Abstract
Gasterophilus spp. (Diptera: Gasterophilidae) has a worldwide distribution; however, no complete mitochondrial (mt) genome data is available for Diptera which has greatly impeded population genetics, phylogenetics, and systematics studies in Gasterophilidae. Mt genome is known to provide genetic markers for investigations in these areas, but complete mt genomic datasets have been lacking for many Gasterophilidae species. Herein, we present the complete mt genome of the third-stage larvae (L3) of Gasterophilus intestinalis from the stomach wall of naturally infected horses in Heilongjiang province (HLJ) and Xinjiang Uygur Autonomous Region (XJ), China. The complete mt genome of G. intestinalis was 15,687 bp (HLJ) and 15,660 bp (XJ) in length and consists of 37 genes, including 13 genes for proteins, 22 genes for tRNA, and 2 genes for rRNA. The gene arrangement is the same as those of Oestroidae species. Phylogenetic analyses using concatenated amino acid sequences of 12 protein-coding genes by Bayesian inference (BI) and maximum likelihood (ML), suggested that the families Gasterophilidae and Oestroidae were more closely related than to Tachinidae. The mt genome of G. intestinalis represents the first mt genome of any member of the family Gasterophilidae. These data provide novel mtDNA markers for studying the molecular epidemiology and population genetics of the G. intestinalis and its congeners.
Similar content being viewed by others
References
Abascal F, Zardoya R, Posada D (2005) ProtTest: selection of best-fit models of protein evolution. Bioinformatics 21:2104–2105
Anderson JR (2005) Oestrid myiasis of humans. In: Colwell DD, Hall MJR, Scholl PJ (eds) The oestrid flies: biology, host-parasite relationships, impact and management. CAB International, Oxford
Beard CB, Hamm DM, Collins FH (1993) The mitochondrial genome of the mosquito Anopheles gambiae: DNA sequence, genome organization, and comparisons with mitochondrial sequences of other insects. Insect Mol Biol 2:103–124
Boore JL (1999) Animal mitochondrial genomes. Nucleic Acids Res 27:1767–1780
Burland TG (2000) DNASTAR’s Lasergene sequence analysis software. Methods Mol Biol 132:71–91
Cameron SL, Barker SC, Whiting MF (2006) Mitochondrial genomics and the relationships and validity of the new insect order Mantophasmatodea. Mol Phylogenet Evol 38:274–279
Cheng T, Liu GH, Song HQ, Lin RQ, Zhu XQ (2016) The complete mitochondrial genome of the dwarf tapeworm Hymenolepis nana-a neglected zoonotic helminth. Parasitol Res. In press.
Clary DO, Wolstenholme DR (1985) The mitochondrial DNA molecular of Drosophila yakuba: nucleotide sequence, gene organization, and genetic code. J Mol Evol 22:252–271
Cogley TP, Cogley MC (1999) Inter-relationship between Gasterophilus larvae and the horse’s gastric and duodenal wall with special reference to penetration. Vet Parasitol 86:127–142
Dart AJ, Hutchins DR, Begg AP (1987) Suppurative splenitis and peritonitis in a horse after gastric ulceration caused by larvae of Gasterophilus intestinalis. Aust Vet J 64:155–158
Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704
Guo A (2015) The complete mitochondrial genome of Anoplocephala perfoliata, the first representative for the family Anoplocephalidae. Parasit Vector 8:549
Hall MJR, Wall R (1995) Myiasis of human and domestic animals. Adv Parasitol 35:257–334
Jabbar A, Mohandas N, Gasser RB (2014) Characterisation of the mitochondrial genome of Parafilaroides normani (lungworm) of Arctocephalus pusillus doriferus (Australian fur seal). Parasitol Res 113:3049–3055
Katoh K, Standley DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30:772–780
Kutty SN, Pape T, Wiegmann BM, Meier R (2010) Molecular phylogeny of the Calyptratae (Diptera: Cyclorrhapha) with an emphasis on the superfamily Oestroidea and the position of Mystacinobiidae and McAlpine’s fly. Syst Entomol 35:614–635
Laslett D, Canback B (2008) Arwen: a program to detect tRNA genes in metazoan mitochondrial nucleotide sequences. Bioinformatics 24:172–175
Lewis DL, Farr CL, Kaguni LS (1995) Drosophila melanogaster mitochondrial DNA: completion of the nucleotide sequence and evolutionary comparisons. Insect Mol Biol 4:263–278
Li J, Chen F, Sugiyama H, Blair D, Lin RQ, Zhu XQ (2015) A specific indel marker for the Philippines Schistosoma japonicum revealed by analysis of mitochondrial genome sequences. Parasitol Res 114:2697–2704
Liu GH, Gasser RB, Young ND, Song HQ, Ai L, Zhu XQ (2014) Complete mitochondrial genomes of the ‘intermediate form’ of Fasciola and Fasciola gigantica, and their comparison with F. hepatica. Parasit Vector 7:150
Liu GH, Tian SQ, Cui P, Fang SF, Wang CR, Zhu XQ (2015a) The complete mitochondrial genomes of five Eimeria species infecting domestic rabbits. Exp Parasitol 159:67–71
Liu GH, Shao R, Cai XQ, Li WW, Zhu XQ (2015b) Gnathostoma spinigerum mitochondrial genome sequence: a novel gene arrangement and its phylogenetic position within the Class Chromadorea. Sci Rep 5:12691
Liu GH, Li S, Zou FC, Wang CR, Zhu XQ (2016) The complete mitochondrial genome of rabbit pinworm Passalurus ambiguus: genome characterization and phylogenetic analysis. Parasitol Res 115:423–429
Marinho MA, Junqueira AC, Paulo DF, Esposito MC, Villet MH, Azeredo-Espin AM (2012) Molecular phylogenetics of Oestroidea (Diptera: Calyptratae) with emphasis on Calliphoridae: insights into the inter-familial relationships and additional evidence for paraphyly among blowflies. Mol Phylogenet Evol 65:840–854
Mitchell SE, Cockburn AF, Seawright JA (1993) The mitochondrial genome of Anopheles quadrimaculatus species A: complete nucleotide sequence and gene organization. Genome 36:1058–1073
Otranto D, Traversa D, Milillo P, De Luca F, Stevens J (2005) Utility of mitochondrial and ribosomal genes for differentiation and phylogenesis of species of gastrointestinal bot flies. J Econ Entomol 98:2235–2245
Pawlas-Opiela M, Wojciech Ł, Sołtysiak Z, Otranto D, Ugorski M (2010) Molecular comparison of Gasterophilus intestinalis and Gasterophilus nasalis from two distinct areas of Poland and Italy based on cox1 sequence analysis. Vet Parasitol 169:219–221
Peng GZ, Liu S, Liu B, Zhu L (2011) The prevention measures of horses myiasis. Chin Abstracts Ani Husbandry Vet Med 5:99–100, in Chinese
Principato M (1988) Classification of the main macroscopic lesions produced by larvae of Gasterophilus spp. (Diptera: Gasterophilidae) in free-ranging horses in Umbria. Cornell Vet 78:43–52
Roelfstra L, Vlimant M, Betschart B, Pfister K, Diehl PA (2010) Light and electron microscopy studies of the midgut and salivary glands of second and third instars of the horse stomach bot, Gasterophilus intestinalis. Med Vet Entomol 24:236–249
Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574
Sandin A, Skidell J, Haggstrom J, Girma K, Nilsson G (1999) Post-mortem findings of gastric ulcers in Swedish horses up to one year of age: a retrospective study 1924–1996. Acta Vet Scand 40:109–120
Sequeira JL, Tostes RA, Oliveira-Sequeira TC (2001) Prevalence and macro- and microscopic lesions produced by Gasterophilus nasalis (Diptera: Oestridae) in the Botucatu Region, SP, Brazil. Vet Parasitol 102:261–266
Spanos L, Koutroumbas G, Kotsyfakis M, Louis C (2000) The mitochondrial genome of the Mediterranean fruit fly, Ceratitis capitata. Insect Mol Biol 9:139–144
Sperling FA, Anderson GS, Hickey DA (1994) A DNA-based approach to the identification of insect species used for postmortem interval estimation. J Forensic Sci 39:418–427
Talavera G, Castresana J (2007) Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Syst Biol 56:564–577
Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA 5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739
Tao M, You CP, Zhao RR, Liu SJ, Zhang ZH, Zhang C, Liu Y (2014) Animal mitochondria: evolution, function, and disease. Curr Mol Med 14:115–124
Waddell AH (1972) The pathogenicity of Gasterophilus intestinalis larvae in the stomach of the horse. Aust Vet J 48:332–335
Wambwa EN, Ogara WO, Mudakha D (2004) A comparative study of gastrointestinal parasites between ranched and free ranging Burchell’s zebra (Equus burchelli antiquorum) in Isiolo district, Kenya. J Vet Sci 3:215–220
Weigl S, Testini G, Parisi A, Dantas-Torres F, Traversa D, Colwell DD, Otranto D (2010) The mitochondrial genome of the common cattle grub, Hypoderma lineatum. Med Vet Entomol 24:329–335
Wells JD, Sperling FAH (1999) Molecular phylogenetics of Chrysomya albiceps and Chrysomya rufifacies (Diptera: Calliphoridae). Med Vet Entomol 36:222–226
Wolstenholme DR (1992) Animal mitochondrial DNA, structure and evolution. Int Rev Cytol 141:173–216
Zhao Z, Su TJ, Chesters D, Wang SD, Ho SY, Zhu CD, Chen XL, Zhang CT (2013) The mitochondrial genome of Elodia flavipalpis Aldrich (Diptera: Tachinidae) and the evolutionary timescale of Tachinid flies. PLoS One 8:e61814
Acknowledgments
This work was supported by the International Science and Technology Cooperation Program of China (Grant No. 2013DFA31840) and the Science Fund for Creative Research Groups of Gansu Province (Grant No. 1210RJIA006) to XQZ.
Author information
Authors and Affiliations
Corresponding authors
Rights and permissions
About this article
Cite this article
Gao, DZ., Liu, GH., Song, HQ. et al. The complete mitochondrial genome of Gasterophilus intestinalis, the first representative of the family Gasterophilidae. Parasitol Res 115, 2573–2579 (2016). https://doi.org/10.1007/s00436-016-5002-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00436-016-5002-9