflict of interest

The authors declare that they have no conflict of interest.

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Authors and Affiliations

  1. Department of Biology, Faculty of Science, Mahasarakham University, Maha Sarakham, 44150, Thailand

    Pairot Pramual

  2. Department of Biology, Faculty of Science, Mahidol University, Rama VI Road, Phayathai, Bangkok, 10400, Thailand

    Chaliow Kuvangkadilok

  3. Conservation Biology Program, Division of Biological and Natural Resource Sciences, Mahidol University, Saiyok, Kanchanaburi Campus, Kanchanaburi, 71150, Thailand

    Sanae Jitklang

  4. Department of Plant Science and Agricultural Resources, Faculty of Agriculture, Khonkaen University, Khonkaen, 40002, Thailand

    Ubon Tangkawanit

  5. Entomology Program, School of Agricultural, Forest, and Environmental Sciences, Clemson University, Clemson, SC, 29634-0310, USA

    Peter H. Adler

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  1. Pairot Pramual
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Pramual, P., Kuvangkadilok, C., Jitklang, S. et al. Geographical versus ecological isolation of closely related black flies (Diptera: Simuliidae) inferred from phylogeny, geography, and ecology. Org Divers Evol 12, 183–195 (2012). https://doi.org/10.1007/s13127-012-0092-4

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