Abstract
Hypoderma bovis (H. bovis) and Hypoderma sinense (H. sinense) are insects that cause hypodermosis in yaks and Bos taurus. Hypodermosis is a severe skin condition that not only impairs the development of local animal husbandry but also poses threats to human health as a zoonosis. The Qinghai-Tibetan Plateau (QTP) is known as the “Roof of the World.” Its unique geographical environment and climate conditions have supported the growth of a wide range of mammals, providing favorable conditions for Hypoderma spp. to complete their life cycles. In this study, the whole mitochondrial genomes of H. bovis and H. sinense collected from the QTP were sequenced and phylogenetically analyzed. We found that the whole genomes of H. bovis and H. sinense are 16,283 bp and 16,300 bp in length, respectively. Both the H. bovis and H. sinense genomes have 37 mitochondrial genes, which include two rRNA genes (16S rRNA and 12S rRNA), 22 tRNA genes, the control region (D-loop region), the light chain replication initiation region, and 13 protein-coding genes (PCGs). The phylogenetic tree generated based on the 13 PCGs revealed close phylogenetic relationships between H. sinense, H. bovis, and Hypoderma lineatum. A similar result was also found in our phylogenetic analysis based on 18S rRNA and 28S rRNA. However, analysis of cytochrome oxidase subunit I (COI) showed cluster of H. bovis, H. sinense, and Cuterebra spp. on the same branch, all belonging to Oestridae. The differentiation time generated based on 13 PCGs indicates that H. bovis and H. sinense differentiated and formed ~4.69 million years ago (Mya) and ~4.06 Mya, respectively. This timing coincides with the differentiation and appearance of yak and Bos taurus in the Pliocene (~4.7 Mya), indicating that the parasites and mammals diverged in close temporal proximity. Of note, this period also witnessed a rapid uplift of the QTP, causing significant climate and environmental changes. Thus, we conjecture that the differentiation of Hypoderma spp. is potentially related to the differentiation of their host species, as well as climate changes caused by the uplift of the QTP. Overall, our study can provide valuable data to support further studies on the phylogeny and differentiation of Hypoderma spp. on the QTP.
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References
Ahmed H, Afzal MS, Mobeen M, Simsek S (2016) An overview on different aspects of hypodermosis: current status and future prospects. Acta Trop 162:35–45. https://doi.org/10.1016/j.actatropica.2016.05.016
Ahmed H, Simsek S, Saki CE, Kesik HK, Kilinc SG (2017) Molecular characterization of Hypoderma spp. in domestic ruminants from Turkey and Pakistan. J Parasitol 103:303–308. https://doi.org/10.1645/16-185
Anderson JR (2006) Adult biology. In: The Oestrid Flies: biology, host-parasite relationships, impact and management, CABI Books, pp 140–166. https://doi.org/10.1079/9780851996844.0140
Antonelli A, Sanmartín I (2011) Why are there so many plant species in the Neotropics? Taxon 60:403–414. https://doi.org/10.1002/tax.602010
Ao H, Rohling EJ, Zhang R, Roberts AP, Holbourn AE, Ladant J-B, Dupont-Nivet G, Kuhnt W, Zhang P, Wu F, Dekkers MJ, Liu Q, Liu Z, Xu Y, Poulsen CJ, Licht A, Sun Q, Chiang JCH, Liu X et al (2021) Global warming-induced Asian hydrological climate transition across the Miocene-Pliocene boundary. Nat Commun 12:6935. https://doi.org/10.1038/s41467-021-27054-5
Badgley C, Barry JC, Morgan ME, Nelson SV, Behrensmeyer AK, Cerling TE, Pilbeam D (2008) Ecological changes in the Miocene mammalian record show impact of prolonged climatic forcing. Proc Natl Acad Sci USA 105:12145–12149. https://doi.org/10.1073/pnas.0805592105
Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, Kulikov AS, Lesin VM, Nikolenko SI, Pham S, Prjibelski AD, Pyshkin AV, Sirotkin AV, Vyahhi N, Tesler G, Alekseyev MA, Pevzner PA (2012) SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 19:455–477. https://doi.org/10.1089/cmb.2012.0021
Barry JC, Morgan ME, Flynn LJ, Pilbeam D, Behrensmeyer AK, Raza SM, Khan IA, Badgley C, Hicks J, Kelley J (2002) Faunal and environmental change in the Late Miocene Siwaliks of Northern Pakistan. Paleobiology 28:1–71. https://doi.org/10.1666/0094-8373(2002)28[1:FAECIT]2.0.CO;2
Behura SK, Severson DW (2013) Codon usage bias: causative factors, quantification methods and genome-wide patterns: with emphasis on insect genomes. Biol Rev Camb Philos Soc 88:49–61. https://doi.org/10.1111/j.1469-185X.2012.00242.x
Benton MJ (2009) The Red Queen and the Court Jester: species diversity and the role of biotic and abiotic factors through time. Science 323:728–732. https://doi.org/10.1126/science.1157719
Bernt M, Donath A, Jühling F, Externbrink F, Florentz C, Fritzsch G, Pütz J, Middendorf M, Stadler PF (2013) MITOS: improved de novo metazoan mitochondrial genome annotation. Mol Phylogenet Evol 69:313–319. https://doi.org/10.1016/j.ympev.2012.08.023
Bibi F (2013) A multi-calibrated mitochondrial phylogeny of extant Bovidae (Artiodactyla, Ruminantia) and the importance of the fossil record to systematics. BMC Evol Biol 13:166. https://doi.org/10.1186/1471-2148-13-166
Bouckaert R, Heled J, Kühnert D, Vaughan T, Wu C-H, Xie D, Suchard MA, Rambaut A, Drummond AJ (2014) BEAST 2: a software platform for Bayesian evolutionary analysis. PLoS Comput Biol 10:e1003537. https://doi.org/10.1371/journal.pcbi.1003537
Boulard C (2002) Durably controlling bovine hypodermosis. Vet Res 33:455–464. https://doi.org/10.1051/vetres:2002032
Cai T, Shao S, Kennedy JD, Alström P, Moyle RG, Qu Y et al (2020) The role of evolutionary time, diversification rates and dispersal in determining the global diversity of a large radiation of passerine birds. J Biogeogr 47(7):1612–1625. https://doi.org/10.1111/jbi.13823
Capella-Gutiérrez S, Silla-Martínez JM, Gabaldón T (2009) trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 25:1972–1973. https://doi.org/10.1093/bioinformatics/btp348
Chalwatzis N, Hauf J, Van De Peer Y, Kinzelbach R, Zimmermann FK (1996) 18S Ribosomal Rna genes of insects: primary structure of the genes and molecular phylogeny of the holometabola. Ann Entomol Soc Am 89:788–803. https://doi.org/10.1093/aesa/89.6.788
Che J, Zhou W-W, Hu J-S, Yan F, Papenfuss TJ, Wake DB, Zhang Y-P (2010) Spiny frogs (Paini) illuminate the history of the Himalayan region and Southeast Asia. Proc Natl Acad Sci USA 107:13765–13770. https://doi.org/10.1073/pnas.1008415107
Chen L, Chen PY, Xue XF, Hua HQ, Li YX, Zhang F, Wei SJ (2018a) Extensive gene rearrangements in the mitochondrial genomes of two egg parasitoids, Trichogramma japonicum and Trichogramma ostriniae (Hymenoptera: Chalcidoidea: Trichogrammatidae). Sci Rep 8(1):7034. https://doi.org/10.1038/s41598-018-25338-3
Chen S, Zhou Y, Chen Y, Gu J (2018b) fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics 34:i884–i890. https://doi.org/10.1093/bioinformatics/bty560
Couzens AMC, Prideaux GJ (2018) Rapid Pliocene adaptive radiation of modern kangaroos. Science (New York, N.Y.) 362(6410):72–75. https://doi.org/10.1126/science.aas8788
Dai L, Qian C, Zhang C, Wang L, Wei G, Li J, Zhu B, Liu C (2015) Characterization of the complete mitochondrial genome of Cerura menciana and comparison with other Lepidopteran insects. PloS One 10(8):e0132951. https://doi.org/10.1371/journal.pone.0132951
de Meeûs T, Michalakis Y, Renaud F (1998) Santa rosalia revisited: or why are there so many kinds of parasites in ;the garden of earthly delights’? Parasitol Today 14:10–13. https://doi.org/10.1016/s0169-4758(97)01163-0
Favre A, Päckert M, Pauls SU, Jähnig SC, Uhl D, Michalak I, Muellner-Riehl AN (2015) The role of the uplift of the Qinghai-Tibetan Plateau for the evolution of Tibetan biotas. Biol Rev Camb Philos Soc 90:236–253. https://doi.org/10.1111/brv.12107
Fjeldså J, Bowie RCK, Rahbek C (2012) The role of mountain ranges in the diversification of birds. Ann Rev Ecol Evol Syst 43:249–265. https://doi.org/10.1146/annurev-ecolsys-102710-145113
Fu Y, Li W, Duo H, Guo Z-H, Li Y, Zhang Y-M (2016) Genetic diversity and population genetics of the warble flies Hypoderma bovis and H. sinense in Qinghai Province, China. Parasit Vectors 9:145. https://doi.org/10.1186/s13071-016-1416-6
Grunin KJ (1964) Die Fliegen der Palaearktischen Region. Familie 64 b: Hypodermatidae. Schweizerbart Science Publishers, Stuttgart
Harris N (2006) The elevation history of the Tibetan Plateau and its implications for the Asian monsoon. Palaeogeogr Palaeoclimatol Palaeoecol Monsoon Tectonics of Asia 241:4–15. https://doi.org/10.1016/j.palaeo.2006.07.009
Hassan M, Khan MN, Abubakar M, Waheed HM, Iqbal Z, Hussain M (2010) Bovine hypodermosis--a global aspect. Trop Anim Health Prod 42:1615–1625. https://doi.org/10.1007/s11250-010-9634-y
Hassanin A, Ropiquet A (2005) Molecular evidence for the polyphyly of the genus Hemitragus (Mammalia, Bovidae). Mol Phylogenet Evol 36(1):154–168. https://doi.org/10.1016/j.ympev.2005.01.002
Hebert PDN, Gregory TR (2005) The promise of DNA barcoding for taxonomy. Syst Biol 54:852–859. https://doi.org/10.1080/10635150500354886
Heled J, Drummond AJ (2015) Calibrated birth-death phylogenetic time-tree priors for Bayesian inference. Syst Biol 64:369–383. https://doi.org/10.1093/sysbio/syu089
Huyse T, Poulin R, Théron A (2005) Speciation in parasites: a population genetics approach. Trends Parasitol 21:469–475. https://doi.org/10.1016/j.pt.2005.08.009
Jacques FM, Guo SX, Su T, Xing YW, Huang YJ, Liu YSC et al (2011) Quantitative reconstruction of the Late Miocene monsoon climates of southwest China: a case study of the Lincang flora from Yunnan Province. Palaeogeogr Palaeoclimatol Palaeoecol 304(3–4):318–327. https://doi.org/10.1016/j.palaeo.2010.04.014
Kalyaanamoorthy S, Minh BQ, Wong TKF, von Haeseler A, Jermiin LS (2017) ModelFinder: fast model selection for accurate phylogenetic estimates. Nat Methods 14:587–589. https://doi.org/10.1038/nmeth.4285
Katoh K, Standley DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30:772–780. https://doi.org/10.1093/molbev/mst010
Larson DE, Zahradka P, Sells BH (1991) Control points in eucaryotic ribosome biogenesis. Biochem Cell Biol 69:5–22. https://doi.org/10.1139/o91-002
Li W, Ano H, Jin J, Nasu T, Ma Y, Zhu X, Makimura S (2004) Cytochrome oxidase I gene sequence of Hypoderma sinense infecting yaks in the Qinghai-Tibet high plateau of China. Vet Parasitol 124:131–135. https://doi.org/10.1016/j.vetpar.2004.03.022
Li W, Fu Y, Duo H, Guo Z, Shen X, Huang F, Feng K, Dang Z, Mao P, Wang F, Nasu T, Nonaka N (2014) An epidemiological study of Hypoderma infection and control using ivermectin in yaks in Qinghai Province, China. J Vet Med Sci 76:183–188. https://doi.org/10.1292/jvms.13-0299
Lin C-P, Danforth BN (2004) How do insect nuclear and mitochondrial gene substitution patterns differ? Insights from Bayesian analyses of combined datasets. Mol Phylogenet Evol 30:686–702. https://doi.org/10.1016/S1055-7903(03)00241-0
Liu JS, Schardl CL (1994) A conserved sequence in internal transcribed spacer 1 of plant nuclear rRNA genes. Plant Mol Biol 26(2):775–778. https://doi.org/10.1007/BF00013763
Liu Z, Yao Z, Wang R, Yu G (2020) Estimation of the Qinghai-Tibetan Plateau runoff and its contribution to large Asian rivers. Sci Total Environ 749:141570. https://doi.org/10.1016/j.scitotenv.2020.141570
Miao Y, Herrmann M, Wu F, Yan X, Yang S (2012) What controlled Mid–Late Miocene long-term aridification in Central Asia? — Global cooling or Tibetan Plateau uplift: a review. Earth-Sci Rev 112:155–172. https://doi.org/10.1016/j.earscirev.2012.02.003
Mulch A, Chamberlain CP (2006) Earth science: the rise and growth of Tibet. Nature 439:670–671. https://doi.org/10.1038/439670a
Nagahama T, Sato H, Shimazu M, Sugiyama J (1995) Phylogenetic divergence of the entomophthoralean fungi: evidence from nuclear 18S ribosomal RNA gene sequences. Mycologia 87:203–209. https://doi.org/10.1080/00275514.1995.12026522
Nguyen L-T, Schmidt HA, von Haeseler A, Minh BQ (2015) IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol 32:268–274. https://doi.org/10.1093/molbev/msu300
Nirmala X, Hypsa V, Zurovec 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 Mol Biol 10(5):475–485. https://doi.org/10.1046/j.0962-1075.2001.00286.x
Otranto D, Colwell DD, Traversa D, Stevens JR (2003) Species identification of Hypoderma affecting domestic and wild ruminants by morphological and molecular characterization. Med Vet Entomol 17:316–325. https://doi.org/10.1046/j.1365-2915.2003.00446.x
Otranto D, Colwell DD, Pape T (2005a) Hypoderma sinense: solving a century-old enigma. Med Vet Entomol 19:315–321. https://doi.org/10.1111/j.1365-2915.2005.00576.x
Otranto D, Traversa D, Milillo P, De Luca F, Stevens J (2005b) Utility of mitochondrial and ribosomal genes for differentiation and phylogenesis of species of gastrointestinal bot flies. J Econ Entomol 98(6):2235–2245. https://doi.org/10.1093/jee/98.6.2235
Päckert M, Favre A, Schnitzler J, Martens J, Sun YH, Tietze DT et al (2020) “Into and Out of” the Qinghai-Tibet Plateau and the Himalayas: centers of origin and diversification across five clades of Eurasian montane and alpine passerine birds. Ecol Evol 10(17):9283–9300. https://doi.org/10.1002/ece3.6615
Parvathy ST, Udayasuriyan V, Bhadana V (2022) Codon usage bias. Mol Biol Rep 49:539–565. https://doi.org/10.1007/s11033-021-06749-4
Paul R (2002) Species concepts versus species criteria. Trends Parasitol 18:439–440; author reply 440. https://doi.org/10.1016/s1471-4922(02)02319-x
Qiang X, An Z, Song Y, Chang H, Sun Y, Liu W et al (2011) New eolian red clay sequence on the western Chinese Loess Plateau linked to onset of Asian desertification about 25 Ma ago. Sci China Earth Sci 54:136–144. https://doi.org/10.1007/s11430-010-4126-5
Rakhshandehroo E, Razavi SM, Farzaneh R, Esmailnejad A, Asadpour M, Shams S (2019) Phylogenetic analysis of goat warble fly (Przhevalskiana silenus) based on mitochondrial COI gene. J Parasit Dis 43:304–307. https://doi.org/10.1007/s12639-019-01093-8
Shi ZG, Liu XD, Sha YY (2015) Did northern Tibetan Plateau uplift during Pliocene? A modeling test. J Earth Environ 6:67–80 (in Chinese)
Smith VS (2005) DNA barcoding: perspectives from a “Partnerships for Enhancing Expertise in Taxonomy” (PEET) debate. Syst Biol 54:841–844. https://doi.org/10.1080/10635150500354894
Sniderman JM, Woodhead JD, Hellstrom J, Jordan GJ, Drysdale RN, Tyler JJ, Porch N (2016) Pliocene reversal of late Neogene aridification. Proc Natl Acad Sci USA 113(8):1999–2004. https://doi.org/10.1073/pnas.1520188113
Stevens JR, Wallman JF (2006) The evolution of myiasis in humans and other animals in the Old and New Worlds (part I): phylogenetic analyses. Trends Parasitol 22(3):129–136. https://doi.org/10.1016/j.pt.2006.01.008
Sun X, Wang P (2005) How old is the Asian monsoon system?—Palaeobotanical records from China. Palaeogeogr Palaeoclimatol Palaeoecol 222:181–222. https://doi.org/10.1016/j.palaeo.2005.03.005
Suzán G, Marcé E, Giermakowski JT, Armién B, Pascale J, Mills J, Ceballos G, Gómez A, Aguirre AA, Salazar-Bravo J, Armién A, Parmenter R, Yates T (2008) The effect of habitat fragmentation and species diversity loss on hantavirus prevalence in Panama. Ann N Y Acad Sci 1149:80–83. https://doi.org/10.1196/annals.1428.063
Tamura K, Stecher G, Kumar S (2021) MEGA11: Molecular Evolutionary Genetics Analysis Version 11. Mol Biol Evol 38:3022–3027. https://doi.org/10.1093/molbev/msab120
Timsit Y, Sergeant-Perthuis G, Bennequin D (2021) Evolution of ribosomal protein network architectures. Sci Rep 11(1):625. https://doi.org/10.1038/s41598-020-80194-4
Toljagic O, Voje KL, Matschiner M, Liow LH, Hansen TF (2018) Millions of years behind: slow adaptation of ruminants to grasslands. Syst Biol 67:145–157. https://doi.org/10.1093/sysbio/syx059
Turelli M, Barton NH, Coyne JA (2001) Theory and speciation. Trends Ecol Evol 16:330–343. https://doi.org/10.1016/s0169-5347(01)02177-2
Whiting MF, Carpenter JC, Wheeler QD, Wheeler WC (1997) The Strepsiptera problem: phylogeny of the holometabolous insect orders inferred from 18S and 28S ribosomal DNA sequences and morphology. Syst Biol 46:1–68. https://doi.org/10.1093/sysbio/46.1.1
Will KW, Mishler BD, Wheeler QD (2005) The perils of DNA barcoding and the need for integrative taxonomy. Syst Biol 54:844–851. https://doi.org/10.1080/10635150500354878
Wu Y-D, Li L, Fan Y-L, Ni X-W, Ohiolei JA, Li W-H, Li J-Q, Zhang N-Z, Fu B-Q, Yan H-B, Jia W-Z (2021) Genetic evolution and implications of the mitochondrial genomes of two newly identified Taenia spp. in rodents from Qinghai-Tibet Plateau. Front Microbiol 12:647119. https://doi.org/10.3389/fmicb.2021.647119
Wu Y-D, Dai G-D, Li L, Littlewood DTJ, Ohiolei JA, Zhang L-S, Guo A-M, Wu Y-T, Ni X-W, Shumuye NA, Li W-H, Zhang N-Z, Fu B-Q, Fu Y, Yan H-B, Jia W-Z (2022) Expansion of Cyclophyllidea biodiversity in rodents of Qinghai-Tibet Plateau and the “Out of Qinghai-Tibet Plateau” hypothesis of Cyclophyllideans. Front Microbiol 13:747484. https://doi.org/10.3389/fmicb.2022.747484
Xie J, Chen Y, Cai G, Cai R, Hu Z, Wang H (2023) Tree Visualization By One Table (tvBOT): a web application for visualizing, modifying and annotating phylogenetic trees. Nucleic Acids Res 51:W587–W592. https://doi.org/10.1093/nar/gkad359
Xin ZZ, Liu Y, Zhu XY, Wang Y, Zhang HB, Zhang DZ et al (2017) Mitochondrial genomes of two Bombycoidea insects and implications for their phylogeny. Sci Rep 7(1):6544. https://doi.org/10.1038/s41598-017-06930-5
Xing Y, Ree RH (2017) Uplift-driven diversification in the Hengduan Mountains, a temperate biodiversity hotspot. Proc Natl Acad Sci USA 114(17):E3444–E3451. https://doi.org/10.1073/pnas.1616063114
Yao T, Wu F, Ding L, Sun J, Zhu L, Piao S, Deng T, Ni X, Zheng H, Ouyang H (2015) Multispherical interactions and their effects on the Tibetan Plateau’s earth system: a review of the recent researches. Natl Sci Rev 2:468–488. https://doi.org/10.1093/nsr/nwv070
Yin H, Ma M, Yuan G, Huang S, Liu Z, Luo J, Guan G (2003) Hypodermosis in China. J Anim Vet Adv 2(3):179–183
Zhang DX, Hewitt GM (1997) Assessment of the universality and utility of a set of conserved mitochondrial COI primers in insects. Insect Mol Biol 6:143–150. https://doi.org/10.1111/j.1365-2583.1997.tb00082.x
Zhang Z, Sun J (2011) Palynological evidence for Neogene environmental change in the foreland basin of the southern Tianshan range, northwestern China. Glob Planet Change 75:56–66. https://doi.org/10.1016/j.gloplacha.2010.10.006
Zhang B, Nardi F, Hull-Sanders H, Wan X, Liu Y (2014) The complete nucleotide sequence of the mitochondrial genome of Bactrocera minax (Diptera: Tephritidae). PLoS One 9:e100558. https://doi.org/10.1371/journal.pone.0100558
Zhang JF, Liu JK, Hyde KD, Ekanayaka AH, Liu ZY (2020) Morpho-phylogenetic evidence reveals new species in Rhytismataceae (Rhytismatales, Leotiomycetes, Ascomycota) from Guizhou Province, China. MycoKeys 76:81–106. https://doi.org/10.3897/mycokeys.76.58465
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This work was supported by grants from the Applied Basic Research of Qinghai Province in China (Grant No. 2021-ZJ-724) and the Open Project of State Key Laboratory of Plateau Ecology and Agriculture, Qinghai University (Grant No. 2022-ZZ-10).
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YF and ZL: conceptualization, project administration, data analysis, manuscript drafting. WKC: executing laboratory experiments and manuscript drafting. HNZ: executing laboratory experiments and data analysis. RM and HD: conceptualization, data analysis, review, and editing. XYZ, ZHG, XYS, and CJC: data analysis. All authors read and approved the final manuscript.
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Chen, W., Zhang, H., Meng, R. et al. Genome-wide phylogenetic and genetic evolutionary analyses of mitochondria in Hypoderma bovis and H. sinense on the Qinghai-Tibetan Plateau. Parasitol Res 123, 43 (2024). https://doi.org/10.1007/s00436-023-08060-6
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DOI: https://doi.org/10.1007/s00436-023-08060-6