Skip to main content
Log in

Phylogenetic relationships among the black fly species (Diptera: Simuliidae) of Thailand based on multiple gene sequences

  • Published:
Genetica Aims and scope Submit manuscript

Abstract

Simulium is a very speciose genus of the black fly family Simuliidae that includes many important pests of humans and animals. Cytotaxonomic and morphological studies have made substantial progress in Simulium systematics. 16S rRNA and ITS-1 DNA sequence studies have assisted this progress. Intensive multi-gene molecular systematic investigations will, however, be required for a comprehensive understanding of the genus’ taxonomy and evolution. Our research was conducted to investigate the relationships of Thai Simulium at the subgeneric, species group and species levels. We also examined the possibility of using mitochondrial DNA sequences to facilitate Simulium species identification. Data were collected from three mitochondrial genes (COI, ND4 and 16S rRNA) and two segments of the nuclear 28S ribosomal RNA (the D1 to D2 and the D4 expansion regions). The subgenera Simulium and Gomphostilbia were monophyletic in most analyses. Nevermannia included Montisimulium but was otherwise monophyletic in multigene analyses. In most analyses, Simulium and Nevermannia were more closely related to each other than to Gomphostilbia which was usually basal. Species groups were generally monophyletic. Within Gomphostilbia, however, the batoense species group was always paraphyletic to the other two species groups found in Thailand. Three species groups in Simulium were not monophyletic. The tendency to gill filament number reduction for some species groups in the subgenus Simulium was associated with a derived position in multigene analyses. Most species were monophyletic with two exceptions that probably represent species complexes and will present difficulties for rapid mitochondrial DNA identification.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Adler PH (2005) Black flies, the Simuliidae. In: Marquardt WC (ed) Biology of disease vectors, 2nd edn. Elsevier, San Diego, pp 127–140

    Google Scholar 

  • Adler PH, Crosskey RW (2009) World blackflies (Diptera: Simuliidae): a fully revised edition of the taxonomic and geographical inventory. Available at: http://entweb.clemson.edu/biomia/pdfs/blackflyinventory.pdf

  • Adler PH, Currie DC, Wood DM (2004) The black flies (Simuliidae) of North America. Cornell University Press, Ithaca

    Google Scholar 

  • Basáñez M-G, Boussinesq M (1999) Population biology of human onchocerciasis. Philos Trans R Soc Lond B 354:809–826

    Article  Google Scholar 

  • Bedo DG (1977) Cytogenetics and evolution of Simulium ornatipes Skuse (Diptera: Simuliidae). I. Sibling speciation. Chromosoma 64:37–65

    Article  Google Scholar 

  • Bedo DG (1979) Cytogenetics and evolution of Simulium ornatipes Skuse (Diptera: Simuliidae). II. Temporal variation in chromosomal polymorphism and homosequential sibling species. Evolution 33:296–308

    Article  Google Scholar 

  • Boakye DA (1993) A pictorial guide to the chromosomal identification of members of the Simulium damnosum Theobald complex in West Africa with particular reference to the Onchocerciasis Control Programme Area. Trop Med Parasitol 44:233–244

    Google Scholar 

  • Brockhouse CL, Vajime CG, Marin R, Tanguay RM (1993) Molecular identification of onchocerciasis vector sibling species in black flies (Diptera: Simuliidae). Biochem Biophys Res Commun 194:628–634

    Article  CAS  PubMed  Google Scholar 

  • Clary DO, Wolstenholme DR (1985) The mitochondrial DNA molecule of Drosophila yakuba: nucleotide sequence, gene organization, and genetic code. J Mol Evol 22:252–271

    Article  CAS  PubMed  Google Scholar 

  • Colgan DJ, Ponder WF, Eggler PE (2000) Gastropod evolutionary rates and phylogenetic relationships assessed using partial 28S rDNA and histone H3 sequences. Zool Scr 29:29–63

    Article  Google Scholar 

  • Collins FH, Mendez MA, Rasmussen MO, Mehaffey PC, Besanky NJ, Finnerty V (1987) A ribosomal RNA gene probe differentiates member species of the Anopheles gambiae complex. Am J Trop Med Hyg 37:37–41

    CAS  PubMed  Google Scholar 

  • Craig DA, Currie DC, Joy DA (2001) Geographical history of the central-western pacific black fly subgenus Inseliellum (Diptera: Simuliidae: Simulium) based on a reconstructed phylogeny of the species, hot-spot archipelagoes and hydrological considerations. J Biogeogr l28:1101–1127

    Article  Google Scholar 

  • Crosskey RW (1981) Simuliid taxonomy. In: Laird M (ed) Blackflies: the future for biological methods in integrated control. Academic Press, London, pp 3–18

    Google Scholar 

  • Crosskey RW (1990) The natural history of black flies. Wiley, London

    Google Scholar 

  • Currie DC, Adler PH (2008) Global diversity of black flies (Diptera: Simuliidae). Hydrobiologia 595:469–475

    Article  Google Scholar 

  • Edwards FW (1928) Diptera Nematocera from the Federated Malay States Museums. J Fed Malay Mus 14:1–139

    Google Scholar 

  • Edwards FW (1934) Deutsche Limnologische Sunda-Expedition: the Simuliidae (Diptera) of java and sumatra. Arch Hydrobiol Stuttg Suppl 13:92–138

    Google 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. Mol Mar Biol Biotechnol 3:294–299

    CAS  PubMed  Google Scholar 

  • Hall R (1998) The plate tectonics of cenozoic SE Asia and the distribution of land and sea. In: Hall R, Holloway JD (eds) Biogeography and geological evolution of SE Asia. Backhuys, Leiden, pp 99–132

    Google Scholar 

  • Hall R (2002) Cenozoic geologic and plate tectonic evolution of SE Asia and the SW Pacific: computer-based reconstructions, model and animations. J Asian Earth Sci 20:353–431

    Article  Google Scholar 

  • Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  • Han HY, McPheron BA (1997) Molecular phylogenetic study of Tephritidae (Insecta: Diptera) using partial sequences of the mitochondrial 16S ribosomal DNA. Mol Phylogenet Evol 7:17–32

    Article  CAS  PubMed  Google Scholar 

  • Hebert PDN, Cywinska A, Ball SL, deWaard JR (2003) Biological identifications through DNA barcodes. Proc R Soc Lond B 270:313–321

    Article  CAS  Google Scholar 

  • Higazi TB, Boakye DA, Wilson MD, Mahmoud BM, Baraka OZ, Mukhtar MM, Unnasch TR (2001) Cytotaxonomic and molecular analysis of Simulium (Edwardsellum) damnosum sensu lato (Diptera: Simuliidae) from Abu Hamed, Sudan. J Med Entomol 37:547–553

    Google Scholar 

  • Huelsenbeck JP, Ronquist FR (2001) MRBAYES: Bayesian inference of phylogeny. Bioinformatics 17:754–755

    Article  CAS  PubMed  Google Scholar 

  • Jitklang S, Kuvangkadilok C (2007) A new species of Simulium (Gomphostilbia) (Diptera: Simuliidae) from southern Thailand, with description of its polytene chromosomes. Stud Dipterol 14:369–375

    Google Scholar 

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

    Google Scholar 

  • Kjer KM, Baldridge GD, Fallon AM (1994) Mosquito large subunit ribosomal RNA: simultaneous alignment of primary and secondary structure. Biochem Biophys Acta 1217:147–155

    CAS  PubMed  Google Scholar 

  • Krüger A, Hennings IC (2006) Molecular phylogenetics of blackflies of the Simulium damnosum complex and cytophylogenetic implications. Mol Phylogenet Evol 39:83–90

    Article  Google Scholar 

  • Krüger A, Gelhaus A, Garms R (2000) Molecular identification and phylogeny of East African Simulium damnosum s.l. and their relationship with West African species of the complex (Diptera: Simuliidae). Insect Mol Biol 9:101–108

    Article  PubMed  Google Scholar 

  • Kuvangkadilok C, Boonkemtong C, Phayuhasena S (1998) C-banding in polytene chromosomes of six Simulium species (Diptera: Simuliidae) from Doi Inthanon National Park, northern Thailand. J Sci Soc Thail 24:215–230

    Article  Google Scholar 

  • Kuvangkadilok C, Phayuhasena S, Boonkemtong C (1999a) Larval polytene chromosomes of five species of blackflies (Diptera: Simuliidae) from Doi Inthanon National Park, northern Thailand. Cytologia 64:197–207

    Google Scholar 

  • Kuvangkadilok C, Phayuhasena S, Baimai V (1999b) Population cytogenetic studies on Simulium feuerborni Edwards (Diptera: Simuliidae) from northern Thailand. Genome 42:80–86

    Article  Google Scholar 

  • Kuvangkadilok C, Boonkemtong C, Phayuhasena S, Baimai V (2003) Larval polytene chromosomes of black flies (Simulium) from Thailand. I. Comparison among five species in the subgenus Gomphostilbia Enderlein. Genetica 118:69–81

    Article  CAS  PubMed  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 

  • Lunt DH, Zhang DX, Szymura JM, Hewitt GM (1996) The insect cytochrome oxidase I gene: evolutionary patterns and conserved primers for phylogenetic studies. Insect Mol Biol 5:153–165

    Article  CAS  PubMed  Google Scholar 

  • Maddison WP, Maddison DR (1992) MacClade: analysis of phylogeny and character evolution. Vers 3. Sinauer, Sunderland

    Google Scholar 

  • McArthur AG, Koop BF (1999) Partial 28S rDNA sequences and the antiquity of the hydrothermal vent endemic gastropods. Mol Phylogenet Evol 13:255–274

    Article  CAS  PubMed  Google Scholar 

  • Moulton JK (2000) Molecular sequence data resolves basal divergences within Simuliidae (Diptera). Syst Entomol 25:95–113

    Article  Google Scholar 

  • Moulton JK (2003) Can the current molecular arsenal adequately track rapid divergence events within Simuliidae (Diptera)? Mol Phylogenet Evol 27:45–57

    Article  CAS  PubMed  Google Scholar 

  • Otsuka Y, Aoki C, Saito K, Hadi UK, Takaoka H (2001) Phylogenetic analyses of a blackfly subgenus Simulium (Nevermannia) based on mitochondrial 16S ribosomal RNA gene sequences. Jpn J Trop Med Hyg 29:261–266

    Google Scholar 

  • Otsuka Y, Takaoka H, Aoki C, Choochote W (2003) Phylogenetic analysis of the subgenus Himalayum within the genus Simulium s.l. (Diptera: Simuliidae) using mitochondrial 16S rRNA gene sequences. Med Entomol Zool 54:113–120

    CAS  Google Scholar 

  • Ottesen EA, Hooper PJ, Bradley M, Biswas G (2008) The global programme to eliminate lymphatic filariasis: health impact after 8 years. PLOS Negl Trop Dis 2 (10). doi: 10.1371/journal.pntd.0000317. Available at http://www.plosntds.org/article/info:doi%2F10.1371%2Fjournal.pntd.0000317

  • Pham XD (1998) New records of six black fly species (Diptera: Simuliidae) from Vietnam. Med Entomol Zool 49:121–123

    Google Scholar 

  • Pham XD (1999) Additional record of three black fly species from Vietnam (Diptera: Simuliidae). Med Entomol Zool 50:335–336

    Google Scholar 

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

    Google Scholar 

  • Porter CH, Collins FH (1996) Phylogeny of Nearctic members of the Anopheles aculipennis species group derived from the D2 variable region of 28S ribosomal RNA. Mol Phylogenet Evol 6:178–188

    Article  CAS  PubMed  Google Scholar 

  • Pramual P, Tangkawanit U (2008) A new species of Simulium (Gomphostilbia) (Diptera: Simuliidae) from Northeastern Thailand. Med Entomol Zool 59:297–303

    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. Mol Ecol 14:3989–4001

    Article  CAS  PubMed  Google Scholar 

  • Procunier WS, Muro AI (1993) Cytotaxonomy of the Simulium damnosum complex from central and northeastern Tanzania. Genome 36:112–130

    Article  CAS  PubMed  Google Scholar 

  • Pruess KP, Zhu X, Powers TO (1992) Mitochondrial transfer RNA genes in a black fly, Simulium vittatum (Diptera: Simuliidae), indicate long divergence from mosquito (Diptera: Culicidae) and fruit fly (Diptera: Drosophilidae). J Med Entomol 29:644–651

    CAS  PubMed  Google Scholar 

  • Raes J, Van de Peer Y (1999) ForCon: a software tool for the conversion of sequence alignments. Available at: http://www.es.embnet.org/embnet_common/embnet.news/vol6_1/ForCon/body_forcon.html

  • Rambaut A, Drummond AJ (2004) Tracer 1.3. Available from http://beastbioedacuk/Tracer

  • Rothfels RH (1979) Cytotaxonomy of black flies (Simuliidae). Ann Rev Entomol 24:507–539

    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. Ann Entomol Soc Am 87:651–701

    CAS  Google Scholar 

  • Soto SIU, Lehmann T, Bowton ED, Vélez BID, Porter CH (2001) Speciation and population structure in the morphospecies Lutzomyia longipalpis (Lutz & Neiva) as derived from the mitochondrial ND4 gene. Mol Phylogenet Evol 18:84–93

    Article  CAS  PubMed  Google Scholar 

  • Summer SLM (1911) Note from Entomological Department of the London School of Tropical Medicine No. II. Description of a new species of Simulium from the Siamese hills. Ann Mag Nat Hist 8:586–588

    Google Scholar 

  • Swofford DL (2002) PAUP*: phylogenetic analysis using parsimony (*and other methods), vers. 4.b.10. Sinauer, Sunderland

    Google Scholar 

  • Takaoka H (1989) Notes on blackflies (Diptera: Simuliidae) from Myanmar (formerly Burma). Jpn J Trop Med Hyg 17:243–257

    Google Scholar 

  • Takaoka H (1996) The geographical distribution of the genus Simulium Latreille in the Oriental and Australasian regions. Jpn J Trop Med Hyg 24:113–124

    Google Scholar 

  • Takaoka H, Adler PH (1997) A new subgenus, Simulium (Daviesellum), and a new species, S. (D.) courtneyi, (Diptera: Simuliidae) from Thailand and Peninsular Malaysia. Jpn J Trop Med Hyg 25:17–27

    Google Scholar 

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

    Article  Google Scholar 

  • Takaoka H, Choochote W (2005a) Two new species of Simulium (Montisimulium) (Diptera: Simuliidae) from Thailand. Med Entomol Zool 56:21–34

    Google Scholar 

  • Takaoka H, Choochote W (2005b) A new subgenus and a new species of Simulium s. l. (Diptera: Simuliidae) from Thailand. Med Entomol Zool 56:33–41

    Google Scholar 

  • Takaoka H, Choochote W (2006a) A new species of the subgenus Simulium (Asiosimulium) (Diptera: Simuliidae) from Thailand. Med Entomol Zool 57:45–48

    Google Scholar 

  • Takaoka H, Choochote W (2006b) Description of adults of Simulium (Simulium) baimaii from Thailand (Diptera: Simuliidae) and its assignment to the malyschevi species-group. Med Entomol Zool 57:49–53

    Google Scholar 

  • Takaoka H, Choochote W (2006c) A new species of the griseifrons species-group of Simulium (Simulium) (Diptera: Simuliidae) in northern Thailand. Med Entomol Zool 57:115–124

    Google Scholar 

  • Takaoka H, Choochote W (2006d) A new species of Simulium (Nevermannia) from northern Thailand (Diptera: Simuliidae). Med Entomol Zool 57:83–92

    Google Scholar 

  • Takaoka H, Choochote W (2006e) A new species of Simulium (Gomphostilbia) (Diptera: Simuliidae) from northern Thailand. Med Entomol Zool 57:229–233

    Google Scholar 

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

    Google Scholar 

  • Takaoka H, Kuvangkadilok C (1999) Four new species of black flies (Diptera: Simuliidae) from Thailand. Jpn J Trop Med Hyg 4:497–509

    Google Scholar 

  • Takaoka H, Saito K (1996) A new species and new records of black flies (Diptera: Simuliidae) from Thailand. Jpn J Trop Med Hyg 24:163–169

    Google Scholar 

  • Takaoka H, Suzuki H (1984) The blackflies (Diptera: Simuliidae) from Thailand. Jpn J Sanit Zool 36:7–45

    Google Scholar 

  • Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599

    Article  CAS  PubMed  Google Scholar 

  • Tang J, Toè L, Back C, Unnasch TR (1995a) Mitochondrial alleles of Simulium damnosum sensu lato infected with Onchocerca volvulus. Int J Parasitol 25:1251–1254

    Article  CAS  PubMed  Google Scholar 

  • Tang J, Toè L, Back C, Zimmerman PA, Pruess K, Unnasch TR (1995b) The Simulium damnosum species complex: phylogenetic analysis and molecular identification based upon mitochondrially encoded gene sequences. Insect Mol Biol 4:79–88

    Article  CAS  PubMed  Google Scholar 

  • Tang J, Pruess K, Cupp EW, Unnasch TR (1996a) Molecular phylogeny and typing of black flies (Diptera: Simuliidae) that serve as vectors of human or bovine onchocerciasis. Med Vet Entomol 10:228–234

    Article  CAS  PubMed  Google Scholar 

  • Tang J, Toè L, Back C, Unnasch TR (1996b) Intra-specific heterogeneity of the rDNA internal transcribed spacer in the Simulium damnosum (Diptera: Simuliidae) complex. Mol Biol Evol 13:244–252

    CAS  PubMed  Google Scholar 

  • Tangkawanit U, Kuvangkadilok C, Baimai V, Adler PH (2009) Cytosystematics of the Simulium tuberosum group (Diptera: Simuliidae) in Thailand. Zool J Linn Soc Lond 155:289–315

    Article  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  CAS  PubMed  Google Scholar 

  • Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 24:4876–4882

    Article  Google Scholar 

  • Vajime CG, Dunbar RW (1975) Chromosomal identification of eight species of the subgenus Edwardsellum near and including Simulium (Edwardsellum) damnosum Theobald (Diptera: Simuliidae). Trop Med Parasitol 26:111–138

    CAS  Google Scholar 

  • Xiong B, Kocher TD (1991) Comparison of mitochondrial DNA sequences of seven morphospecies of black flies (Diptera: Simuliidae). Genome 34:306–311

    CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We thank Professor Hiroyuki Takaoka of the Department of Infectious Disease Control, Faculty of Medicine, Oita Medical University, Oita, Japan for advice about larval identification and with the clarification of taxonomic issues. We thank Sue Livingston and Denis O’Meally of the Australian Museum for electrophoresis of the sequencing reactions on an automatic capillary sequencer. This research was supported by the Thailand Research Fund (RDG 4530034), the TRF/BIOTEC Special Program for Biodiversity Research and Training grant BRT R_250003 and the Australian Museum.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Donald J. Colgan.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Phayuhasena, S., Colgan, D.J., Kuvangkadilok, C. et al. Phylogenetic relationships among the black fly species (Diptera: Simuliidae) of Thailand based on multiple gene sequences. Genetica 138, 633–648 (2010). https://doi.org/10.1007/s10709-010-9437-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10709-010-9437-0

Keywords

Navigation