Hostname: page-component-55f67697df-zh294 Total loading time: 0 Render date: 2025-05-09T16:26:11.787Z Has data issue: false hasContentIssue false

The complete mitochondrial genome of Brachytarsina amboinensis (Diptera: Hippoboscoidea: Streblidae) provides new insights into phylogenetic relationships of Hippoboscoidea

Published online by Cambridge University Press:  18 December 2024

Jinting Yang
Affiliation:
Yunnan Provincial Key Laboratory for Zoonosis Control and Prevention, Institute of Pathogens and Vectors, Dali University, Dali, Yunnan, China
Wang Yujuan
Affiliation:
Jilin Provincial Key Laboratory of Animal Resource Conservation and Utilization, Northeast Normal University, Changchun, China
Huijuan Yang
Affiliation:
Department of Pathogen Biology, Institute of Tropical Medicine, School of Public Health, Southern Medical University, Guangzhou, China
Xiaobin Huang*
Affiliation:
Yunnan Provincial Key Laboratory for Zoonosis Control and Prevention, Institute of Pathogens and Vectors, Dali University, Dali, Yunnan, China
*
Corresponding author: Xiaobin Huang; Email: [email protected]

Abstract

The family Streblidae is a significant grouping of dipteran insects within the superfamily Hippoboscoidea, which parasitizes the body surface of bats. With the global spread of bat-related pathogens in recent years, Streblidae has gained increasing attention due to its potential for pathogen transmission. A sample of Brachytarsina amboinensis was sequenced on the B. amboinensis were obtained, compared with available Streblidae mitogenomes, and the phylogeny of Hippoboscoidea was reconstructed. The results indicate that the mitochondrial genome of B. amboinensis exhibits a relatively high degree of conservation, with an identical gene count, arrangement, and orientation as the ancestral insect's genome. Base composition analysis revealed a strong bias towards A and T in the base composition. Selection pressure analysis indicated strong purifying selection acting on cox1. Pairwise genetic distance analysis showed that cox1 evolved at a relatively slow rate. Regarding phylogenetic relationships, the constructed phylogenetic trees using Bayesian inference and Maximum Likelihood methods supported the monophyly of the Hippoboscoidea, Glossinidae, Hippoboscidae, and Nycteribiidae clades, with high nodal support values. Our research confirmed the paraphyly of the families Streblidae. In the familial relations between Nycteribiidae and Streblidae, New World Streblidae share a closer kinship with Nycteribiidae. This contrasts with prior findings which indicated that Old World Streblidae share a closer kinship with Nycteribiidae. This study not only enhances the molecular database for bat flies but also provides a valuable reference for the identification and phylogenetic analysis of Streblidae.

Type
Research Paper
Copyright
Copyright © The Author(s), 2024. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Article purchase

Temporarily unavailable

References

Alberfkani, MI, Albarwary, AJ, Jaafar, GM, Zubair, AI and Abdullah, RY (2022) Molecular characterization and phylogenetic analysis of cox1 and ITS 1 gene fragments of Moniezia species isolated from sheep. Pakistan Veterinary Journal 42, 566570.CrossRefGoogle Scholar
Beard, C, Hamm, DM and Collins, F (1993) The mitochondrial genome of the mosquito Anopheles gambiae: DNA sequence, genome organization, and comparisons with mitochondrial sequences of other insects. Insect Molecular Biology 2, 103124.CrossRefGoogle ScholarPubMed
Boore, JL (1999) Animal mitochondrial genomes. Nucleic Acids Research 27, 17671780.CrossRefGoogle ScholarPubMed
Briscoe, AG, Sivell, D and Harbach, RE (2017) The complete mitochondrial genome of Dixella aestivalis (Diptera: Nematocera: Dixidae). Mitochondrial DNA Part A 28, 8384.CrossRefGoogle ScholarPubMed
Cameron, SL, Lambkin, CL, Barker, SC and Whiting, MF (2007) A mitochondrial genome phylogeny of Diptera: whole genome sequence data accurately resolve relationships over broad timescales with high precision. Systematic Entomology 32, 4059.CrossRefGoogle Scholar
Castresana, J (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Molecular Biology and Evolution 17, 540552.CrossRefGoogle ScholarPubMed
Chan, PP and Lowe, TM (2019) tRNAscan-SE: searching for tRNA genes in genomic sequences. Gene Prediction: Methods and Protocols 1962, 114.Google ScholarPubMed
Chang, H, Qiu, Z, Yuan, H, Wang, X, Li, X, Sun, H, Guo, X, Lu, Y, Feng, X and Majid, M (2020) Evolutionary rates of and selective constraints on the mitochondrial genomes of Orthoptera insects with different wing types. Molecular Phylogenetics and Evolution 145, 106734.CrossRefGoogle ScholarPubMed
Chen, W-H, Lu, G, Bork, P, Hu, S and Lercher, MJ (2016) Energy efficiency trade-offs drive nucleotide usage in transcribed regions. Nature Communications 7, 11334.CrossRefGoogle ScholarPubMed
Clary, DO and Wolstenholme, DR (1985) The mitochondrial DNA molecule of Drosophila yakuba: nucleotide sequence, gene organization, and genetic code. Journal of Molecular Evolution 22, 252271.CrossRefGoogle ScholarPubMed
Conant, GC and Wolfe, KH (2008) GenomeVx: simple web-based creation of editable circular chromosome maps. Bioinformatics 24, 861862.CrossRefGoogle ScholarPubMed
Crozier, RH and Crozier, YC (1993) The mitochondrial genome of the honeybee Apis mellifera: complete sequence and genome organization. Genetics 133, 97117.CrossRefGoogle ScholarPubMed
da Silva, SG, Ferreira, FF, Hrycyna, G, Eriksson, A, Graciolli, G and Canale, GR (2023) Determinants of the composition of ectoparasitic flies of bats (Diptera: Streblidae, Nycteribiidae) in the Amazon and Cerrado landscape scales and ecotonal areas. Parasitology Research 122, 18511861.CrossRefGoogle ScholarPubMed
Dick, CW, Graciolli, G and Guerrero, R (2016) Family streblidae. Zootaxa 4122, 784802.CrossRefGoogle ScholarPubMed
Dierckxsens, N, Mardulyn, P and Smits, G (2017) NOVOPlasty: de novo assembly of organelle genomes from whole genome data. Nucleic Acids Research 45, e18.Google ScholarPubMed
Dittmar, K, Porter, ML, Murray, S and Whiting, MF (2006) Molecular phylogenetic analysis of nycteribiid and streblid bat flies (Diptera: Brachycera, Calyptratae): implications for host associations and phylogeographic origins. Molecular Phylogenetics and Evolution 38, 155170.CrossRefGoogle ScholarPubMed
Donath, A, Jühling, F, Al-Arab, M, Bernhart, SH, Reinhardt, F, Stadler, PF, Middendorf, M and Bernt, M (2019) Improved annotation of protein-coding genes boundaries in metazoan mitochondrial genomes. Nucleic Acids Research 47, 1054310552.CrossRefGoogle ScholarPubMed
Han, HJ, Li, ZM, Li, X, Liu, JX, Peng, QM, Wang, R, Gu, XL, Jiang, Y, Zhou, CM and Li, D (2022) Bats and their ectoparasites (Nycteribiidae and Spinturnicidae) carry diverse novel Bartonella genotypes, China. Transboundary and Emerging Diseases 69, e845e858.CrossRefGoogle ScholarPubMed
Hennig, W (1971) Neue untersuchungen ueber die familien der Diptera Schizophora (Diptera: Cyclorrhapha). Stuttgart: The Germany: Staatliches Museum für Naturkunde.Google Scholar
Hurst, LD (2002) The Ka/Ks ratio: diagnosing the form of sequence evolution. TRENDS in Genetics 18, 486487.CrossRefGoogle ScholarPubMed
Kalyaanamoorthy, S, Minh, BQ, Wong, TK, Von Haeseler, A and Jermiin, LS (2017) ModelFinder: fast model selection for accurate phylogenetic estimates. Nature Methods 14, 587589.CrossRefGoogle ScholarPubMed
Kono, N, Tomita, M and Arakawa, K (2018) Accelerated laboratory evolution reveals the influence of replication on the GC skew in Escherichia coli. Genome Biology and Evolution 10, 31103117.CrossRefGoogle Scholar
Kuang, G, Xu, Z, Wang, J, Gao, Z, Yang, W, Wu, W, Liang, G, Shi, M and Feng, Y (2023) Nelson bay reovirus isolated from bats and blood-sucking arthropods collected in Yunnan Province, China. Microbiology Spectrum 11, e05122.CrossRefGoogle ScholarPubMed
Kutty, SN, Pape, T, Wiegmann, BM and 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. Systematic Entomology 35, 614635.CrossRefGoogle Scholar
Letko, M, Seifert, SN, Olival, KJ, Plowright, RK and Munster, VJ (2020) Bat-borne virus diversity, spillover and emergence. Nature Reviews Microbiology 18, 461471.CrossRefGoogle ScholarPubMed
Li, XY, Yan, LP, Pape, T, Gao, YY and Zhang, D (2020) Evolutionary insights into bot flies (Insecta: Diptera: Oestridae) from comparative analysis of the mitochondrial genomes. International Journal of Biological Macromolecules 149, 371380.CrossRefGoogle ScholarPubMed
Li, X, Wang, L and Yang, D (2022) The complete mitochondrial genome of Ornithomya biloba (Diptera, Hippoboscidae). Mitochondrial DNA Part B 7, 856858.CrossRefGoogle ScholarPubMed
Liu, Z-Q, Kuermanali, N, Li, Z, Chen, S-J, Wang, Y-Z, Tao, H and Chen, C-F (2017) The complete mitochondrial genome of the parasitic sheep ked Melophagus ovinus (Diptera: Hippoboscidae). Mitochondrial DNA Part B 2, 432434.CrossRefGoogle ScholarPubMed
Ma, XX, Wang, FF, Wu, TT, Li, Y, Sun, XJ, Wang, CR and Chang, QC (2022) First description of the mitogenome and phylogeny: Aedes vexans and Ochlerotatus caspius of the Tribe Aedini (Diptera: Culicidae). Infection, Genetics and Evolution 102, 105311.CrossRefGoogle ScholarPubMed
McAlpine, J (1989) Phylogeny and classification of the Muscomorpha. Manual of Nearctic Diptera 3, 13971518.Google Scholar
Minh, BQ, Schmidt, HA, Chernomor, O, Schrempf, D, Woodhams, MD, Von Haeseler, A and Lanfear, R (2020) IQ-TREE 2: new models and efficient methods for phylogenetic inference in the genomic era. Molecular Biology and Evolution 37, 15301534.CrossRefGoogle ScholarPubMed
Nelson, L, Lambkin, CL, Batterham, P, Wallman, JF, Dowton, M, Whiting, MF, Yeates, DK and Cameron, SL (2012) Beyond barcoding: a mitochondrial genomics approach to molecular phylogenetics and diagnostics of blowflies (Diptera: Calliphoridae). Gene 511, 131142.CrossRefGoogle ScholarPubMed
Nirmala, X, Hypša, V and Žurovec, M (2001) Molecular phylogeny of Calyptratae (Diptera: Brachycera): the evolution of 18S and 16S ribosomal rDNAs in higher dipterans and their use in phylogenetic inference. Insect Molecular Biology 10, 475485.CrossRefGoogle ScholarPubMed
Ožana, S, Dolný, A and Pánek, T (2022) Nuclear copies of mitochondrial DNA as a potential problem for phylogenetic and population genetic studies of Odonata. Systematic Entomology 47, 591602.CrossRefGoogle Scholar
Petersen, FT, Meier, R, Kutty, SN and Wiegmann, BM (2007) The phylogeny and evolution of host choice in the Hippoboscoidea (Diptera) as reconstructed using four molecular markers. Molecular Phylogenetics and Evolution 45, 111122.CrossRefGoogle ScholarPubMed
Poon, ESK, Chen, G, Tsang, HY, Shek, CT, Tsui, WC, Zhao, H, Guénard, B and Sin, SYW (2023) Species richness of bat flies and their associations with host bats in a subtropical east Asian region. Parasites & Vectors 16, 115.CrossRefGoogle Scholar
Porter, ML, Lutz, H, Steck, M and Chong, RA (2022) The complete mitochondrial genomes and phylogenetic analysis of two Nycteribiidae bat flies (Diptera: Hippoboscoidea). Mitochondrial DNA Part B 7, 14861488.CrossRefGoogle ScholarPubMed
Ramírez-Martínez, MM, Bennett, AJ, Dunn, CD, Yuill, TM and Goldberg, TL (2021) Bat flies of the family streblidae (Diptera: Hippoboscoidea) host relatives of medically and agriculturally important ‘bat-associated’ viruses. Viruses 13, 860.CrossRefGoogle ScholarPubMed
Ren, L, Shang, Y, Yang, L, Shen, X, Chen, W, Wang, Y, Cai, J and Guo, Y (2019) Comparative analysis of mitochondrial genomes among four species of muscid flies (Diptera: Muscidae) and its phylogenetic implications. International Journal of Biological Macromolecules 127, 357364.CrossRefGoogle ScholarPubMed
Ronquist, F, Teslenko, M, Van Der Mark, P, Ayres, DL, Darling, A, Höhna, S, Larget, B, Liu, L, Suchard, MA and Huelsenbeck, JP (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61, 539542.CrossRefGoogle ScholarPubMed
Rozas, J, Ferrer-Mata, A, Sánchez-DelBarrio, JC, Guirao-Rico, S, Librado, P, Ramos-Onsins, SE and Sánchez-Gracia, A (2017) DnaSP 6: DNA sequence polymorphism analysis of large data sets. Molecular Biology and Evolution 34, 32993302.CrossRefGoogle ScholarPubMed
Rozewicki, J, Li, S, Amada, KM, Standley, DM and Katoh, K (2019) MAFFT-DASH: integrated protein sequence and structural alignment. Nucleic Acids Research 47, W5W10.Google ScholarPubMed
Szentiványi, T, Heintz, AC, Markotter, W, Wassef, J, Christe, P and Glaizot, O (2023) Vector-borne protozoan and bacterial pathogen occurrence and diversity in ectoparasites of the Egyptian Rousette bat. Medical and Veterinary Entomology 37, 189194.CrossRefGoogle ScholarPubMed
Tamura, K, Stecher, G and Kumar, S (2021) MEGA11: molecular evolutionary genetics analysis version 11. Molecular Biology and Evolution 38, 30223027.CrossRefGoogle ScholarPubMed
Trevisan, B, Alcantara, DM, Machado, DJ, Marques, FP and Lahr, DJ (2019) Genome skimming is a low-cost and robust strategy to assemble complete mitochondrial genomes from ethanol preserved specimens in biodiversity studies. PeerJ 7, e7543.CrossRefGoogle ScholarPubMed
Wang, D, Zhang, Y, Zhang, Z, Zhu, J and Yu, J (2010) KaKs_Calculator 2.0: a toolkit incorporating gamma-series methods and sliding window strategies. Genomics, Proteomics & Bioinformatics 8, 7780.CrossRefGoogle ScholarPubMed
Wang, M, Wang, J, Guo, Y, Zheng, Q, Nouhoum, D and Meng, F (2021) Complete mitochondrial genome of a potential vector louse fly, Lipoptena grahami (Diptera, Hippoboscidae). Mitochondrial DNA Part B 6, 17521753.CrossRefGoogle ScholarPubMed
Wang, R, Li, ZM, Peng, QM, Gu, XL, Zhou, CM, Xiao, X, Han, HJ and Yu, XJ (2023) High prevalence and genetic diversity of hemoplasmas in bats and bat ectoparasites from China. One Health 16, 100498.CrossRefGoogle ScholarPubMed
Wenzel, RL (1976) The streblid batflies of Venezuela (Diptera: Streblidae). Brigham Young University Science Bulletin, Biological Series 20, 1.Google Scholar
Yang, H, Chen, T and Dong, W (2023 a) Comparative analysis of the mitochondrial genome of Dermacentor steini from different regions in China. Parasitology 150, 195205.CrossRefGoogle ScholarPubMed
Yang, JT, Huang, XB, Wang, YJ, Yang, HJ, Zhang, XZ and Zheng, XY (2023 b) Complete mitochondrial genome of Penicillidia jenynsii (Diptera: Hippoboscoidea: Nycteribiidae) and phylogenetic relationship. Parasitology 150, 623630.CrossRefGoogle ScholarPubMed
Yang, JT, Huang, XB, Wang, YJ, Yang, HJ, Zhang, XZ and Zheng, XY (2023 c) Complete mitogenome of Nycteribia allotopa Speiser, 1901 (Diptera, Hippoboscoidea, Nycteribiidae) and comparative analysis of mitochondrial genomes of Nycteribiidae. Parasitology International 96, 102769.CrossRefGoogle ScholarPubMed
Yang, JT, Huang, XB, Wang, YJ, Yang, HJ, Zhang, XZ and Zheng, XY (2023 d) The complete mitochondrial genome of Nycteribia parvula Speiser, 1901 (Diptera, Nycteribiidae). Mitochondrial DNA Part B 8, 276280.CrossRefGoogle ScholarPubMed
Yang, JT, Wang, YJ, Yang, HJ, Zhang, XZ, Zheng, XY and Huang, XB (2024) Infection status and molecular detection of pathogens carried by ectoparasites of Miniopterus fuliginosus bats in Yunnan, China. Parasitology International 98, 102823.CrossRefGoogle ScholarPubMed
Zhang, DX and Hewitt, GM (1997) Insect mitochondrial control region: a review of its structure, evolution and usefulness in evolutionary studies. Biochemical Systematics and Ecology 25, 99120.CrossRefGoogle Scholar
Zhang, D, Gao, F, Jakovlić, I, Zou, H, Zhang, J, Li, WX and Wang, GT (2020) PhyloSuite: an integrated and scalable desktop platform for streamlined molecular sequence data management and evolutionary phylogenetics studies. Molecular Ecology Resources 20, 348355.CrossRefGoogle ScholarPubMed
Zhang, X, Huang, X, Wang, Y, Yang, H, Yang, J and Zheng, X (2023) The complete mitochondrial genome of Phthiridium szechuanum (Nycteribiidae, Diptera). Mitochondrial DNA Part B 8, 211214.CrossRefGoogle ScholarPubMed
Ziegler, J (2003) Ordnung Diptera, Zweiflügler (Fliegen und Mücken). Lehrbuch der Speziellen Zoologie. Begründet von Alfred Kaestner 2, 756860.Google Scholar
Supplementary material: File

Yang et al. supplementary material

Yang et al. supplementary material
Download Yang et al. supplementary material(File)
File 12.3 KB